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Running Head Auxin regulates herbivory-induced secondary metabolites 1
Correspondence Matthias Erb University of Bern Institute of Plant Sciences 2
Altenbergrain 21 3013 Bern Switzerland Tel +41 31 631 86 68 matthiaserbipsunibech 3
Research area Signaling and response 4
Plant Physiology Preview Published on August 2 2016 as DOI101104pp1600940
Copyright 2016 by the American Society of Plant Biologists
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Auxin is rapidly induced by herbivore attack and regulates a subset of systemic 5
jasmonate-dependent secondary metabolites 6
Ricardo AR Machado12 Christelle AM Robert12 Carla CM Arce123 Abigail P Ferrieri1 7
Shuqing Xu1 Guillermo H Jimenez-Aleman1 Ian T Baldwin1 and Matthias Erb12 8
9
1Max Planck Institute for Chemical Ecology Hans-Knoumlll-Str 8 07745 Jena Germany 10
2Institute of Plant Sciences University of Bern Altenbergrain 21 3013 Bern Switzerland 11
3Departamento de Entomologia Universidade Federal de Viccedilosa 36570-000 Viccedilosa MG 12
Brazil 13
14
One sentence summary Herbivory-induced auxin promotes the production of anthocyanins 15
and phenolamides 16
17
18
This work was supported by the Max Planck Society a Humboldt Postdoctoral Research 19
Fellowship (AF) the Brazilian National Council for Research CNPq Grant No 2379292012-20
0 (CA) a Marie Curie Intra European Fellowship Grant No 328935 (SX) a Marie Curie 21
Intra European Fellowship Grant No 273107 (ME) a Swiss National Foundation Fellowship 22
Grant No 140196 (CR) a European Research Council advanced Grant No 293926 (ITB) and 23
Human Frontier Science Program Grant No RGP00022012 (ITB) 24
25
26
Author for correspondence (Phone +41 31 631 8668 E-mail matthiaserbipsunibech)27
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ABSTRACT 28
Plant responses to herbivore attack are regulated by phytohormonal networks To date the 29
role of the auxin indole-3-acetic acid (IAA) in this context is not well understood We 30
quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-31
attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary 32
metabolism We found that IAA is strongly rapidly and specifically induced by herbivore 33
attack IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is 34
accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes 35
IAA accumulation starts 30-60 seconds after local induction and peaks within 5 minutes after 36
induction thereby preceding the jasmonate (JA) burst IAA accumulation does not require JA 37
signaling and spreads rapidly from the wound site to systemic tissues Complementation and 38
transport inhibition experiments reveal that IAA is required for the herbivore-specific 39
jasmonate-dependent accumulation of anthocyanins and phenolamides in the stems In 40
contrast IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool 41
diterpene glycosides in the same tissue Taken together our results uncover IAA as a rapid 42
and specific signal that regulates a subset of systemic jasmonate-dependent secondary 43
metabolites in herbivore-attacked plants 44
45
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4
INTRODUCTION 46
Plants withstand herbivore attack by specifically recognizing the attacker and mounting 47
appropriate defenses Induced defense responses are activated by hormone-mediated 48
signaling cascades (Erb et al 2012 Wu and Baldwin 2009) and jasmonates (JA) have 49
emerged as key regulators in this context (Geyter et al 2012 Howe and Jander 2008) As a 50
consequence their behavior and mode of action have been studied in great detail (Wasternack 51
and Hause 2013) Similarly other stress-related hormones such as salicylic acid abscisic 52
acid and ethylene have been shown to play important roles in the orchestration of plant 53
defenses against herbivores (Dahl et al 2007 Winz and Baldwin 2001 Thaler and Bostock 54
2004 Zhang et al 2013 Kroes et al 2014) Recent evidence also suggests that hormones 55
which have traditionally been classified as growth regulators participate in induced defense 56
responses Cytokinins for instance modulate wound-induced local and systemic defense 57
responses (Schaumlfer et al 2015) and gibberellins are involved in regulating the plantrsquos 58
investment into growth and defense (Li et al 2015 Hou et al 2010 Yang et al 2012) 59
In contrast to the hormones mentioned above little is known about the role of auxins in 60
induced responses against herbivores Auxins regulate a vast array of plant processes 61
including growth and development as well as responses to light gravity abiotic stress and 62
pathogen attack (Glick 2015 Mano and Nemoto 2012 Yang et al 2014) Several studies 63
suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation by many 64
herbivores since some gall-forming herbivores contain high levels of IAA (Mapes and 65
Davies 2001b 2001a Tooker and Moraes 2011a Straka et al 2010 Dorchin et al 2009 66
Yamaguchi et al 2012 Tanaka et al 2013) IAA pools and signaling are enhanced in 67
parasitized plant tissue (Yamaguchi et al 2012 Tooker and Moraes 2011b) and direct 68
applications of IAA can result in the formation of gall-resembling structures (Hamner and 69
Kraus 1937 Guiscafrearrillaga 1949 Schaumlller 1968 Bartlett and Connor 2014 Connor et 70
al 2012) In the context of chewing insects however our understanding is more limited 71
(Dafoe et al 2013) IAA levels seem to remain unaltered in Solidago altissima and Triticum 72
aestivum attacked by Heliothis virescens caterpillars (Tooker and Moraes 2011a 2011b) and 73
to be reduced in Helicoverpa zea attacked Zea mays (Schmelz et al 2003) and Manduca 74
sexta-challenged Nicotiana attenuata leaves (Onkokesung et al 2010 Woldemariam et al 75
2012) Moreover mechanical wounding alone can either increase or decrease IAA levels in 76
the leaves (Thornburg and Li 1991 Tanaka and Uritani 1979 Machado et al 2013) A 77
limitation of some of these early studies is that IAA was measured at single time points or 78
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5
during the later stages of infestation (Onkokesung et al 2010 Schmelz et al 2003 Tooker 79
and Moraes 2011a 2011b) which may have resulted in an incomplete picture of IAA 80
dynamics under herbivore attack We recently demonstrated in N attenuata that IAA is 81
induced in locally damaged leaves upon simulated M sexta attack (Machado et al 2013) 82
IAA signaling may influence plant responses to herbivore attack by modulating other 83
hormonal pathways and defenses (Erb et al 2012) Exogenous IAA for instance reduces the 84
herbivory-induced accumulation of nicotine and jasmonates (Baldwin et al 1997 Baldwin 85
1989) gene expression of jasmonate-dependent proteinase inhibitors genes (Kernan and 86
Thornburg 1989) and vegetative storage proteins (DeWald et al 1994 Liu et al 2005) 87
Conversely IAA promotes the production of phenolics and flavonoids in root-cell cultures in 88
a dose-dependent manner (Lulu et al 2015 Mahdieh et al 2015) and the auxin homologue 89
24-dichlorophenoxyacetic acid (24-D) acts as a strong inducer of defense responses in rice 90
(Xin et al 2012 Song 2014) 91
In this study we aimed to understand the spatiotemporal patterns of IAA accumulation in 92
herbivore-attacked Nicotiana attenuata plants as well as the role of IAA in regulating the 93
biosynthesis of secondary metabolites In an earlier study we found that IAA accumulates 94
within 1 h following the application of M sexta oral secretions to wounded leaves To 95
understand this pattern in more detail we first evaluated IAA accumulation dynamics in 96
several plant organs in response to real and simulated M sexta attack including the 97
application of a specific herbivore elicitor to wounded leaves at different time points ranging 98
from 15 seconds to 6 h Secondly we analyzed the induction of potential IAA biosynthetic 99
genes Lastly we manipulated IAA accumulation and transport as well as jasmonate 100
signaling to unravel the impact of M sexta-induced IAA on systemic jasmonate-dependent 101
secondary metabolites Our experiments reveal that IAA is a rapid herbivory-induced signal 102
that acts in concert with jasmonates to regulate the systemic induction of plant secondary 103
metabolites104
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
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2
Auxin is rapidly induced by herbivore attack and regulates a subset of systemic 5
jasmonate-dependent secondary metabolites 6
Ricardo AR Machado12 Christelle AM Robert12 Carla CM Arce123 Abigail P Ferrieri1 7
Shuqing Xu1 Guillermo H Jimenez-Aleman1 Ian T Baldwin1 and Matthias Erb12 8
9
1Max Planck Institute for Chemical Ecology Hans-Knoumlll-Str 8 07745 Jena Germany 10
2Institute of Plant Sciences University of Bern Altenbergrain 21 3013 Bern Switzerland 11
3Departamento de Entomologia Universidade Federal de Viccedilosa 36570-000 Viccedilosa MG 12
Brazil 13
14
One sentence summary Herbivory-induced auxin promotes the production of anthocyanins 15
and phenolamides 16
17
18
This work was supported by the Max Planck Society a Humboldt Postdoctoral Research 19
Fellowship (AF) the Brazilian National Council for Research CNPq Grant No 2379292012-20
0 (CA) a Marie Curie Intra European Fellowship Grant No 328935 (SX) a Marie Curie 21
Intra European Fellowship Grant No 273107 (ME) a Swiss National Foundation Fellowship 22
Grant No 140196 (CR) a European Research Council advanced Grant No 293926 (ITB) and 23
Human Frontier Science Program Grant No RGP00022012 (ITB) 24
25
26
Author for correspondence (Phone +41 31 631 8668 E-mail matthiaserbipsunibech)27
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3
ABSTRACT 28
Plant responses to herbivore attack are regulated by phytohormonal networks To date the 29
role of the auxin indole-3-acetic acid (IAA) in this context is not well understood We 30
quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-31
attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary 32
metabolism We found that IAA is strongly rapidly and specifically induced by herbivore 33
attack IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is 34
accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes 35
IAA accumulation starts 30-60 seconds after local induction and peaks within 5 minutes after 36
induction thereby preceding the jasmonate (JA) burst IAA accumulation does not require JA 37
signaling and spreads rapidly from the wound site to systemic tissues Complementation and 38
transport inhibition experiments reveal that IAA is required for the herbivore-specific 39
jasmonate-dependent accumulation of anthocyanins and phenolamides in the stems In 40
contrast IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool 41
diterpene glycosides in the same tissue Taken together our results uncover IAA as a rapid 42
and specific signal that regulates a subset of systemic jasmonate-dependent secondary 43
metabolites in herbivore-attacked plants 44
45
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4
INTRODUCTION 46
Plants withstand herbivore attack by specifically recognizing the attacker and mounting 47
appropriate defenses Induced defense responses are activated by hormone-mediated 48
signaling cascades (Erb et al 2012 Wu and Baldwin 2009) and jasmonates (JA) have 49
emerged as key regulators in this context (Geyter et al 2012 Howe and Jander 2008) As a 50
consequence their behavior and mode of action have been studied in great detail (Wasternack 51
and Hause 2013) Similarly other stress-related hormones such as salicylic acid abscisic 52
acid and ethylene have been shown to play important roles in the orchestration of plant 53
defenses against herbivores (Dahl et al 2007 Winz and Baldwin 2001 Thaler and Bostock 54
2004 Zhang et al 2013 Kroes et al 2014) Recent evidence also suggests that hormones 55
which have traditionally been classified as growth regulators participate in induced defense 56
responses Cytokinins for instance modulate wound-induced local and systemic defense 57
responses (Schaumlfer et al 2015) and gibberellins are involved in regulating the plantrsquos 58
investment into growth and defense (Li et al 2015 Hou et al 2010 Yang et al 2012) 59
In contrast to the hormones mentioned above little is known about the role of auxins in 60
induced responses against herbivores Auxins regulate a vast array of plant processes 61
including growth and development as well as responses to light gravity abiotic stress and 62
pathogen attack (Glick 2015 Mano and Nemoto 2012 Yang et al 2014) Several studies 63
suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation by many 64
herbivores since some gall-forming herbivores contain high levels of IAA (Mapes and 65
Davies 2001b 2001a Tooker and Moraes 2011a Straka et al 2010 Dorchin et al 2009 66
Yamaguchi et al 2012 Tanaka et al 2013) IAA pools and signaling are enhanced in 67
parasitized plant tissue (Yamaguchi et al 2012 Tooker and Moraes 2011b) and direct 68
applications of IAA can result in the formation of gall-resembling structures (Hamner and 69
Kraus 1937 Guiscafrearrillaga 1949 Schaumlller 1968 Bartlett and Connor 2014 Connor et 70
al 2012) In the context of chewing insects however our understanding is more limited 71
(Dafoe et al 2013) IAA levels seem to remain unaltered in Solidago altissima and Triticum 72
aestivum attacked by Heliothis virescens caterpillars (Tooker and Moraes 2011a 2011b) and 73
to be reduced in Helicoverpa zea attacked Zea mays (Schmelz et al 2003) and Manduca 74
sexta-challenged Nicotiana attenuata leaves (Onkokesung et al 2010 Woldemariam et al 75
2012) Moreover mechanical wounding alone can either increase or decrease IAA levels in 76
the leaves (Thornburg and Li 1991 Tanaka and Uritani 1979 Machado et al 2013) A 77
limitation of some of these early studies is that IAA was measured at single time points or 78
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5
during the later stages of infestation (Onkokesung et al 2010 Schmelz et al 2003 Tooker 79
and Moraes 2011a 2011b) which may have resulted in an incomplete picture of IAA 80
dynamics under herbivore attack We recently demonstrated in N attenuata that IAA is 81
induced in locally damaged leaves upon simulated M sexta attack (Machado et al 2013) 82
IAA signaling may influence plant responses to herbivore attack by modulating other 83
hormonal pathways and defenses (Erb et al 2012) Exogenous IAA for instance reduces the 84
herbivory-induced accumulation of nicotine and jasmonates (Baldwin et al 1997 Baldwin 85
1989) gene expression of jasmonate-dependent proteinase inhibitors genes (Kernan and 86
Thornburg 1989) and vegetative storage proteins (DeWald et al 1994 Liu et al 2005) 87
Conversely IAA promotes the production of phenolics and flavonoids in root-cell cultures in 88
a dose-dependent manner (Lulu et al 2015 Mahdieh et al 2015) and the auxin homologue 89
24-dichlorophenoxyacetic acid (24-D) acts as a strong inducer of defense responses in rice 90
(Xin et al 2012 Song 2014) 91
In this study we aimed to understand the spatiotemporal patterns of IAA accumulation in 92
herbivore-attacked Nicotiana attenuata plants as well as the role of IAA in regulating the 93
biosynthesis of secondary metabolites In an earlier study we found that IAA accumulates 94
within 1 h following the application of M sexta oral secretions to wounded leaves To 95
understand this pattern in more detail we first evaluated IAA accumulation dynamics in 96
several plant organs in response to real and simulated M sexta attack including the 97
application of a specific herbivore elicitor to wounded leaves at different time points ranging 98
from 15 seconds to 6 h Secondly we analyzed the induction of potential IAA biosynthetic 99
genes Lastly we manipulated IAA accumulation and transport as well as jasmonate 100
signaling to unravel the impact of M sexta-induced IAA on systemic jasmonate-dependent 101
secondary metabolites Our experiments reveal that IAA is a rapid herbivory-induced signal 102
that acts in concert with jasmonates to regulate the systemic induction of plant secondary 103
metabolites104
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
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26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
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3
ABSTRACT 28
Plant responses to herbivore attack are regulated by phytohormonal networks To date the 29
role of the auxin indole-3-acetic acid (IAA) in this context is not well understood We 30
quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-31
attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary 32
metabolism We found that IAA is strongly rapidly and specifically induced by herbivore 33
attack IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is 34
accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes 35
IAA accumulation starts 30-60 seconds after local induction and peaks within 5 minutes after 36
induction thereby preceding the jasmonate (JA) burst IAA accumulation does not require JA 37
signaling and spreads rapidly from the wound site to systemic tissues Complementation and 38
transport inhibition experiments reveal that IAA is required for the herbivore-specific 39
jasmonate-dependent accumulation of anthocyanins and phenolamides in the stems In 40
contrast IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool 41
diterpene glycosides in the same tissue Taken together our results uncover IAA as a rapid 42
and specific signal that regulates a subset of systemic jasmonate-dependent secondary 43
metabolites in herbivore-attacked plants 44
45
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4
INTRODUCTION 46
Plants withstand herbivore attack by specifically recognizing the attacker and mounting 47
appropriate defenses Induced defense responses are activated by hormone-mediated 48
signaling cascades (Erb et al 2012 Wu and Baldwin 2009) and jasmonates (JA) have 49
emerged as key regulators in this context (Geyter et al 2012 Howe and Jander 2008) As a 50
consequence their behavior and mode of action have been studied in great detail (Wasternack 51
and Hause 2013) Similarly other stress-related hormones such as salicylic acid abscisic 52
acid and ethylene have been shown to play important roles in the orchestration of plant 53
defenses against herbivores (Dahl et al 2007 Winz and Baldwin 2001 Thaler and Bostock 54
2004 Zhang et al 2013 Kroes et al 2014) Recent evidence also suggests that hormones 55
which have traditionally been classified as growth regulators participate in induced defense 56
responses Cytokinins for instance modulate wound-induced local and systemic defense 57
responses (Schaumlfer et al 2015) and gibberellins are involved in regulating the plantrsquos 58
investment into growth and defense (Li et al 2015 Hou et al 2010 Yang et al 2012) 59
In contrast to the hormones mentioned above little is known about the role of auxins in 60
induced responses against herbivores Auxins regulate a vast array of plant processes 61
including growth and development as well as responses to light gravity abiotic stress and 62
pathogen attack (Glick 2015 Mano and Nemoto 2012 Yang et al 2014) Several studies 63
suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation by many 64
herbivores since some gall-forming herbivores contain high levels of IAA (Mapes and 65
Davies 2001b 2001a Tooker and Moraes 2011a Straka et al 2010 Dorchin et al 2009 66
Yamaguchi et al 2012 Tanaka et al 2013) IAA pools and signaling are enhanced in 67
parasitized plant tissue (Yamaguchi et al 2012 Tooker and Moraes 2011b) and direct 68
applications of IAA can result in the formation of gall-resembling structures (Hamner and 69
Kraus 1937 Guiscafrearrillaga 1949 Schaumlller 1968 Bartlett and Connor 2014 Connor et 70
al 2012) In the context of chewing insects however our understanding is more limited 71
(Dafoe et al 2013) IAA levels seem to remain unaltered in Solidago altissima and Triticum 72
aestivum attacked by Heliothis virescens caterpillars (Tooker and Moraes 2011a 2011b) and 73
to be reduced in Helicoverpa zea attacked Zea mays (Schmelz et al 2003) and Manduca 74
sexta-challenged Nicotiana attenuata leaves (Onkokesung et al 2010 Woldemariam et al 75
2012) Moreover mechanical wounding alone can either increase or decrease IAA levels in 76
the leaves (Thornburg and Li 1991 Tanaka and Uritani 1979 Machado et al 2013) A 77
limitation of some of these early studies is that IAA was measured at single time points or 78
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5
during the later stages of infestation (Onkokesung et al 2010 Schmelz et al 2003 Tooker 79
and Moraes 2011a 2011b) which may have resulted in an incomplete picture of IAA 80
dynamics under herbivore attack We recently demonstrated in N attenuata that IAA is 81
induced in locally damaged leaves upon simulated M sexta attack (Machado et al 2013) 82
IAA signaling may influence plant responses to herbivore attack by modulating other 83
hormonal pathways and defenses (Erb et al 2012) Exogenous IAA for instance reduces the 84
herbivory-induced accumulation of nicotine and jasmonates (Baldwin et al 1997 Baldwin 85
1989) gene expression of jasmonate-dependent proteinase inhibitors genes (Kernan and 86
Thornburg 1989) and vegetative storage proteins (DeWald et al 1994 Liu et al 2005) 87
Conversely IAA promotes the production of phenolics and flavonoids in root-cell cultures in 88
a dose-dependent manner (Lulu et al 2015 Mahdieh et al 2015) and the auxin homologue 89
24-dichlorophenoxyacetic acid (24-D) acts as a strong inducer of defense responses in rice 90
(Xin et al 2012 Song 2014) 91
In this study we aimed to understand the spatiotemporal patterns of IAA accumulation in 92
herbivore-attacked Nicotiana attenuata plants as well as the role of IAA in regulating the 93
biosynthesis of secondary metabolites In an earlier study we found that IAA accumulates 94
within 1 h following the application of M sexta oral secretions to wounded leaves To 95
understand this pattern in more detail we first evaluated IAA accumulation dynamics in 96
several plant organs in response to real and simulated M sexta attack including the 97
application of a specific herbivore elicitor to wounded leaves at different time points ranging 98
from 15 seconds to 6 h Secondly we analyzed the induction of potential IAA biosynthetic 99
genes Lastly we manipulated IAA accumulation and transport as well as jasmonate 100
signaling to unravel the impact of M sexta-induced IAA on systemic jasmonate-dependent 101
secondary metabolites Our experiments reveal that IAA is a rapid herbivory-induced signal 102
that acts in concert with jasmonates to regulate the systemic induction of plant secondary 103
metabolites104
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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4
INTRODUCTION 46
Plants withstand herbivore attack by specifically recognizing the attacker and mounting 47
appropriate defenses Induced defense responses are activated by hormone-mediated 48
signaling cascades (Erb et al 2012 Wu and Baldwin 2009) and jasmonates (JA) have 49
emerged as key regulators in this context (Geyter et al 2012 Howe and Jander 2008) As a 50
consequence their behavior and mode of action have been studied in great detail (Wasternack 51
and Hause 2013) Similarly other stress-related hormones such as salicylic acid abscisic 52
acid and ethylene have been shown to play important roles in the orchestration of plant 53
defenses against herbivores (Dahl et al 2007 Winz and Baldwin 2001 Thaler and Bostock 54
2004 Zhang et al 2013 Kroes et al 2014) Recent evidence also suggests that hormones 55
which have traditionally been classified as growth regulators participate in induced defense 56
responses Cytokinins for instance modulate wound-induced local and systemic defense 57
responses (Schaumlfer et al 2015) and gibberellins are involved in regulating the plantrsquos 58
investment into growth and defense (Li et al 2015 Hou et al 2010 Yang et al 2012) 59
In contrast to the hormones mentioned above little is known about the role of auxins in 60
induced responses against herbivores Auxins regulate a vast array of plant processes 61
including growth and development as well as responses to light gravity abiotic stress and 62
pathogen attack (Glick 2015 Mano and Nemoto 2012 Yang et al 2014) Several studies 63
suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation by many 64
herbivores since some gall-forming herbivores contain high levels of IAA (Mapes and 65
Davies 2001b 2001a Tooker and Moraes 2011a Straka et al 2010 Dorchin et al 2009 66
Yamaguchi et al 2012 Tanaka et al 2013) IAA pools and signaling are enhanced in 67
parasitized plant tissue (Yamaguchi et al 2012 Tooker and Moraes 2011b) and direct 68
applications of IAA can result in the formation of gall-resembling structures (Hamner and 69
Kraus 1937 Guiscafrearrillaga 1949 Schaumlller 1968 Bartlett and Connor 2014 Connor et 70
al 2012) In the context of chewing insects however our understanding is more limited 71
(Dafoe et al 2013) IAA levels seem to remain unaltered in Solidago altissima and Triticum 72
aestivum attacked by Heliothis virescens caterpillars (Tooker and Moraes 2011a 2011b) and 73
to be reduced in Helicoverpa zea attacked Zea mays (Schmelz et al 2003) and Manduca 74
sexta-challenged Nicotiana attenuata leaves (Onkokesung et al 2010 Woldemariam et al 75
2012) Moreover mechanical wounding alone can either increase or decrease IAA levels in 76
the leaves (Thornburg and Li 1991 Tanaka and Uritani 1979 Machado et al 2013) A 77
limitation of some of these early studies is that IAA was measured at single time points or 78
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5
during the later stages of infestation (Onkokesung et al 2010 Schmelz et al 2003 Tooker 79
and Moraes 2011a 2011b) which may have resulted in an incomplete picture of IAA 80
dynamics under herbivore attack We recently demonstrated in N attenuata that IAA is 81
induced in locally damaged leaves upon simulated M sexta attack (Machado et al 2013) 82
IAA signaling may influence plant responses to herbivore attack by modulating other 83
hormonal pathways and defenses (Erb et al 2012) Exogenous IAA for instance reduces the 84
herbivory-induced accumulation of nicotine and jasmonates (Baldwin et al 1997 Baldwin 85
1989) gene expression of jasmonate-dependent proteinase inhibitors genes (Kernan and 86
Thornburg 1989) and vegetative storage proteins (DeWald et al 1994 Liu et al 2005) 87
Conversely IAA promotes the production of phenolics and flavonoids in root-cell cultures in 88
a dose-dependent manner (Lulu et al 2015 Mahdieh et al 2015) and the auxin homologue 89
24-dichlorophenoxyacetic acid (24-D) acts as a strong inducer of defense responses in rice 90
(Xin et al 2012 Song 2014) 91
In this study we aimed to understand the spatiotemporal patterns of IAA accumulation in 92
herbivore-attacked Nicotiana attenuata plants as well as the role of IAA in regulating the 93
biosynthesis of secondary metabolites In an earlier study we found that IAA accumulates 94
within 1 h following the application of M sexta oral secretions to wounded leaves To 95
understand this pattern in more detail we first evaluated IAA accumulation dynamics in 96
several plant organs in response to real and simulated M sexta attack including the 97
application of a specific herbivore elicitor to wounded leaves at different time points ranging 98
from 15 seconds to 6 h Secondly we analyzed the induction of potential IAA biosynthetic 99
genes Lastly we manipulated IAA accumulation and transport as well as jasmonate 100
signaling to unravel the impact of M sexta-induced IAA on systemic jasmonate-dependent 101
secondary metabolites Our experiments reveal that IAA is a rapid herbivory-induced signal 102
that acts in concert with jasmonates to regulate the systemic induction of plant secondary 103
metabolites104
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
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8
Control 3 6
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trol
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3 min 7 min
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IAA
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gFW
)
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ontro
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+W
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+OS
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a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
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Control 15 30 60 180
aa a
bb
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ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
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30
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
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Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
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Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
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Control ab
Early rosette
0
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10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
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a
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05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
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0123
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4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
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Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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during the later stages of infestation (Onkokesung et al 2010 Schmelz et al 2003 Tooker 79
and Moraes 2011a 2011b) which may have resulted in an incomplete picture of IAA 80
dynamics under herbivore attack We recently demonstrated in N attenuata that IAA is 81
induced in locally damaged leaves upon simulated M sexta attack (Machado et al 2013) 82
IAA signaling may influence plant responses to herbivore attack by modulating other 83
hormonal pathways and defenses (Erb et al 2012) Exogenous IAA for instance reduces the 84
herbivory-induced accumulation of nicotine and jasmonates (Baldwin et al 1997 Baldwin 85
1989) gene expression of jasmonate-dependent proteinase inhibitors genes (Kernan and 86
Thornburg 1989) and vegetative storage proteins (DeWald et al 1994 Liu et al 2005) 87
Conversely IAA promotes the production of phenolics and flavonoids in root-cell cultures in 88
a dose-dependent manner (Lulu et al 2015 Mahdieh et al 2015) and the auxin homologue 89
24-dichlorophenoxyacetic acid (24-D) acts as a strong inducer of defense responses in rice 90
(Xin et al 2012 Song 2014) 91
In this study we aimed to understand the spatiotemporal patterns of IAA accumulation in 92
herbivore-attacked Nicotiana attenuata plants as well as the role of IAA in regulating the 93
biosynthesis of secondary metabolites In an earlier study we found that IAA accumulates 94
within 1 h following the application of M sexta oral secretions to wounded leaves To 95
understand this pattern in more detail we first evaluated IAA accumulation dynamics in 96
several plant organs in response to real and simulated M sexta attack including the 97
application of a specific herbivore elicitor to wounded leaves at different time points ranging 98
from 15 seconds to 6 h Secondly we analyzed the induction of potential IAA biosynthetic 99
genes Lastly we manipulated IAA accumulation and transport as well as jasmonate 100
signaling to unravel the impact of M sexta-induced IAA on systemic jasmonate-dependent 101
secondary metabolites Our experiments reveal that IAA is a rapid herbivory-induced signal 102
that acts in concert with jasmonates to regulate the systemic induction of plant secondary 103
metabolites104
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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6
RESULTS 105
Real and simulated M sexta attack induce the accumulation of indole-3-acetic acid 106
(IAA) in the leaves 107
To investigate the behavior of IAA in herbivore-attacked plants we measured IAA 108
concentrations in the leaves of Nicotiana attenuata subjected to either real or simulated M 109
sexta attack (Figure 1A to 1D) We observed a significant increase in IAA levels in response 110
to real M sexta herbivory 3h after infestation This effect could be mimicked by leaf 111
wounding and simultaneous application of either M sexta oral secretions (W+OS) or the fatty 112
acid-amino acid conjugate N-linolenoyl-glutamic acid as a specific herbivore elicitor 113
(W+FAC) (Figure 1A to 1D) Wounding alone led to a delayed and weaker increase in IAA 114
(Figure 1C) The herbivory-induced accumulation of IAA started 30-60 seconds after 115
induction (Figure 1B) and occurred independently of the time of day at which the induction 116
took place (Supplemental Figure 1) Overall IAA concentrations increased 2-3 fold in 117
herbivore induced leaves compared to controls 118
IAA induction gradually spreads through the shoots of attacked plants 119
To explore whether IAA also increases in systemic tissues we induced N attenuata plants 120
and measured IAA concentrations in local treated plant tissues and systemic untreated plant 121
tissues at different time points over a 2 h time period Again we found a rapid increase in 122
IAA levels locally upon simulated M sexta attack (W+OS) which transiently and steadily 123
spread to systemic untreated tissues (Figure 2A to 2F) IAA levels slightly increased in 124
petioles 10 min post treatment in stems 60 min post treatment and in systemic leaves 120 125
min post treatment No significant changes were found in the main and lateral roots (Figure 126
2A to 2F) 127
IAA induction in leaves is conserved across different developmental stages 128
Herbivore-induced jasmonate and ethylene signaling are influenced by plant development 129
(Diezel et al 2011a) To test whether plant development specifically influences M sexta-130
induced IAA levels we induced plants by simulated M sexta attack and measured IAA levels 131
in the leaves of early rosette elongated and flowering plants We found that the herbivore-132
elicited increase in IAA concentration was independent of plant developmental stage (Figure 133
3A to 3C) However the absolute IAA levels and magnitude of induction were strongest in 134
early rosette plants (Figure 3A to 3C) 135
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
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Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
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m c
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Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
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Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
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12
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gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
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ns
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ns
ns
ns
0
60
120
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360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
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A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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7
YUCCA-like IAA-biosynthesis homologues are rapidly upregulated upon herbivore 136
attack 137
In Arabidopsis thaliana YUCCA-genes encode for flavin monooxygenase-like proteins that 138
convert indole-3-pyruvic acid into IAA a reaction which likely represents the rate-limiting 139
step in IAA biosynthesis (Mashiguchi et al 2011) (Figure 4A) We identified YUCCA-like 140
genes in N attenuata and measured their transcript levels upon herbivore elicitation To 141
achieve this we first searched the sequence of the Arabidopsis thaliana YUCCA2 gene 142
(NCBI accession number NM_1173993) in N attenuata draft genome (Ling et al 2015) and 143
reconstructed the phylogenetic tree of the gene family (Mashiguchi et al 2011) Our analysis 144
revealed that the N attenuata genome contains at least nine YUCCA-like genes that share 145
high similarity with AtYUCCA2 and contain the four conserved amino acid motifs 146
characteristic of this gene family (Supplemental Figure 2) (Expoacutesito-Rodriacuteguez et al 2011 147
Expoacutesito-Rodriacuteguez et al 2007) We designed specific primers and profiled the expression 148
patterns of these genes upon simulated M sexta attack Several YUCCA-like genes were 149
upregulated in response to simulated M sexta attack (Figure 4B to 4I) NaYUCCA-like 1 3 150
5 6 and 9 were upregulated 3 min after the application of M sexta oral secretions and fatty 151
acid-conjugates (Figure 4B to 4H) The upregulation of NaYUCCA-like 1 and 3 was 152
maintained for at least one hour (Figure 4G to 4H) The expression of NaYUCCA-like 2 4 7 153
and 8 was not significantly influenced by simulated M sexta attack (Supplemental Figure 3) 154
IAA accumulation precedes the JA burst 155
To investigate the temporal dynamics of IAA and JA accumulation in M sexta-attacked 156
plants we quantified IAA and JA in plants subjected to simulated M sexta herbivory at 157
different time points We found that IAA peaked more rapidly than jasmonic acid in response 158
to herbivore attack (Figure 5) IAA accumulation commenced within minutes after the onset 159
of the elicitation and reached its maximum five minutes after induction JA accumulated in an 160
equally rapid fashion but peaked significantly later than IAA (Figure 5) 161
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
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8
Control 3 6
0
1
2
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Con
trol
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W+F
AC
s
Con
trol
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s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
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a
b
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0
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C
ontro
l
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+W
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+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
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4
Control 15 30 60 180
aa a
bb
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A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
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05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
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400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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8
Jasmonate signaling is not required for the M sexta-induced IAA accumulation 162
Plant responses to attackers are modulated by a complex signaling network consisting of 163
antagonistic neutral and synergistic effects (Erb et al 2012) For example jasmonate 164
signaling antagonizes IAA signaling (Chen et al 2011) To further explore the potential 165
crosstalk between these two phytohormones we measured M sexta-induced IAA in 166
transgenic plants that are impaired to different degrees in jasmonate signaling biosynthesis 167
andor perception (Table 1) We found that the M sexta-triggered accumulation of IAA does 168
not require JA signaling as it was induced in all of the evaluated JA-deficient genotypes 169
(Figure 6 and supplemental Figure 4) 170
M sexta-induced IAA is required for the induction of anthocyanins in the stems 171
To investigate the impact of IAA on plant secondary metabolites we sought to manipulate its 172
perception in planta Our initial attempts to create transgenic dexamethasone (DEX) 173
inducible plants (Schaumlfer et al 2013) harboring a silencing construct for the IAA receptor 174
TIR1 failed either because of promotor methylation in the F2 crosses (Weinhold et al 2013) 175
or because the identified TIR1 homologue was inactive We therefore took advantage of our 176
knowledge on systemic IAA accumulation to devise a series of chemical manipulation 177
experiments First we exogenously applied IAA and MeJA at doses that exceed endogenous 178
levels (Baldwin 1989 Machado et al 2013) Second we inhibited local IAA synthesis with 179
L-kynurenine (L-Kyn) L-kynurenine is a specific inhibitor of tryptophan aminotransferases 180
(TATs) which are key enzymes of the indole-3-pyruvic acid pathway that leads to IAA 181
formation (He et al 2011) Third we inhibited IAA transport at the leaf base and petiole of 182
the induced leaves using 235-triiodobenzoic acid (TIBA) TIBA inhibits auxin polar 183
transport by blocking auxin efflux transporter PIN-FORMED PIN1 cycling (Geldner et al 184
2001) We observed that within hours following M sexta attack N attenuata stems became 185
red (Figure 7D inset) a phenotype that is likely due to anthocyanin accumulation As IAA 186
can regulate the production of anthocyanins in plants (Pasqua et al 2005) we quantitatively 187
and qualitatively evaluated anthocyanin accumulation in the stems following several 188
simulated and real herbivory in combination with IAA manipulation We observed that the 189
levels of anthocyanins in the stems were strongly induced by real M sexta attack an effect 190
that could be mimicked by wounding and applications of M sexta oral secretions (W+OS) 191
but not by wounding alone (W+W) (Figure 7A) Application of IAA or MeJA alone did not 192
trigger anthocyanin accumulation (Figure 7A) By contrast the simultaneous application of 193
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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9
IAA and MeJA (IAA+MeJA) triggered anthocyanin accumulation (Figure 7A) Chemical 194
inhibition of IAA biosynthesis or transport as well as genetic inhibition of JA biosynthesis led 195
to the complete disappearance of induced anthocyanin accumulation (Figure 7B and 7C) 196
Furthermore we found a positive correlation between anthocyanin contents and red 197
pigmentation in the stems (Figure 7D) 198
IAA specifically potentiates the herbivore-induced accumulation of phenolamides in the 199
stems 200
To investigate the role of IAA in the accumulation of known defensive metabolites in the 201
stems of N attenuata (Onkokesung et al 2012 Heiling et al 2010 Paschold et al 2007) 202
we induced leaves of N attenuata plants by different simulated and real herbivory treatments 203
and complemented them with IAA at doses that exceed endogenous levels (Baldwin 1989 204
Machado et al 2013) The stems of N attenuata are often attacked by herbivores including 205
stem borers (Diezel et al 2011b Lee et al 2016) and are very important for plant fitness 206
(Machado et al 2016) We observed a strong upregulation of defensive secondary 207
metabolites in the stems in response to M sexta attack (Figure 8A to 8D) Petiole 208
pretreatments with IAA dramatically increased the accumulation of caffeoylputrescine and 209
dicaffeoylspermidine in response to real and simulated herbivory as well as MeJA 210
application IAA application alone did not induce the metabolites (Figure 8A and 8B) By 211
contrast nicotine and 7-hydroxygeranyllinalool diterpene glycosides did not respond to IAA 212
petiole pretreatments (Figure 8A to 8D) 213
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
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gFW
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ontro
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Time after M sextafeeding start (h)
a
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A B
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AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Control 15 30 60 180
aa a
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ggF
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gFW
)
IAA
(ng
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D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
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Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
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Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
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a
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a
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Early rosette
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05 1 3
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Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
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Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
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Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
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a a
b bP lt 0001
P lt 0001
a
b
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Fold
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nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
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115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
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YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
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1600
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10
20
30
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0 45 90
IAA Control
a
ba
b
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b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
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4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
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5
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-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
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SM
sex
taIA
AM
eJA
IAA+
MeJ
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P lt 0001
0
4
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12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
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trol
IAA
Control W+W W+OS M sexta MeJA
0
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IAA
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trol
IAA
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trol
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IAA
Con
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IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
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300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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10
DISCUSSION 214
In this study we show that auxin is a rapidly and specifically induced regulator of defensive 215
secondary metabolites in Nicotiana attenuata Infestation by M sexta caterpillars induced the 216
accumulation of IAA levels in local tissues an effect that could be mimicked by both the 217
applications of M sexta oral secretions and the application of the well-known insect elicitor 218
N-linolenoyl-glutamic acid (Halitschke et al 2003) and to a lesser extent by mechanical 219
wounding These results are in contrast to earlier studies in maize goldenrod and coyote 220
tobacco which found either a slight decrease or no changes in IAA levels in response to 221
herbivore attack (Schmelz et al 2003 Tooker and Moraes 2011a Onkokesung et al 2010 222
Tooker and Moraes 2011b) but are in agreement with our previous study (Machado et al 223
2013) Interestingly in comparison with our previous study we observed differences in both 224
absolute quantities and timing of IAA induction One possible explanation for these 225
differences is that plants were grown using different substrates While sand was used in the 226
previous study potting soil was used in the present paper Given the strong feedback effects 227
of soil bacteria soil nutrients and root growth on IAA signaling (Lambrecht et al 2000 228
Kurepin et al 2015 Tian et al 2008 Sassi et al 2012) it is likely that the growth substrate 229
affected IAA homeostasis and responsiveness in N attenuata On the other hand the absence 230
of IAA induction reported in earlier studies may be due to the fact that late time points were 231
measured (Onkokesung et al 2010 Schmelz et al 2003 Tooker and Moraes 2011a) which 232
may not have captured the rapid and dynamic accumulation of IAA following herbivore 233
attack To further investigate these contradicting results we determined IAA responses in 234
herbivore attacked maize plants (Maag et al submitted) We found that IAA levels increased 235
in an herbivore-specific manner 1-6 h after the onset of the attack Together these 236
experiments suggest that the rapid and transient herbivory-induced accumulation of IAA may 237
be a conserved plant response to insect attack 238
Spatiotemporal IAA profiling revealed that the rapid increase in IAA pools at the site of 239
attack is followed by a weak and transient increase in auxin pools in systemic tissues Similar 240
to what has been observed for other phytohormones (Koo et al 2009 Stitz et al 2011 241
VanDoorn et al 2011) IAA levels increased sequentially in petioles stems and systemic 242
leaves Together with the rapid local induction of YUCCA-like IAA biosynthetic homologues 243
and the absence of IAA dependent systemic defense induction in transport inhibitor treated 244
plants these data suggest that IAA might be synthesized de novo at the site of the attack and 245
then transported across the plant Several studies have demonstrated that auxin is a mobile 246
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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11
signal in plants (Reed et al 1998 Bhalerao et al 2002 Jin et al 2015 van Noorden et al 247
2006) Based on the IAA accumulation kinetics we estimate that herbivory-induced IAA 248
would need to be transported at a speed of at least 029 cmmin-1 to reach the petioles 5-10 249
minutes after elicitation (based on the fact that IAA accumulates locally 30-60 seconds after 250
elicitation) This value is at least tenfold greater than typical values of polar auxin transport 251
velocities (Kramer et al 2011) but twenty fold slower than wound-induced electrical signals 252
that trigger systemic JA accumulation (Mousavi et al 2013) We propose two hypotheses 253
that may be responsible for the atypical signal propagation speed that we observed First it is 254
possible that IAA is transported to systemic tissues by a combination of both polar and non-255
polar phloem-based transport (Friml 2003) Second rapid secondary signals including 256
electrical potentials may spread through the plant at high speeds and induce de novo IAA 257
biosynthesis in systemic tissues Further experiments with IAA radiotracers (Agtuca et al 258
2014) and transient tissue-specific deactivation of IAA biosynthesis (Koo et al 2009) would 259
help to shed further light on the exact mechanisms responsible for the systemic spread of IAA 260
following herbivore attack 261
Impairing key genes of the jasmonate signaling cascade including mitogen-activated protein 262
kinases jasmonate biosynthesis and jasmonate perception elements did not impair the 263
herbivory-induced accumulation of IAA suggesting that IAA induction does not require JA 264
signaling This observation is consistent with the temporal dynamics of herbivory-induced 265
IAA and JA that we observed IAA accumulation peaks within 5 minutes after the onset of 266
the elicitation while JA starts accumulating in an equally rapid fashion but peaks 267
significantly later than IAA (Figure 5) 268
An important aim of our study was to understand whether IAA is involved in the regulation 269
of induced secondary metabolites in N attenuata Because of the systemic accumulation 270
pattern of IAA and the possibility to block this effect through the local application of 271
transport inhibitors we chose to focus on the induction of stem secondary metabolites The 272
stem of N attenuata is vital for its reproduction and can be attacked by a wide variety of 273
organisms including vertebrates and invertebrate stem borers (Machado et al 2016 Diezel 274
et al 2011b) We observed that real and simulated M sexta attack induced anthocyanin 275
accumulation in the stems an effect that could not be reproduced by MeJA or IAA treatments 276
alone but by the combination of these two hormones Together with the IAA transport and 277
biosynthesis inhibitor treatments and the genetic silencing of JA biosynthesis all of which led 278
to the disappearance of the anthocyanin response these results strongly suggest that IAA is 279
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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12
required to activate the JA-dependent accumulation of stem anthocyanins In A thaliana 280
anthocyanin production is controlled by the MYB75 transcription factor Production of 281
Anthocyanin Pigment 1 (PAP1) (Shin et al 2015 Borevitz et al 2000) which is 282
transcriptionally upregulated by IAA (Lewis et al 2011) and postranscriptionally repressed 283
by jasmonate-ZIM-Domain (JAZ) proteins (Qi et al 2011) The resulting co-regulation of 284
MYB transcription factors by IAA and JA provides a potential mechanism for the synergistic 285
interaction between JA and IAA observed in our study 286
In a second set of experiments we found that IAA also boosts the production of 287
phenolamides in herbivore-attacked plants Phenolamide accumulation in N attenuata is 288
controlled by the transcription factor MYB8 in a JA-dependent manner (Onkokesung et al 289
2012 Paschold et al 2007) This transcription factor may therefore represent a target for the 290
integration of IAA and JA signaling While IAA strongly potentiated the accumulation of 291
stem phenolamides it had little effect on the accumulation of other JA-dependent secondary 292
metabolites including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado 293
et al 2013 Paschold et al 2007 Jimenez-Aleman et al 2015 Machado et al 2016) This 294
result is consistent with earlier studies showing neutral to negative effects of auxin 295
application on nicotine accumulation in Nicotiana spp (Baldwin 1989 Baldwin et al 1997 296
Shi et al 2006) The direct application of IAA to wounded tissues can even suppress local 297
damage-induced JA accumulation (Dahl and Baldwin 2004 Baldwin et al 1997 Shi et al 298
2006) From these results it is evident that IAA does not simply enhance JA signaling but 299
that it specifically modulates a plantrsquos defensive network Thereby IAA signaling may help 300
plants to mount specific fine-tuned responses to different attackers 301
The ecological function of an upregulation of anthocyanin and phenolamide compounds in 302
the stems upon M sexta attack remains an open question The current literature however 303
provides interesting insights in this context Trichobaris stem weevils prefer to feed and 304
perform better on defenseless jasmonate-deficient plants in a species-specific manner T 305
compacta grows better on nicotine-impaired N attenuata plants while T mucorea is not 306
affected by nicotine but by other yet unknown jasmonate-dependent defenses (Diezel et al 307
2011b Lee et al 2016) It is therefore possible that the IAA-triggered potentiation of 308
jasmonate-dependent secondary metabolite accumulation in the stems may reduce the 309
performance of stem feeders To disentangle the specific effects that IAA signaling has in this 310
context requires the development of IAA-signaling impaired genotypes and represents an 311
interesting prospect of this study 312
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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A B
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Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Early JA-signaling JA-biosynthesis JA-Ile-perception
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Impaired in
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Caffeoylputrescine
Dicaffeoylspermidine
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A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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13
In conclusion this study identifies IAA as a rapid and specific signal that regulates a 313
biologically relevant subset of herbivory-induced secondary metabolites Current models on 314
plant defense signaling networks in plant-herbivore interactions can now be expanded to 315
include auxins as potentially important defense hormones 316
METHODS 317
Plant genotypes germination and planting conditions 318
Wild-type N attenuata Torr Ex Watson plants of the 31th inbred generation derived from 319
seeds collected at the Desert Inn Ranch in Utah in 1988 and all genetically engineered plant 320
genotypes were germinated on Gamborgrsquos B5 medium as described (Kruumlgel et al 2002) 321
Nine to ten days later seedlings were transferred to Teku pots (Poumlppelmann GmbH amp Co 322
KG Lohne Germany) for 10-12 days before transferring them into 1 L pots filled with either 323
sand (to facilitate the harvesting of belowground tissues) or soil All plants were grown at 45-324
55 relative humidity and 23-25 degC during days and 19-23 degC during nights under 16 h of 325
light (6am-10pm) Plants planted in soil were watered every day by a flood irrigation system 326
Plants planted in sand were watered twice a day The characteristics of the transgenic plants 327
used in this study are presented in table 1 328
Auxin and jasmonate measurements 329
Phytohormone measurements were conducted as described earlier (Machado et al 2013 330
Machado et al 2015) Briefly plant tissues were harvested flash frozen and stored at -80degC 331
After grinding 100 mg of plant tissue per sample were extracted with 1 mL ethyl acetate 332
formic acid (99505 vv) containing the following phytohormone standards 40ng of 910-333
D2-910-dihydrojasmonic acid (JA) 8 ng of jasmonic acid-[13C6] isoleucine (JA-Ile) and 20 334
ng of D5-indole-3-acetic-acid (IAA) All samples were then vortexed for 10 min and 335
centrifuged at 14000 rpm for 20 min at 4 degC Supernatants were evaporated to dryness in a 336
centrifugal vacuum concentrator (Eppendorf 5301 Eppendorf Hamburg Germany) at room 337
temperature The remaining pellets were resuspended in 50 μL methanol water (7030) and 338
dissolved using an ultrasonic cleaner (Branson 1210 Branson Ultrasonics 339
Danbury Connecticut USA) for 5 min Samples were then analyzed using liquid 340
chromatography (Agilent 1260 Infinity Quaternary LC system Agilent Technologies Santa 341
Clara California USA) coupled to a triple quadrupole mass spectrometer (API 5000 342
LCMSMS Applied Biosystems Foster City California USA) 343
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
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31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
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8
Control 3 6
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trol
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3 min 7 min
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gFW
)
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ontro
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+W
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+OS
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a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
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Control 15 30 60 180
aa a
bb
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ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
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30
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
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Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
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Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
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Control ab
Early rosette
0
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10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
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a
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b
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0
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05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
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4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
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Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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14
IAA levels in herbivore attacked plants 344
IAA levels were determined in local treated leaves of plant subjected to real or simulated M 345
sexta attack Plants were infested by placing 3 first-instar larvae on one fully developed 346
rosette leaf (n=3) Caterpillars were removed and attacked leaves were harvested M sexta 347
attack was simulated by rolling a pattern wheel over the leaves on each side of the midvein 348
Three fully developed rosette leaves were wounded and the resulting wounds were 349
immediately treated with either 15 (vv) water-diluted M sexta oral secretions (W+OS) with 350
pure water (W+W) or with fatty acid-amino acid conjugates (FACs N-linolenoyl-glutamic 351
acid) as described (Xu et al 2015 Machado et al 2013) Intact plants were used as controls 352
(n=5) 353
M sexta-induced auxin levels in different plant tissues 354
Forty-day-old elongating plants were subjected to simulated M sexta attack as described 355
above Five 10 30 60 and 120 min after elicitation treated leaves and their untreated 356
petioles as well as stems systemic leaves (young leaves directly above treated leaves) and 357
main and lateral roots were harvested The same plant tissues were collected from untreated 358
control plants at each time point (n=5) 359
M sexta-induced auxin levels at different developmental stages 360
IAA levels were measured at three developmental stages early rosette (32 days after 361
germination DAG) elongating (39 DAG) and flowering (46 DAG) Tissues were harvested 362
at three time points after elicitation as described above 05 1 and 3h (n=5) 363
Identification and expression profiling of YUCCA-like genes 364
YUCCA genes encode for flavin monooxygenase-like proteins that convert indole-3-pyruvic 365
acid into indole-3-acetic acid (IAA) a catalytic reaction that is currently seen as the limiting 366
step of IAA biosynthesis (Mashiguchi et al 2011) To identify YUCCA-like genes in N 367
attenuata we searched the Arabidopsis thaliana YUCCA2 gene sequence (NCBI accession 368
number NM_1173993) in the N attenuata draft genome (Ling et al 2015) using BLAST (E-369
valuelt1e-10 bit scoregt200) and reconstructed the phylogenetic tree of the gene family We 370
then designed specific primers (Supplemental Table 1) for each gene using Primique 371
(Fredslund and Lange 2007) and profiled gene expression patterns upon simulated M sexta 372
attack by quantitative real-time PCR (qPCR)(n=3) Total RNA was extracted by the TRIZOL 373
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
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AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
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A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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15
method followed by DNase-I treatment (Fermentas St Leon-Rot Germany) according to 374
the manufacturerrsquos instructions Five micrograms of total RNA were reverse-transcribed 375
using oligo (dT)18 and the SuperScript-II Reverse Transcriptase kit (Invitrogen) The 376
obtained cDNA was used for gene expression profiling with SYBR Green I following the 377
manufacturerrsquos protocol and the ∆Ct method was used for transcript evaluation The 378
housekeeping gene actin was used as reference Gene expression levels were determined 3 5 379
and 60 minutes after elicitation 380
Characterization of the YUCCA-like gene family 381
The YUCCA-like gene family sequences were aligned by Clustal W (Thompson et al 1994) 382
in BioEdit (Hall 1999) and the occurrence of the already described conserved amino acid 383
motifs characteristic of the flavin monooxygenase gene family was determined (Expoacutesito-384
Rodriacuteguez et al 2011 Expoacutesito-Rodriacuteguez et al 2007) 385
OS-induced auxin and jasmonate kinetics 386
Rosette leaves of wild type plants were subjected to simulated M sexta attack (W+OS) as 387
described and harvested 5 45 and 90 min after elicitation (n=5) Phytohormone 388
measurements were carried out as described 389
M sexta-induced auxin levels in jasmonate and signaling impaired genotypes 390
Three rosette leaves of rosette-stage plant genotypes impaired in salicylic acid-induced and 391
wound-induced mitogen-activated protein kinases (irSIPK irWIPK respectively) jasmonic 392
acid biosynthesis (irGLA irAOS irAOC irOPR3) jasmonic acid-isoleucine biosynthesis 393
(irJAR46) jasmonate perception (irCOI1) and wild type empty vector (EV) were subjected 394
to M sexta simulated attack as described 45 min after elicitation the leaves were harvested 395
and analyzed for IAA jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) (n=5) These 396
transgenic plant genotypes were selected as they are impaired at different layers of the 397
jasmonate signaling cascade early regulatory elements (irSIPK irWIPK) jasmonate 398
biosynthesis (irGLA irAOS irAOC irOPR3) hormone activation (irJAR46) and hormone 399
perception (irCOI1) and their main characteristics are listed in table 1 400
Stem anthocyanin quantifications 401
To determine the role of IAA in M sexta induced stem anthocyanin accumulation we carried 402
out three experiments First we measured anthocyanins in the stem of plants whose rosette 403
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
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31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
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trol
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gFW
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ontro
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a
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bP lt 0001
Time after M sextafeeding start (h)
a
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bP lt 0015
A B
C
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AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Control 15 30 60 180
aa a
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ggF
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gFW
)
IAA
(ng
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D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
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Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
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Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
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a
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a
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Early rosette
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Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
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Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
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Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
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a a
b bP lt 0001
P lt 0001
a
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Fold
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nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
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115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
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YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
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1600
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10
20
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0 45 90
IAA Control
a
ba
b
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b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
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4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
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-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
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sex
taIA
AM
eJA
IAA+
MeJ
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P lt 0001
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4
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16
Con
trol
W+O
SC
ontro
lW
+OS
Con
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W+O
SC
ontro
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+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
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trol
IAA
Control W+W W+OS M sexta MeJA
0
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IAA
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trol
IAA
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trol
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IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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16
leaves were either left intact (Control) wounded and treated with water (W+W) wounded 404
and treated with M sexta oral secretions (W+OS) subjected to real continuous M sexta 405
attack (M sexta) treated with the natural auxin IAA (IAA) methyl jasmonic acid (MeJA) or 406
with both IAA and MeJA (IAA+MeJA) dissolved in lanoline paste (n=5) Simulated M sexta 407
attack treatments were carried out as described above Hormonal treatments were carried out 408
as described below In the second experiment we measured stem anthocyanins in plants 409
whose petioles were treated (petiole pretreatment) with the IAA biosynthesis inhibitor L-410
kynurenine (L-Kyn) (He et al 2011) the IAA transport inhibitor 235-triiodobenzoic acid 411
(TIBA) (Hertel et al 1983 Goldsmith 1982 Rubery 1979) or with the natural auxin indole-412
3-acetic acid (IAA) prior to eliciting the plants by simulated M sexta attack (W+OS) (n=12) 413
One hour prior to the simulated M sexta attack treatments approximately 2 microg of L-Kyn 414
TIBA or IAA or 150 microg MeJA dissolved in lanoline paste were applied to the petioles 415
Applied doses were selected according to previous studies (Baldwin 1989 Morris et al 416
1973 Kang et al 2006 He et al 2011) (n=12) In a third experiment we measured changes 417
in stem anthocyanin levels upon simulated M sexta herbivory in jasmonate-deficient irAOC 418
and empty vector (EV) controls (n=10) Simulated and real M sexta attack treatments were 419
carried out as described For all the experiments the stems were harvested five days after 420
treatments and the anthocyanin content of the outer layer (epidermis cortex phloem and 421
cambium) was determined 5 cm above the shoot-root junction as described (Steppuhn et al 422
2010) 423
Stem secondary metabolite quantifications 424
To further explore the regulatory role of IAA in secondary metabolite production we induced 425
the leaves of N attenuata plants using real and simulated M sexta attack treatments Plants 426
were either pretreated with IAA in lanolin paste or with pure lanolin as controls as described 427
above Petiole pretreatments with IAA were carried out one hour prior to induction Five days 428
after induction the stems were harvested and secondary metabolites were measured as 429
described (Gaquerel et al 2010 Ferrieri et al 2015)(n=5) 430
Statistics 431
All data were analyzed by ANOVA using Sigma Plot 120 (Systat Software Inc San Jose 432
CA USA) Normality and equality of variance were verified using ShapirondashWilk and 433
Levenersquos tests respectively HolmndashSidak post hoc tests were used for multiple comparisons 434
Datasets from experiments that did not fulfill the assumptions for ANOVA were natural log- 435
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
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Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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ControlW+OS
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Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
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Time after treatment (h)
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
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C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
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Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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+OS
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+OS
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olg
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m a
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A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Caffeoylputrescine
Dicaffeoylspermidine
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Nicotine
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eak
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microgg
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A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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- Parsed Citations
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17
root square- or rank-transformed before analysis Correlation between jasmonate and IAA 436
levels and stem coloration index and stem anthocyanin content were evaluated by Pearson 437
product moment test 438
ACKNOWLEDGEMENTS 439
All experimental work of this study was supported by the Max Planck Society We would 440
also like to thank the members of the Department of Molecular Ecology and the glasshouse 441
team of the MPI-CE for their help Special thanks go to Mareike Schirmer and Mareike 442
Schmidt for technical support and to Wenwu Zhou Martin Schaumlfer and Michael Reichelt for 443
their valuable help with the auxin measurements CAMR was supported by a Swiss National 444
Foundation Fellowship (grant no 140196) CCMA by the Brazilian National Council for 445
Research (grant no 2379292012-0) APF by an Alexander von Humboldt Postdoctoral 446
Fellowship SX by a Marie Curie Intra European Fellowship (grant no 328935) ITB by a 447
European Research Council advanced (grant no 293926) and by a Human Frontier Science 448
Program (grant no RGP00022012) and ME by an SNF early post doc fellowship (grant no 449
134930) and a Marie Curie Intra European Fellowship (grant no 273107) 450
AUTHOR CONTRIBUTIONS 451
Designed the research RARM ME ITB Carried out the experimental work RARM 452
CCMA APF CAMR GHJA SX Analyzed data RARM ME ITB Wrote the first draft of 453
the paper RARM ME Revised the paper ME RARM ITB APF CCMA GHJA SX 454
CAMR All authors read and approved the final manuscript 455
456
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
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Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
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Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
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Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
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Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
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Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
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Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
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Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
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Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
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Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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18
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 457
Genotype Gene silencedoverexpressed
Impaired function Phenotype Reference
irSIPK Salicylic acid-induced
mitogen activated protein kinase Early
jasmonate signalling
Reduced levels of jasmonates
Meldau et al 2009
irWIPK Wound-induced
mitogen activated protein kinase
irGLA1 Glycerolipase A1
Jasmonate biosynthesis
Bonaventure et al 2011
irAOS Allene oxide synthase
Kallenbach et al 2012 irAOC Allene oxide cyclase
irOPR3 12-oxo-phytodienoic acid reductase
irJAR46 JA-Ile synthetase Reduced levels of JA-Ile
Wang et al 2008
irCOI1 Coronatine-insensitive 1 JA-Ile perception
Reduced JA-Ile perception
Paschold et al 2007
458
TABLE LEGENDS 463
Table 1 Characteristics of the inverted repeat (ir) transgenic lines used in the present study 464
FIGURE LEGENDS 465
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated 466
M sexta attack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars 467
(A) treated with M sexta oral secretions (B C) or treated with an herbivore elicitor (D) 468
(n=5) Different letters indicate significant differences between treatments (P lt 005) 469
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 470
sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid conjugate-471
treated plants 472
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19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
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21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
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22
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root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
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25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
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26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
19
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels 473
following simulated M sexta attack in local treated leaves (A) and in untreated petioles (B) 474
stem (C) systemic leaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate 475
significant differences between treatments within plant tissues and time points ( P lt 005 476
P lt 0001) Control intact plants W+OS wounded and M sexta oral secretion-treated 477
plants 478
Figure 3 IAA induction in leaves occurs across different developmental stages Average 479
(plusmnSE) IAA levels in local treated leaves following simulated M sexta attack at the early 480
rosette (A) elongated (B) and flowering stage (C) (n=5) Different letters indicate significant 481
differences between treatments within developmental stages and time points (P lt 005) 482
Control intact plants W+W wounded and water-treated plants W+OS wounded and M 483
sexta oral secretion-treated plants 484
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory 485
(A) Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into 486
IAA Average (plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-487
like 5 (C) YUCCA-like 6 (D) and YUCCA-like 9 (E) in treated leaves three minutes after 488
elicitation and YUCCA-like 1 (F) and YUCCA-like 3 (G) 5 and 60 min following simulated 489
M sexta attack (n=3) Different letters indicate significant differences between treatments (P 490
lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded 491
and M sexta oral secretion-treated plants W+FACs wounded and fatty acid-amino acid 492
conjugate-treated plants 493
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis 494
average (plusmnSE) leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) 495
leaf JA levels in response to M sexta attack Closed squares IAA levels upon W+OS 496
treatments closed triangles IAA levels in control untreated plants Grey squares JA levels 497
upon W+OS treatments grey triangles jasmonic acid (JA) levels in control untreated plants 498
(n=5) Different letters indicate significant differences between treatments for individual 499
metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Time treatment P = 500
0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Control 501
intact plants W+OS wounded and M sexta oral secretion-treated plants 502
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA 503
(A) Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) 504
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
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8
Control 3 6
0
1
2
3
Con
trol
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AC
s
Con
trol
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s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
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a
b
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C
ontro
l
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+W
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+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
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4
Control 15 30 60 180
aa a
bb
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A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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- Figure 1
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- Figure 4
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- Figure 7
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- Parsed Citations
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20
and plant genotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile 505
perception 45 minutes after elicitation (n=5) Different letters indicate significant differences 506
between treatments within each genotype (P lt 005) C control intact plants W wounded 507
and water-treated plants OS wounded and M sexta oral secretions-treated plants 508
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin 509
accumulation in the stems (A) Average (plusmnSE) stem anthocyanin content 5 days following 510
either simulated or continuous M sexta attack exogenous application of methyl jasmonate 511
(MeJA) andor IAA (n=5) (B) Average (plusmnSE) stem anthocyanin content 5 days following 512
simulated M sexta attack and petiole-pretreatments with either IAA the IAA biosynthesis 513
inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic 514
acid) (n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta 515
attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem 516
anthocyanin content and stem coloration Inset Photograph of the red stem phenotype 517
Asterisks indicate significant differences between treatments and control (A) between 518
simulated herbivory treatments within petiole pretreatments (B) and between treatments 519
within genotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between 520
stem coloration index and stem anthocyanin content was evaluated by a Pearson product 521
moment test Leaf treatments Control intact plants W+W wounded and water-treated 522
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 523
to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJA rosette 524
leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and 525
MeJA Petiole pretreatments Petioles treated with either pure lanoline paste (Lanoline) L-526
kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) 527
dissolved in lanoline 1h prior to leaf treatments 528
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of 529
phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) 530
and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta 531
attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences 532
between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P 533
lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline 534
paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior 535
to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated 536
plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected 537
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
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Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
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specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
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Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
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Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
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Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
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Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
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Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
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gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
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Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
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Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
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Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
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Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
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Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
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Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
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Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
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Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
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Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
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Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
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Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
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Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
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Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
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Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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- Figure 1
- Figure 2
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- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
21
to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in 538
lanoline paste 539
SUPPLEMENTAL DATA 540
Supplemental Figure 1 IAA is induced locally in response to simulated M sexta herbivory 541
independently of time of day 542
Supplemental Figure 2 The N attenuata genome contains nine YUCCA-like genes 543
Supplemental Figure 3 Gene expression patterns of YUCCA-like genes upon simulated M 544
sexta attack 545
Supplemental Figure 4 Jasmonate signaling is not required for the M sexta-induced 546
accumulation of IAA 547
Supplemental Table 1 Sequence of primers used for quantitative PCR analysis 548
549
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
22
REFERENCES 550
Agtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and 551
Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in 552
regulating leaf physiology leaf metabolism and resource allocation patterns that impact 553
root growth in Zea mays Journal of plant growth regulation 33 (2) 328ndash339 554
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco 555
Journal of Chemical Ecology 15 (5) 1661ndash1680 556
Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and 557
Schmelz EA (1997) Quantification correlations and manipulations of wound-induced 558
changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397ndash404 559
Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant 560
galls by insects Arthropod-Plant Interactions 8 (4) 339ndash348 561
Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G 562
(2002) Shoot‐derived auxin is essential for early lateral root emergence in Arabidopsis 563
seedlings The Plant Journal 29 (3) 325ndash332 564
Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and 565
specificity in the activation of lipase‐mediated oxylipin biosynthesis a specific role of the 566
Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves 567
and roots Plant cell amp environment 34 (9) 1507ndash1520 568
Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging 569
identifies a conserved MYB regulator of phenylpropanoid biosynthesis The Plant Cell 12 570
(12) 2383ndash2393 571
Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and 572
Qi J (2011) The basic helix-loop-helix transcription factor MYC2 directly represses 573
PLETHORA expression during jasmonate-mediated modulation of the root stem cell 574
niche in Arabidopsis The Plant Cell 23 (9) 3335ndash3352 575
Connor EF Bartlett L OrsquoToole S Byrd S Biskar K and Orozco J (2012) The 576
mechanism of gall induction makes galls red Arthropod-Plant Interactions 6 (4) 489ndash577
495 578
Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A 579
Teal PE and Schmelz EA (2013) European corn borer (Ostrinia nubilalis) induced 580
responses enhance susceptibility in maize PloS one 8 (9) 581
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23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
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24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
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AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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22
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Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
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Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
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Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
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response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
23
Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis‐jasmone do not dispose 582
of the herbivore‐induced jasmonate burst in Nicotiana attenuata Physiologia Plantarum 583
120 (3) 474ndash481 584
Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT 585
(2007) Tuning the herbivore‐induced ethylene burst the role of transcript accumulation 586
and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293ndash307 587
DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp 588
gene expression is inhibited by auxin Plant Physiology 104 (2) 439ndash444 589
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns 590
in Nicotiana attenuata Flowering attenuates herbivory‐elicited ethylene and jasmonate 591
Signaling Journal of integrative plant biology 53 (12) 971ndash983 592
Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatarsquos 593
jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae Plant 594
Physiology 155 (4) 1936ndash1946 595
Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J 596
(2009) Sexually dimorphic gall structures correspond to differential phytohormone 597
contents in male and female wasp larvae Physiological Entomology 34 (4) 359ndash369 598
Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific 599
plant reactions Trends in plant science 17 (5) 250ndash259 600
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA 601
(2007) Cloning and biochemical characterization of ToFZY a tomato gene encoding a 602
flavin monooxygenase involved in a tryptophan-dependent auxin biosynthesis pathway 603
Journal of plant growth regulation 26 (4) 329ndash340 604
Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene 605
structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like 606
flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry 49 607
(7) 782ndash791 608
Ferrieri AP Arce C Machado RAR Meza‐Canales ID Lima E Baldwin IT 609
and Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) 610
reduces growth and increases secondary metabolite biosynthesis in herbivore‐attacked 611
plants New Phytologist 612
Fredslund J and Lange M (2007) Primique automatic design of specific PCR primers 613
for each sequence in a family BMC bioinformatics 8 (1) 369 614
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
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Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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020406080
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Time P = 0764Treatment P = 0558TT P = 0093
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Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
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1010
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Time after treatment (h)
01020304050
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
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IAA
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
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C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
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Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
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+OS
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ontro
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+OS
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Genotype P lt 0001Treatment P lt 0001GT P lt 0001
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olg
FW)
Ste
m a
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in c
onte
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(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
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Caffeoylputrescine
Dicaffeoylspermidine
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Nicotine
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eak
area
103
gFW
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ns
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360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin IT and Erb M (2013) Leaf-herbivore attackreduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234-1246
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits of jasmonate-dependent defenses againstvertebrate herbivores in nature Elife 5 e13720
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root Induction and Flavonoid Profiles inRumex crispus Advances in Life Sciences 5 (3) 53-57
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of Experimental Botany ers091Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurostasolidaginis New Phytologist 151 (1) 203-212
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001b) Indole-3-acetic acid and ball gall development on Solidago altissima New Phytologist 151(1) 195-202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M Hanada A Yaeno T Shirasu K and Yao H(2011) The main auxin biosynthesis pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 18512-18517
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory-activated MAP kinases SIPK and WIPK does not increaseNicotiana attenuatas susceptibility to herbivores in the glasshouse and in nature New Phytologist 181 (1) 161-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings (Pisum sativum L) the inhibition oftransport by 2 3 5-triiodobenzoic acid Planta 110 (2) 173-182
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediateleaf-to-leaf wound signalling Nature 500 (7463) 422-426
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT (2010) Jasmonic acid and ethylene modulatelocal responses to wounding and simulated herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785-798
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) MYB8 controls inducible phenolamide levels wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
by activating three novel hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant Physiology 158 (1)389-407
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paschold A Halitschke R and Baldwin IT (2007) Co (i)-ordinating defenses NaCOI1 mediates herbivore-induced resistance inNicotiana attenuata and reveals the role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79-91
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and Vinceri FF (2005) The effect of growthregulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 43(3) 293-298
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral rootdevelopment in Arabidopsis Plant Physiology 118 (4) 1369-1378
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on auxin transport by suspension-culturedcrown gall cells Planta 144 (2) 173-178
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr die Gallenbildung Zool Jb Physiol 7454-87
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
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Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
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Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
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Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
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Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
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Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
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Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
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Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
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Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
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Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
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Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
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- Foliennummer 1
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
24
Friml J (2003) Auxin transportmdashshaping the plant Current opinion in plant biology 6 (1) 615
7ndash12 616
Gaquerel E Heiling S Schoumlttner M Zurek G and Baldwin IT (2010) 617
Development and validation of a liquid chromatographyminus electrospray ionizationminus time-618
of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves 619
during simulated herbivory Journal of Agricultural and Food Chemistry 58 (17) 9418ndash620
9427 621
Geldner N Friml J Stierhof Y-D Juumlrgens G and Palme K (2001) Auxin transport 622
inhibitors block PIN1 cycling and vesicle trafficking Nature 413 (6854) 425ndash428 623
Geyter N de Gholami A Goormachtig S and Goossens A (2012) Transcriptional 624
machineries in jasmonate-elicited plant secondary metabolism Trends in plant science 17 625
(6) 349ndash359 626
Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer) 627
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-628
acetic acid in sections of maize coleoptiles Planta 155 (1) 68ndash75 629
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in 630
response to injections of growth-regulating substances Phytopathology 39 (6) 489ndash493 631
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular 632
interactions between the specialist herbivore Manduca sexta (Lepidoptera Sphingidae) 633
and its natural host Nicotiana attenuata VI Microarray analysis reveals that most 634
herbivore-specific transcriptional changes are mediated by fatty acid-amino acid 635
conjugates Plant Physiology 131 (4) 1894ndash1902 636
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis 637
program for Windows 9598NT Nucleic acids symposium series (41) 95-98 638
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth 639
promoting substances Botanical Gazette 735ndash807 640
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An 641
F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of 642
TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in 643
Arabidopsis The Plant Cell 23 (11) 3944ndash3960 644
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B 645
Jassbi AR and Baldwin IT (2010) Jasmonate and ppHsystemin regulate key 646
malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides 647
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
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30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
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AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles from Cucurbita pepo L Planta 157 (3) 193-201
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Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZsDevelopmental cell 19 (6) 884-894
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Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant Biol 59 41-66Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W (2015) Synthesis structural characterization andbiological activity of two diastereomeric JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885-5893
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Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal that acts independently of ethylene signalingon leaf abscission in Populus Frontiers in plant science 6 634
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Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT (2012) Empoasca leafhoppers attack wild tobaccoplants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations Proceedings of the NationalAcademy of Sciences 109 (24) E1548-E1557
Pubmed Author and Title wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairsjasmonic acid-isoleucine-mediated defenses against Manduca sexta The Plant Cell 18 (11) 3303-3320
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Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in vitro and in vivo Plant Physiology 91 (1) 73-78
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Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactivejasmonates in Arabidopsis The Plant Journal 59 (6) 974-986
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Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin transport velocities Trends in plant science 16 (9)461-463
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of aphids with caterpillar-induced defenses inArabidopsis Involvement of phytohormones and transcription factors Plant and cell physiology pcu150
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotianaattenuata a model ecological expression system Chemoecology 12 (4) 177-183
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Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia phytofirmans-induced shoot and root growthpromotion is associated with endogenous changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199-207
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Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic acid a reciprocal signalling molecule in bacteria-plant interactions evolution 54 59
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Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris weevils distinguish amongst toxic host plants bysensing volatiles that do not affect larval performance Molecular ecology
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Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF Winkel BSJ and Muday GK (2011) Auxin andethylene induce flavonol accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144-164
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Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) Prioritizing plant defence over growth throughWRKY regulation facilitates infestation by non-target herbivores Elife 4 e04805
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Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome-wide alternative splicing responses in Nicotianaattenuata The Plant Journal 84 (1) 228-243
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Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 1545-1556
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and bioactive compounds from adventitious roots byoptimization of culturing conditions of Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience andbioengineering 119 (6) 712-717
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Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate-dependent depletion of soluble sugarscompromises plant resistance to Manduca sexta New Phytologist 207 (1) 91-105
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Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin IT and Erb M (2013) Leaf-herbivore attackreduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234-1246
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Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits of jasmonate-dependent defenses againstvertebrate herbivores in nature Elife 5 e13720
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Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root Induction and Flavonoid Profiles inRumex crispus Advances in Life Sciences 5 (3) 53-57
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Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT (2010) Jasmonic acid and ethylene modulatelocal responses to wounding and simulated herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785-798
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Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
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Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
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Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
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Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
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Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
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Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
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Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
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Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
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Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
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in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
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Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
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Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
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Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
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Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
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Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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- Parsed Citations
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- Parsed Citations
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25
an abundant and effective direct defense against herbivores in Nicotiana attenuata The 648
Plant Cell 22 (1) 273ndash292 649
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles 650
from Cucurbita pepo L Planta 157 (3) 193ndash201 651
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate 652
signaling via competitive binding to JAZs Developmental cell 19 (6) 884ndash894 653
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant 654
Biol 59 41ndash66 655
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W 656
(2015) Synthesis structural characterization and biological activity of two diastereomeric 657
JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885ndash5893 658
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal 659
that acts independently of ethylene signaling on leaf abscission in Populus Frontiers in 660
plant science 6 634 661
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT 662
(2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent 663
manner and identify jasmonate mutants in natural populations Proceedings of the 664
National Academy of Sciences 109 (24) E1548-E1557 665
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase 666
and JAR4 in Nicotiana attenuata impairs jasmonic acidndashisoleucinendashmediated defenses 667
against Manduca sexta The Plant Cell 18 (11) 3303ndash3320 668
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a 669
wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in 670
vitro and in vivo Plant Physiology 91 (1) 73ndash78 671
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal 672
activates the systemic synthesis of bioactive jasmonates in Arabidopsis The Plant Journal 673
59 (6) 974ndash986 674
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin 675
transport velocities Trends in plant science 16 (9) 461ndash463 676
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of 677
aphids with caterpillar-induced defenses in Arabidopsis Involvement of phytohormones 678
and transcription factors Plant and cell physiology pcu150 679
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
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26
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-680
mediated transformation of Nicotiana attenuata a model ecological expression system 681
Chemoecology 12 (4) 177ndash183 682
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia 683
phytofirmans-induced shoot and root growth promotion is associated with endogenous 684
changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199ndash207 685
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic 686
acid a reciprocal signalling molecule in bacteriandashplant interactions evolution 54 59 687
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris 688
weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval 689
performance Molecular ecology 690
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF 691
Winkel BSJ and Muday GK (2011) Auxin and ethylene induce flavonol 692
accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144ndash693
164 694
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) 695
Prioritizing plant defence over growth through WRKY regulation facilitates infestation by 696
non-target herbivores Elife 4 e04805 697
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome‐wide 698
alternative splicing responses in Nicotiana attenuata The Plant Journal 84 (1) 228ndash243 699
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B 700
Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis 701
vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 702
1545ndash1556 703
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and 704
bioactive compounds from adventitious roots by optimization of culturing conditions of 705
Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience and 706
bioengineering 119 (6) 712ndash717 707
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate‐708
dependent depletion of soluble sugars compromises plant resistance to Manduca sexta 709
New Phytologist 207 (1) 91ndash105 710
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
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- Foliennummer 1
- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
27
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin 711
IT and Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth 712
from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234ndash1246 713
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits 714
of jasmonate-dependent defenses against vertebrate herbivores in nature Elife 5 e13720 715
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root 716
Induction and Flavonoid Profiles in Rumex crispus Advances in Life Sciences 5 (3) 53ndash717
57 718
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of 719
Experimental Botany ers091 720
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and 721
in the gall forming larvae of Eurosta solidaginis New Phytologist 151 (1) 203ndash212 722
Mapes CC and Davies PJ (2001b) Indole‐3‐acetic acid and ball gall development on 723
Solidago altissima New Phytologist 151 (1) 195ndash202 724
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M 725
Hanada A Yaeno T Shirasu K and Yao H (2011) The main auxin biosynthesis 726
pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 727
18512ndash18517 728
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory‐activated MAP 729
kinases SIPK and WIPK does not increase Nicotiana attenuatas susceptibility to 730
herbivores in the glasshouse and in nature New Phytologist 181 (1) 161ndash173 731
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings 732
(Pisum sativum L) the inhibition of transport by 2 3 5-triiodobenzoic acid Planta 110 733
(2) 173ndash182 734
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) 735
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature 736
500 (7463) 422ndash426 737
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT 738
(2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated 739
herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785ndash798 740
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) 741
MYB8 controls inducible phenolamide levels by activating three novel 742
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco Journal of Chemical Ecology 15 (5) 1661-1680
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
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28
hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant 743
Physiology 158 (1) 389ndash407 744
Paschold A Halitschke R and Baldwin IT (2007) Co (i)‐ordinating defenses 745
NaCOI1 mediates herbivore‐induced resistance in Nicotiana attenuata and reveals the 746
role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79ndash91 747
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and 748
Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin 749
production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 750
43 (3) 293ndash298 751
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and 752
Xie D (2011) The Jasmonate-ZIM-domain proteins interact with the WD-753
RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin 754
accumulation and trichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 755
1795ndash1814 756
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the 757
shoot into the root inhibits lateral root development in Arabidopsis Plant Physiology 118 758
(4) 1369ndash1378 759
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on 760
auxin transport by suspension-cultured crown gall cells Planta 144 (2) 173ndash178 761
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong 762
X and Jaillais Y (2012) COP1 mediates the coordination of root and shoot growth by 763
light through modulation of PIN1-and PIN2-dependent auxin transport in Arabidopsis 764
Development 139 (18) 3402ndash3412 765
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) 766
lsquoReal timersquogenetic manipulation a new tool for ecological field studies The Plant Journal 767
76 (3) 506ndash518 768
Schaumlfer M Meza‐Canales ID Bruumltting C Baldwin IT and Meldau S (2015) 769
Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 770
(NaCHK2)‐and NaCHK3‐mediated perception modulate herbivory‐induced defense 771
signaling and defenses in Nicotiana attenuata New Phytologist 772
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr 773
die Gallenbildung Zool Jb Physiol 74 54ndash87 774
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
6
8
Control 3 6
0
1
2
3
Con
trol
W+W
W+F
AC
s
Con
trol
W+W
W+F
AC
s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
4
C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
Time after W+OS-induction (s)IA
A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
6
05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
300
400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
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Baldwin IT Zhang Z-P Diab N Ohnmeiss TE McCloud ES Lynds GY and Schmelz EA (1997) Quantificationcorrelations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 (4) 397-404
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Bartlett L and Connor EF (2014) Exogenous phytohormones and the induction of plant galls by insects Arthropod-PlantInteractions 8 (4) 339-348
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Bhalerao RP Ekloumlf J Ljung K Marchant A Bennett M and Sandberg G (2002) Shoot-derived auxin is essential for earlylateral root emergence in Arabidopsis seedlings The Plant Journal 29 (3) 325-332
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Bonaventure G Schuck S and Baldwin IT (2011) Revealing complexity and specificity in the activation of lipase-mediatedoxylipin biosynthesis a specific role of the Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis inleaves and roots Plant cell amp environment 34 (9) 1507-1520
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Borevitz JO Xia Y Blount J Dixon RA and Lamb C (2000) Activation tagging identifies a conserved MYB regulator ofphenylpropanoid biosynthesis The Plant Cell 12 (12) 2383-2393
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Chen Q Sun J Zhai Q Zhou W Qi L Xu L Wang B Chen R Jiang H and Qi J (2011) The basic helix-loop-helixtranscription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cellniche in Arabidopsis The Plant Cell 23 (9) 3335-3352
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Connor EF Bartlett L OToole S Byrd S Biskar K and Orozco J (2012) The mechanism of gall induction makes galls redArthropod-Plant Interactions 6 (4) 489-495
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Dafoe NJ Thomas JD Shirk PD Legaspi ME Vaughan MM Huffaker A Teal PE and Schmelz EA (2013) Europeancorn borer (Ostrinia nubilalis) induced responses enhance susceptibility in maize PloS one 8 (9)
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Dahl CC von and Baldwin IT (2004) Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonateburst in Nicotiana attenuata Physiologia Plantarum 120 (3) 474-481
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Dahl CC von Winz RA Halitschke R Kuumlhnemann F Gase K and Baldwin IT (2007) Tuning the herbivore-inducedethylene burst the role of transcript accumulation and ethylene perception in Nicotiana attenuata The Plant Journal 51 (2) 293-307
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DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp gene expression is inhibited by auxin PlantPhysiology 104 (2) 439-444
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29
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H 775
and Tumlinson JH (2003) Simultaneous analysis of phytohormones phytotoxins and 776
volatile organic compounds in plants Proceedings of the National Academy of Sciences 777
100 (18) 10552ndash10557 778
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced 779
by mechanical wounding is regulated by auxin Journal of Experimental Botany 57 (11) 780
2899ndash2907 781
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I 782
(2015) Identification of genes that may regulate the expression of the transcription factor 783
production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis 784
anthocyanin biosynthesis Plant cell reports 34 (5) 805ndash815 785
Song Y (2014) Insight into the mode of action of 2 4‐dichlorophenoxyacetic acid (2 4‐D) 786
as an herbicide Journal of integrative plant biology 56 (2) 106ndash113 787
Steppuhn A Gaquerel E and Baldwin IT (2010) The two α-dox genes of Nicotiana 788
attenuata overlapping but distinct functions in development and stress responses BMC 789
plant biology 10 (1) 171 790
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT 791
in Nicotiana attenuata creating a metabolic sink has tissue-specific consequences for the 792
jasmonate metabolic network and silences downstream gene expression Plant Physiology 793
157 (1) 341ndash354 794
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis 795
(Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones Journal 796
of Plant Interactions 5 (3) 197ndash203 797
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall 798
induction by a gall-inducing sawfly Biosci Biotechnol Biochem 77 1942ndash1948 799
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in 800
wounded sweet potato root tissues Plant and cell physiology 20 (6) 1087ndash1095 801
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated 802
responses and plant resistance to pathogens and insects Ecology 85 (1) 48ndash58 803
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the 804
sensitivity of progressive multiple sequence alignment through sequence weighting 805
position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22) 806
4673ndash4680 807
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
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0
2
4
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8
Control 3 6
0
1
2
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Con
trol
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W+F
AC
s
Con
trol
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s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
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a
b
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0
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C
ontro
l
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+W
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+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
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4
Control 15 30 60 180
aa a
bb
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A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
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020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
20
30
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
c
b
a
c
Elongated
0
2
4
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05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
5
10
0123
0
2
4
Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
c
Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
005
115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
1
2
YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
800
1200
1600
0
10
20
30
40
0 45 90
IAA Control
a
ba
b
A
b
a
A
B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
3
4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
1
2
3
4
5
6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
W+W
W+O
SM
sex
taIA
AM
eJA
IAA+
MeJ
A
P lt 0001
0
4
8
12
16
Con
trol
W+O
SC
ontro
lW
+OS
Con
trol
W+O
SC
ontro
lW
+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
1
2
3
Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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0
15
30
45
60
75
90
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
0
100
200
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400
500
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Con
trol
IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
120
180
240
300
360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
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Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
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Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
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Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
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Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
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Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
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Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
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Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
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Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
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Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
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Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
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Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
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Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
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Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
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Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
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Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
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van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
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Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
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Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
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Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
30
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline 808
in endogenous indole-3-acetic acid Plant Physiology 96 (3) 802ndash805 809
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth 810
by high nitrate supply is correlated with reduced IAA levels in roots Journal of plant 811
physiology 165 (9) 942ndash951 812
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species 813
alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems 814
Arthropod-Plant Interactions 5 (2) 115ndash124 815
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor 816
[Say]) larvae on wheat increases levels of fatty acids and indole-3-acetic acid but not 817
hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2) 818
158ndash165 819
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) 820
Defective long-distance auxin transport regulation in the Medicago truncatula super 821
numeric nodules mutant Plant Physiology 140 (4) 1494ndash1506 822
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of 823
jasmonate metabolism and activation of systemic signaling in Solanum nigrum COI1 and 824
JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640ndash652 825
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of 826
LIPOXYGENASE3-and JASMONATE-RESISTANT46-silenced plants reveal that 827
jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore 828
resistance of Nicotiana attenuata Plant Physiology 146 (3) 904ndash915 829
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal 830
transduction and action in plant stress response growth and development An update to 831
the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021ndash1058 832
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter 833
methylation increases rapidly during vegetative development in transgenic Nicotiana 834
attenuata plants BMC plant biology 13 (1) 99 835
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist 836
herbivore Manduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana 837
attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotine accumulation 838
by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189ndash839
2202 840
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
2
4
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0
1
2
3
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s
Con
trol
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s
3 min 7 min
Treatment P lt 0001Time P = 0570TT P = 0782
IAA
(ng
gFW
)
a
a
b
a
b
c
0
1
2
3
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C
ontro
l
W
+W
W
+OS
3 min
a
a
bP lt 0001
Time after M sextafeeding start (h)
a
b
bP lt 0015
A B
C
W+F
AC
W+F
AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
0
1
2
3
4
Control 15 30 60 180
aa a
bb
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A (n
ggF
W)
P lt 0001
IAA
(ng
gFW
)
IAA
(ng
gFW
)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
0
35
70
0 30 60 90 120
Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
10
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30
0 30 60 90 120
Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
0 30 60 90 120
Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
b
W+OS
Control ab
Early rosette
0
5
10
05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
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Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
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Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
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Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
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Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
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Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
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Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
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Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
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Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
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Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
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Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
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Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
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Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
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van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
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in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
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Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
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Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
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Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
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Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
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Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
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Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
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Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
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Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
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Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
31
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl‐l‐841
isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant 842
defenses against herbivores The Plant Journal 72 (5) 758ndash767 843
Wu J and Baldwin IT (2009) Herbivory‐induced signalling in plants perception and 844
action Plant cell amp environment 32 (9) 1161ndash1174 845
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) 846
The broad‐leaf herbicide 2 4‐dichlorophenoxyacetic acid turns rice into a living trap for a 847
major insect pest and a parasitic wasp New Phytologist 194 (2) 498ndash510 848
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-849
induced defences are highly specific among closely related Nicotiana species BMC plant 850
biology (1) 2 851
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y 852
(2012) Phytohormones and willow gall induction by a gall‐inducing sawfly New 853
Phytologist 196 (2) 586ndash595 854
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p 855
Li J and Deng X-W (2012) Plant hormone jasmonate prioritizes defense over growth 856
by interfering with gibberellin signaling cascade Proceedings of the National Academy of 857
Sciences 109 (19) E1192-E1200 858
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin‐responsive 859
endogenous peptide regulates root development in Arabidopsis Journal of integrative 860
plant biology 56 (7) 635ndash647 861
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) 862
Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting 863
salicylic acid signaling Journal of Chemical Ecology 39 (5) 612ndash619 864
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
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IAA
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gFW
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ontro
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A B
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AC
Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Control 15 30 60 180
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)
IAA
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)
D
Time after treatment Time after treatment
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
020406080
100
0 30 60 90 120
Stem
Time P = 0764Treatment P = 0558TT P = 0093
IAA
(ng
gFW
)
Time after treatment (min)
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Main root
Time P = 0232Treatment P = 0486TT P = 0146 0
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Lateral roots
Time P = 0151Treatment P = 0368TT P = 0514
01234
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Petioles
Time P = 0008Treatment P = 0612TT P = 0122
012345
0 30 60 90 120
Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Time after treatment (h)
01020304050
05 1 3
W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
a
b
c
a
b
a
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W+OS
Control ab
Early rosette
0
5
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05 1 3
Time P = 0002Treatment P lt 0001TT P lt 0001
b
a
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Elongated
0
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05 1 3
Time P = 0049Treatment P lt 0001TT P = 0414
a
b
a
a
ab
b
Flowering
IAA
(ng
gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
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0123
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Control 5 60Time after W+OS treatment (min)
YUCCA-like 3
YUCCA-like 9
a
YUCCA-like 3
a
b b
a a
b bP lt 0001
P lt 0001
a
b
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Fold
cha
nge
YUCCA-mediated oxidative decarboxylation
Indole-3-pyruvic acid Indole-3-acetic acid
A
B
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115
YUCCA-like 5
a ab b
P lt 0001
C
E
G
0
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YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
Time after W+OS treatment (min)
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
IAA
(ng
gFW
) JA (nggFW)
0
400
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1600
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10
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30
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0 45 90
IAA Control
a
ba
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a
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B BJA Control
Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
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4
C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
a
c
ba a
b
a a
b
a a
b
a a
b
IAA
(ng
gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
1
2
3
4
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6
-1 0 1 2 3 4 5
Ste
m a
ntho
cyan
in c
onte
nt (micro
mol
gFW
)
Stem color
plt0001
M sexta
W+OSIAA+MeJA
W+WMeJAControl
IAA
0
1
2
3
4
5
Con
trol
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sex
taIA
AM
eJA
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MeJ
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P lt 0001
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16
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SC
ontro
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+OS
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ontro
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+OS
Lanolin L-Kyn TIBA IAA Petiole pretreatment
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
Leaf treatment
0
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Con
trol
W+O
SC
ontro
lW
+OS
EV irAOC
Genotype P lt 0001Treatment P lt 0001GT P lt 0001
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
0
15
30
45
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Con
trol
IAA
Con
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IAA
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Control W+W W+OS M sexta MeJA
0
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IAA
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IAA
Control W+W W+OS M sexta MeJA
Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
03
06
09
12
15
18
mg
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0431 LTPPT P = 0888
ns
ns
ns
ns
ns
nsns
ns
ns
ns
0
60
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360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
FWmicrog
gFW
Petiole pretreatment
Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Parsed CitationsAgtuca B Rieger E Hilger K Song L Am Robert C Erb M Karve A and Ferrieri RA (2014) Carbon-11 reveals opposingroles of auxin and salicylic acid in regulating leaf physiology leaf metabolism and resource allocation patterns that impact rootgrowth in Zea mays Journal of plant growth regulation 33 (2) 328-339
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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Figure 1 Indole-3-acetic acid (IAA) is induced specifically and rapidly by real and simulated M sextaattack Average (plusmnSE) IAA levels in leaves that are attacked by M sexta caterpillars (A) treated with Msexta oral secretions (B C) or treated with an herbivore elicitor (D) (n=5) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
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Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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020406080
100
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Stem
Time P = 0764Treatment P = 0558TT P = 0093
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gFW
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Time P = 0232Treatment P = 0486TT P = 0146 0
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Time P = 0151Treatment P = 0368TT P = 0514
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Time P = 0008Treatment P = 0612TT P = 0122
012345
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Systemic leaves
Time P = 0361Treatment P = 0072TT P = 0445
05
101520
0 30 60 90 120
Local leaves
Time P = 0131Treatment P lt 0001TT P = 0085
ControlW+OS
A B
C D
E F
Figure 2 Herbivory induces IAA both locally and systemically Average (plusmnSE) IAA levels followingsimulated M sexta attack in local treated leaves (A) and in untreated petioles (B) stem (C) systemicleaves (D) main root (E) and lateral roots (F) (n=5) Asterisks indicate significant differences betweentreatments within plant tissues and time points ( P lt 005 P lt 0001) Control intact plantsW+OS wounded and M sexta oral secretion-treated plants
10 10
10
1010
10
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Time after treatment (h)
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W+W
Time P lt 0001Treatment P lt 0001TT P = 0036
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gFW
)
A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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0
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Control 5 60Time after W+OS treatment (min)
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a a
b bP lt 0001
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Indole-3-pyruvic acid Indole-3-acetic acid
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a ab b
P lt 0001
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G
0
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YUCCA-like 6P = 0001 b
a
b
a
D
P lt 0001
Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
012345
Control 5 60
YUCCA-like 1
a
b
c
F
P lt 0001
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a
ba
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Time after treatment (min)
Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
5
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0
1
2
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C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
a a
b
a a
b
a a
b
a a
b
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ba a
b
a a
b
a a
b
a a
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IAA
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gFW
)
Genotype P lt 0001Treatment P lt 0001GT P = 0113
Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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0
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-1 0 1 2 3 4 5
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m a
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onte
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mol
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+OS
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+OS
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trol
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ontro
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+OS
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Genotype P lt 0001Treatment P lt 0001GT P lt 0001
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m a
ntho
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in c
onte
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(microm
olg
FW)
Ste
m a
ntho
cyan
in c
onte
nt
(microm
olg
FW)
A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
onte
nt
Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P = 0004
Nicotine
DTGsP
eak
area
103
gFW
Leaf treatment P lt 0001Petiole pretreatment P = 0800LTPPT P = 0968
0
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ns
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microgg
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gFW
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A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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Time after treatment (h)
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A B C
Figure 3 IAA induction in leaves occurs across different developmental stages Average (plusmnSE) IAAlevels in local treated leaves following simulated M sexta attack at the early rosette (A) elongated (B)and flowering stage (C) (n=5) Different letters indicate significant differences between treatments withindevelopmental stages and time points (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants
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a ab b
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YUCCA-like 6P = 0001 b
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
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Early JA-signaling JA-biosynthesis JA-Ile-perception
Wild type
Impaired in
JA-Ile-biosynthesis
Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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+OS
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+OS
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A B
C D
Control M sexta
Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Caffeoylputrescine
Dicaffeoylspermidine
Ste
m c
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Nicotine
DTGsP
eak
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gFW
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ns
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360 Leaf treatment P lt 0001Petiole pretreatment P lt 0001LTPPT P lt 0001
microgg
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Leaf treatment
A C
B D
Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Figure 4 YUCCA-like genes are upregulated in response to simulated M sexta herbivory (A)Schematic representation of YUCCA-mediated conversion of indole-3-pyruvic acid into IAA Average(plusmnSE) transcript abundance relative to control of YUCCA-like 3 (B) YUCCA-like 5 (C) YUCCA-like 6(D) and YUCCA-like 9 (E) in treated leaves three minutes after elicitation and YUCCA-like 1 (F) andYUCCA-like 3 (G) 5 and 60 min following simulated M sexta attack (n=3) Different letters indicatesignificant differences between treatments (P lt 005) Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants W+FACs wounded and fattyacid-amino acid conjugate-treated plants
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Figure 5 Manduca sexta-induced IAA peaks earlier than jasmonic acid (JA) Left Y-axis average (plusmnSE)leaf IAA levels in response to M sexta attack Right Y-axis average (plusmnSE) leaf JA levels in response toM sexta attack Closed squares IAA levels upon W+OS treatments closed triangles IAA levels incontrol untreated plants Grey squares JA levels upon W+OS treatments grey triangles jasmonic acid(JA) levels in control untreated plants (n=5) Different letters indicate significant differences betweentreatments for individual metabolites (P lt 005) IAA Time P = 0015 treatment P lt 0001 Timetreatment P = 0638 JA Time P lt 0001 treatment P lt 0001 Time treatment P lt 0001) Controlintact plants W+OS wounded and M sexta oral secretion-treated plants
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C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS C W OS
EV irSIPK irWIPK irGLA irAOS irAOC irOPR3 irJAR46 irCOI1
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Figure 6 Jasmonate signaling is not required for the M sexta-induced accumulation of IAA (A)Average (plusmnSE) IAA levels in local treated leaves of wild type plants (empty vector EV) and plantgenotypes impaired in early JA signaling jasmonate biosynthesis andor JA-Ile perception 45 minutesafter elicitation (n=5) Different letters indicate significant differences between treatments within eachgenotype (P lt 005) C control intact plants W wounded and water-treated plants OS wounded andM sexta oral secretions-treated plants
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Figure 7 Manduca sexta-induced IAA and JA act synergistically to trigger anthocyanin accumulation in thestems (A) Average (plusmnSE) stem anthocyanin content 5 days following either simulated or continuous M sextaattack exogenous application of methyl jasmonate (MeJA) andor IAA (n=5) (B) Average (plusmnSE) stemanthocyanin content 5 days following simulated M sexta attack and petiole-pretreatments with either IAA theIAA biosynthesis inhibitor L-kynurenine (L-Kyn) or the IAA transport inhibitor TIBA (235-triiodobenzoic acid)(n=12) (C) Average (plusmnSE) stem anthocyanin contents following simulated M sexta attack of wild type and JA-impaired irAOC plants (n=10) (D) Correlation between stem anthocyanin content and stem coloration InsetPhotograph of the red stem phenotype Asterisks indicate significant differences between treatments and control(A) between simulated herbivory treatments within petiole pretreatments (B) and between treatments withingenotypes (C) ( P lt 005 P lt 001 P lt 0001) The correlation between stem coloration index andstem anthocyanin content was evaluated by a Pearson product moment test Leaf treatments Control intactplants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants Msexta plants subjected to actual M sexta attack IAA rosette leaves treated with indole-3-acetic acid MeJArosette leaves treated with methyl jasmonic acid IAA+MeJA rosette leaves treated with IAA and MeJA Petiolepretreatments Petioles treated with either pure lanoline paste (Lanoline) L-kynurenine (L-Kyn) 235-triiodobenzoic acid (TIBA) or indole-3-acetic acid (IAA) dissolved in lanoline 1h prior to leaf treatments
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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Figure 8 IAA specifically potentiates the herbivore-induced systemic production of phenolamides Average (plusmnSE) caffeoylputrescine (A) dicaffeoylspermidine (B) nicotine (C) and diterpene glycoside (D) levels in the stems 5 days following simulated or real M sexta attack and petiole pretreatments with IAA (n=5) Asterisks indicate significant differences between petiole pretreatments within simulated M sexta attack treatments ( P lt 005 P lt 001 P lt 0001) Petiole pretreatments Control petioles treated with pure lanoline paste 1h prior to leaf treatments IAA petioles treated with IAA dissolved in lanoline 1h prior to leaf treatments Leaf treatments Control intact plants W+W wounded and water-treated plants W+OS wounded and M sexta oral secretion-treated plants M sexta plants subjected to actual M sexta attack MeJA rosette leaves treated with methyl jasmonic acid dissolved in lanoline paste
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DeWald DB Sadka A and Mullet JE (1994) Sucrose modulation of soybean Vsp gene expression is inhibited by auxin PlantPhysiology 104 (2) 439-444
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Diezel C Allmann S and Baldwin IT (2011a) Mechanisms of optimal defense patterns in Nicotiana attenuata Floweringattenuates herbivory-elicited ethylene and jasmonate Signaling Journal of integrative plant biology 53 (12) 971-983
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Diezel C Kessler D and Baldwin IT (2011b) Pithy protection Nicotiana attenuatas jasmonic acid-mediated defenses arerequired to resist stem-boring weevil larvae Plant Physiology 155 (4) 1936-1946
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Dorchin N Hoffmann JH Stirk WA NOVAacuteK O Strnad M and van Staden J (2009) Sexually dimorphic gall structurescorrespond to differential phytohormone contents in male and female wasp larvae Physiological Entomology 34 (4) 359-369
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Erb M Meldau S and Howe GA (2012) Role of phytohormones in insect-specific plant reactions Trends in plant science 17(5) 250-259
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Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A Hernaacutendez M and Peacuterez JA (2007) Cloning and biochemicalcharacterization of ToFZY a tomato gene encoding a flavin monooxygenase involved in a tryptophan-dependent auxinbiosynthesis pathway Journal of plant growth regulation 26 (4) 329-340
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Expoacutesito-Rodriacuteguez M Borges AA Borges-Peacuterez A and Peacuterez JA (2011) Gene structure and spatiotemporal expressionprofile of tomato genes encoding YUCCA-like flavin monooxygenases the ToFZY gene family Plant Physiology and Biochemistry49 (7) 782-791
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Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer)
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-acetic acid in sections of maize coleoptilesPlanta 155 (1) 68-75
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Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular interactions between the specialist herbivoreManduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana attenuata VI Microarray analysis reveals that mostherbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates Plant Physiology 131 (4) 1894-1902
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Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth promoting substances Botanical Gazette735-807
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He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in ArabidopsisThe Plant Cell 23 (11) 3944-3960
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Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B Jassbi AR and Baldwin IT (2010)Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpeneglycosides an abundant and effective direct defense against herbivores in Nicotiana attenuata The Plant Cell 22 (1) 273-292
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Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles from Cucurbita pepo L Planta 157 (3) 193-201
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Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZsDevelopmental cell 19 (6) 884-894
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Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant Biol 59 41-66Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W (2015) Synthesis structural characterization andbiological activity of two diastereomeric JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885-5893
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Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal that acts independently of ethylene signalingon leaf abscission in Populus Frontiers in plant science 6 634
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Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT (2012) Empoasca leafhoppers attack wild tobaccoplants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations Proceedings of the NationalAcademy of Sciences 109 (24) E1548-E1557
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Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairsjasmonic acid-isoleucine-mediated defenses against Manduca sexta The Plant Cell 18 (11) 3303-3320
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Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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Glick BR (2015) Beneficial Plant-bacterial Interactions (Springer)
Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-acetic acid in sections of maize coleoptilesPlanta 155 (1) 68-75
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Guiscafrearrillaga J (1949) Formation of galls in stems and leaves of sugar cane in response to injections of growth-regulatingsubstances Phytopathology 39 (6) 489-493
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Halitschke R Gase K Hui D Schmidt DD and Baldwin IT (2003) Molecular interactions between the specialist herbivoreManduca sexta (Lepidoptera Sphingidae) and its natural host Nicotiana attenuata VI Microarray analysis reveals that mostherbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates Plant Physiology 131 (4) 1894-1902
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hall TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis program for Windows 9598NT Nucleicacids symposium series (41) 95-98
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hamner KC and Kraus EJ (1937) Histological reactions of bean plants to growth promoting substances Botanical Gazette735-807
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
He W Brumos J Li H Ji Y Ke M Gong X Zeng Q Li W Zhang X and An F (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1TAR activity in ethylene-directed auxin biosynthesis and root growth in ArabidopsisThe Plant Cell 23 (11) 3944-3960
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Heiling S Schuman MC Schoettner M Mukerjee P Berger B Schneider B Jassbi AR and Baldwin IT (2010)Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpeneglycosides an abundant and effective direct defense against herbivores in Nicotiana attenuata The Plant Cell 22 (1) 273-292
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hertel R Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles from Cucurbita pepo L Planta 157 (3) 193-201
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hou X Lee LYC Xia K Yan Y and Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZsDevelopmental cell 19 (6) 884-894
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Howe GA and Jander G (2008) Plant immunity to insect herbivores Annu Rev Plant Biol 59 41-66Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jimenez-Aleman GH Machado RAR Goumlrls H Baldwin IT and Boland W (2015) Synthesis structural characterization andbiological activity of two diastereomeric JA-Ile macrolactones Organic amp biomolecular chemistry 13 (21) 5885-5893
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jin X Zimmermann J Polle A and Fischer U (2015) Auxin is a long-range signal that acts independently of ethylene signalingon leaf abscission in Populus Frontiers in plant science 6 634
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kallenbach M Bonaventure G Gilardoni PA Wissgott A and Baldwin IT (2012) Empoasca leafhoppers attack wild tobaccoplants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations Proceedings of the NationalAcademy of Sciences 109 (24) E1548-E1557
Pubmed Author and Title wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairsjasmonic acid-isoleucine-mediated defenses against Manduca sexta The Plant Cell 18 (11) 3303-3320
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in vitro and in vivo Plant Physiology 91 (1) 73-78
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactivejasmonates in Arabidopsis The Plant Journal 59 (6) 974-986
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin transport velocities Trends in plant science 16 (9)461-463
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of aphids with caterpillar-induced defenses inArabidopsis Involvement of phytohormones and transcription factors Plant and cell physiology pcu150
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotianaattenuata a model ecological expression system Chemoecology 12 (4) 177-183
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia phytofirmans-induced shoot and root growthpromotion is associated with endogenous changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199-207
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic acid a reciprocal signalling molecule in bacteria-plant interactions evolution 54 59
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris weevils distinguish amongst toxic host plants bysensing volatiles that do not affect larval performance Molecular ecology
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF Winkel BSJ and Muday GK (2011) Auxin andethylene induce flavonol accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144-164
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) Prioritizing plant defence over growth throughWRKY regulation facilitates infestation by non-target herbivores Elife 4 e04805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome-wide alternative splicing responses in Nicotianaattenuata The Plant Journal 84 (1) 228-243
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 1545-1556
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and bioactive compounds from adventitious roots byoptimization of culturing conditions of Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience andbioengineering 119 (6) 712-717
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate-dependent depletion of soluble sugarscompromises plant resistance to Manduca sexta New Phytologist 207 (1) 91-105
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin IT and Erb M (2013) Leaf-herbivore attackreduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234-1246
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits of jasmonate-dependent defenses againstvertebrate herbivores in nature Elife 5 e13720
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root Induction and Flavonoid Profiles inRumex crispus Advances in Life Sciences 5 (3) 53-57
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of Experimental Botany ers091Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurostasolidaginis New Phytologist 151 (1) 203-212
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001b) Indole-3-acetic acid and ball gall development on Solidago altissima New Phytologist 151(1) 195-202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M Hanada A Yaeno T Shirasu K and Yao H(2011) The main auxin biosynthesis pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 18512-18517
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory-activated MAP kinases SIPK and WIPK does not increaseNicotiana attenuatas susceptibility to herbivores in the glasshouse and in nature New Phytologist 181 (1) 161-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings (Pisum sativum L) the inhibition oftransport by 2 3 5-triiodobenzoic acid Planta 110 (2) 173-182
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediateleaf-to-leaf wound signalling Nature 500 (7463) 422-426
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT (2010) Jasmonic acid and ethylene modulatelocal responses to wounding and simulated herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785-798
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) MYB8 controls inducible phenolamide levels wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
by activating three novel hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant Physiology 158 (1)389-407
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paschold A Halitschke R and Baldwin IT (2007) Co (i)-ordinating defenses NaCOI1 mediates herbivore-induced resistance inNicotiana attenuata and reveals the role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79-91
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and Vinceri FF (2005) The effect of growthregulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 43(3) 293-298
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral rootdevelopment in Arabidopsis Plant Physiology 118 (4) 1369-1378
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on auxin transport by suspension-culturedcrown gall cells Planta 144 (2) 173-178
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr die Gallenbildung Zool Jb Physiol 7454-87
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
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Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
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Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
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Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
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Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
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van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
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in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
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Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
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Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
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Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
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Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
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Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
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Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
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Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
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Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
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wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
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CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kang J-H Wang L Giri A and Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairsjasmonic acid-isoleucine-mediated defenses against Manduca sexta The Plant Cell 18 (11) 3303-3320
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kernan A and Thornburg RW (1989) Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in vitro and in vivo Plant Physiology 91 (1) 73-78
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koo AJK Gao X Daniel Jones A and Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactivejasmonates in Arabidopsis The Plant Journal 59 (6) 974-986
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kramer EM Rutschow HL and Mabie SS (2011) AuxV a database of auxin transport velocities Trends in plant science 16 (9)461-463
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kroes A van Loon JJA and Dicke M (2014) Density-dependent interference of aphids with caterpillar-induced defenses inArabidopsis Involvement of phytohormones and transcription factors Plant and cell physiology pcu150
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kruumlgel T Lim M Gase K Halitschke R and Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotianaattenuata a model ecological expression system Chemoecology 12 (4) 177-183
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kurepin LV Park JM Lazarovits G and Bernards MA (2015) Burkholderia phytofirmans-induced shoot and root growthpromotion is associated with endogenous changes in plant growth hormone levels Plant Growth Regulation 75 (1) 199-207
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lambrecht M Okon Y Broek AV and Vanderleyden J (2000) Indole-3-acetic acid a reciprocal signalling molecule in bacteria-plant interactions evolution 54 59
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lee G Joo Y Diezel C Lee EJ Baldwin IT and Kim S (2016) Trichobaris weevils distinguish amongst toxic host plants bysensing volatiles that do not affect larval performance Molecular ecology
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lewis DR Ramirez MV Miller ND Vallabhaneni P Ray WK Helm RF Winkel BSJ and Muday GK (2011) Auxin andethylene induce flavonol accumulation through distinct transcriptional networks Plant Physiology 156 (1) 144-164
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li R Zhang J Li J Zhou G Wang Q Bian W Erb M and Lou Y (2015) Prioritizing plant defence over growth throughWRKY regulation facilitates infestation by non-target herbivores Elife 4 e04805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Z Zhou W Baldwin IT and Xu S (2015) Insect herbivory elicits genome-wide alternative splicing responses in Nicotianaattenuata The Plant Journal 84 (1) 228-243
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu Y Ahn J-E Datta S Salzman RA Moon J Huyghues-Despointes B Pittendrigh B Murdock LL Koiwa H and Zhu-Salzman K (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase Plant Physiology 139 (3) 1545-1556
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and bioactive compounds from adventitious roots byoptimization of culturing conditions of Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience andbioengineering 119 (6) 712-717
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate-dependent depletion of soluble sugarscompromises plant resistance to Manduca sexta New Phytologist 207 (1) 91-105
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin IT and Erb M (2013) Leaf-herbivore attackreduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234-1246
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits of jasmonate-dependent defenses againstvertebrate herbivores in nature Elife 5 e13720
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root Induction and Flavonoid Profiles inRumex crispus Advances in Life Sciences 5 (3) 53-57
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of Experimental Botany ers091Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurostasolidaginis New Phytologist 151 (1) 203-212
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001b) Indole-3-acetic acid and ball gall development on Solidago altissima New Phytologist 151(1) 195-202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M Hanada A Yaeno T Shirasu K and Yao H(2011) The main auxin biosynthesis pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 18512-18517
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory-activated MAP kinases SIPK and WIPK does not increaseNicotiana attenuatas susceptibility to herbivores in the glasshouse and in nature New Phytologist 181 (1) 161-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings (Pisum sativum L) the inhibition oftransport by 2 3 5-triiodobenzoic acid Planta 110 (2) 173-182
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediateleaf-to-leaf wound signalling Nature 500 (7463) 422-426
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT (2010) Jasmonic acid and ethylene modulatelocal responses to wounding and simulated herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785-798
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) MYB8 controls inducible phenolamide levels wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
by activating three novel hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant Physiology 158 (1)389-407
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paschold A Halitschke R and Baldwin IT (2007) Co (i)-ordinating defenses NaCOI1 mediates herbivore-induced resistance inNicotiana attenuata and reveals the role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79-91
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and Vinceri FF (2005) The effect of growthregulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 43(3) 293-298
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral rootdevelopment in Arabidopsis Plant Physiology 118 (4) 1369-1378
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on auxin transport by suspension-culturedcrown gall cells Planta 144 (2) 173-178
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr die Gallenbildung Zool Jb Physiol 7454-87
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
Lulu T Park S-Y Ibrahim R and Paek K-Y (2015) Production of biomass and bioactive compounds from adventitious roots byoptimization of culturing conditions of Eurycoma longifolia in balloon-type bubble bioreactor system Journal of bioscience andbioengineering 119 (6) 712-717
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Arce C Ferrieri AP Baldwin IT and Erb M (2015) Jasmonate-dependent depletion of soluble sugarscompromises plant resistance to Manduca sexta New Phytologist 207 (1) 91-105
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR Ferrieri AP Am Robert C Glauser G Kallenbach M Baldwin IT and Erb M (2013) Leaf-herbivore attackreduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling New Phytologist 200 (4) 1234-1246
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Machado RAR McClure M Herveacute M Baldwin IT and Erb M (2016) Benefits of jasmonate-dependent defenses againstvertebrate herbivores in nature Elife 5 e13720
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mahdieh M Noori M and Hoseinkhani S (2015) Studies of in vitro Adventitious Root Induction and Flavonoid Profiles inRumex crispus Advances in Life Sciences 5 (3) 53-57
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mano Y and Nemoto K (2012) The pathway of auxin biosynthesis in plants Journal of Experimental Botany ers091Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurostasolidaginis New Phytologist 151 (1) 203-212
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mapes CC and Davies PJ (2001b) Indole-3-acetic acid and ball gall development on Solidago altissima New Phytologist 151(1) 195-202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mashiguchi K Tanaka K Sakai T Sugawara S Kawaide H Natsume M Hanada A Yaeno T Shirasu K and Yao H(2011) The main auxin biosynthesis pathway in Arabidopsis Proceedings of the National Academy of Sciences 108 (45) 18512-18517
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meldau S Wu J and Baldwin IT (2009) Silencing two herbivory-activated MAP kinases SIPK and WIPK does not increaseNicotiana attenuatas susceptibility to herbivores in the glasshouse and in nature New Phytologist 181 (1) 161-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Morris DA Kadir GO and Barry AJ (1973) Auxin transport in intact pea seedlings (Pisum sativum L) the inhibition oftransport by 2 3 5-triiodobenzoic acid Planta 110 (2) 173-182
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mousavi SAR Chauvin A Pascaud F Kellenberger S and Farmer EE (2013) GLUTAMATE RECEPTOR-LIKE genes mediateleaf-to-leaf wound signalling Nature 500 (7463) 422-426
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaacutelis I Dahl CC von Matsuoka K Saluz H-P and Baldwin IT (2010) Jasmonic acid and ethylene modulatelocal responses to wounding and simulated herbivory in Nicotiana attenuata leaves Plant Physiology 153 (2) 785-798
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Onkokesung N Gaquerel E Kotkar H Kaur H Baldwin IT and Galis I (2012) MYB8 controls inducible phenolamide levels wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
by activating three novel hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant Physiology 158 (1)389-407
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paschold A Halitschke R and Baldwin IT (2007) Co (i)-ordinating defenses NaCOI1 mediates herbivore-induced resistance inNicotiana attenuata and reveals the role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79-91
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and Vinceri FF (2005) The effect of growthregulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 43(3) 293-298
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral rootdevelopment in Arabidopsis Plant Physiology 118 (4) 1369-1378
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on auxin transport by suspension-culturedcrown gall cells Planta 144 (2) 173-178
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr die Gallenbildung Zool Jb Physiol 7454-87
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
by activating three novel hydroxycinnamoyl-coenzyme A polyamine transferases in Nicotiana attenuata Plant Physiology 158 (1)389-407
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paschold A Halitschke R and Baldwin IT (2007) Co (i)-ordinating defenses NaCOI1 mediates herbivore-induced resistance inNicotiana attenuata and reveals the role of herbivore movement in avoiding defenses The Plant Journal 51 (1) 79-91
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pasqua G Monacelli B Mulinacci N Rinaldi S Giaccherini C Innocenti M and Vinceri FF (2005) The effect of growthregulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures Plant Physiology and Biochemistry 43(3) 293-298
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Qi T Song S Ren Q Wu D Huang H Chen Y Fan M Peng W Ren C and Xie D (2011) The Jasmonate-ZIM-domainproteins interact with the WD-RepeatbHLHMYB complexes to regulate Jasmonate-mediated anthocyanin accumulation andtrichome initiation in Arabidopsis thaliana The Plant Cell 23 (5) 1795-1814
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Reed RC Brady SR and Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral rootdevelopment in Arabidopsis Plant Physiology 118 (4) 1369-1378
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rubery PH (1979) The effects of 2 4-dinitrophenol and chemical modifying reagents on auxin transport by suspension-culturedcrown gall cells Planta 144 (2) 173-178
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sassi M Lu Y Zhang Y Wang J Dhonukshe P Blilou I Dai M Li J Gong X and Jaillais Y (2012) COP1 mediates thecoordination of root and shoot growth by light through modulation of PIN1-and PIN2-dependent auxin transport in ArabidopsisDevelopment 139 (18) 3402-3412
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Bruumltting C Gase K Reichelt M Baldwin I and Meldau S (2013) Real timegenetic manipulation a new tool forecological field studies The Plant Journal 76 (3) 506-518
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlfer M Meza-Canales ID Bruumltting C Baldwin IT and Meldau S (2015) Cytokinin concentrations and CHASE-DOMAINCONTAINING HIS KINASE 2 (NaCHK2)-and NaCHK3-mediated perception modulate herbivory-induced defense signaling anddefenses in Nicotiana attenuata New Phytologist
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schaumlller G (1968) Biochemische Analyse des Aphidenspeichels und seine Bedeutung fuumlr die Gallenbildung Zool Jb Physiol 7454-87
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schmelz EA Engelberth J Alborn HT ODonnell P Sammons M Toshima H and Tumlinson JH (2003) Simultaneousanalysis of phytohormones phytotoxins and volatile organic compounds in plants Proceedings of the National Academy ofSciences 100 (18) 10552-10557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shi Q Li C and Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated byauxin Journal of Experimental Botany 57 (11) 2899-2907
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shin DH Cho M Choi MG Das PK Lee S-K Choi S-B and Park Y-I (2015) Identification of genes that may regulate theexpression of the transcription factor production of anthocyanin pigment 1 (PAP1)MYB75 involved in Arabidopsis anthocyaninbiosynthesis Plant cell reports 34 (5) 805-815 wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
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- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song Y (2014) Insight into the mode of action of 2 4-dichlorophenoxyacetic acid (2 4-D) as an herbicide Journal of integrativeplant biology 56 (2) 106-113
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Steppuhn A Gaquerel E and Baldwin IT (2010) The two a-dox genes of Nicotiana attenuata overlapping but distinct functionsin development and stress responses BMC plant biology 10 (1) 171
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stitz M Gase K Baldwin IT and Gaquerel E (2011) Ectopic expression of AtJMT in Nicotiana attenuata creating a metabolicsink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression PlantPhysiology 157 (1) 341-354
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Straka JR Hayward AR and Emery RN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with highconcentrations of phytohormones Journal of Plant Interactions 5 (3) 197-203
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y Okada K Asami T and Suzuki Y (2013) Phytohormones and willow gall induction by a gall-inducing sawfly BiosciBiotechnol Biochem 77 1942-1948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tanaka Y and Uritani I (1979) Polar transport and content of indole-3-acetic acid in wounded sweet potato root tissues Plantand cell physiology 20 (6) 1087-1095
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thaler JS and Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogensand insects Ecology 85 (1) 48-58
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thompson JD Higgins DG and Gibson TJ (1994) CLUSTAL W improving the sensitivity of progressive multiple sequencealignment through sequence weighting position-specific gap penalties and weight matrix choice Nucleic acids research 22 (22)4673-4680
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Thornburg RW and Li X (1991) Wounding Nicotiana tabacum leaves causes a decline in endogenous indole-3-acetic acid PlantPhysiology 96 (3) 802-805
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tian Q Chen F Liu J Zhang F and Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated withreduced IAA levels in roots Journal of plant physiology 165 (9) 942-951
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011a) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic andabscisic acid in Solidago altissima (Asteraceae) stems Arthropod-Plant Interactions 5 (2) 115-124
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tooker JF and Moraes CM de (2011b) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae on wheat increases levels offatty acids and indole-3-acetic acid but not hormones involved in plant-defense signaling Journal of plant growth regulation 30 (2)158-165
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
van Noorden GE Ross JJ Reid JB Rolfe BG and Mathesius U (2006) Defective long-distance auxin transport regulation wwwplantphysiolorgon June 1 2020 - Published by Downloaded from
Copyright copy 2016 American Society of Plant Biologists All rights reserved
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
in the Medicago truncatula super numeric nodules mutant Plant Physiology 140 (4) 1494-1506Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
VanDoorn A Bonaventure G Schmidt DD and Baldwin IT (2011) Regulation of jasmonate metabolism and activation ofsystemic signaling in Solanum nigrum COI1 and JAR4 play overlapping yet distinct roles New Phytologist 190 (3) 640-652
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang L Allmann S Wu J and Baldwin IT (2008) Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT46-silencedplants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotianaattenuata Plant Physiology 146 (3) 904-915
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wasternack C and Hause B (2013) Jasmonates biosynthesis perception signal transduction and action in plant stressresponse growth and development An update to the 2007 review in Annals of Botany Annals of Botany 111 (6) 1021-1058
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weinhold A Kallenbach M and Baldwin IT (2013) Progressive 35S promoter methylation increases rapidly during vegetativedevelopment in transgenic Nicotiana attenuata plants BMC plant biology 13 (1) 99
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Winz RA and Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (LepidopteraSphingidae) and its natural host Nicotiana attenuata IV Insect-induced ethylene reduces jasmonate-induced nicotineaccumulation by regulating putrescine N-methyltransferase transcripts Plant Physiology 125 (4) 2189-2202
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Woldemariam MG Onkokesung N Baldwin IT and Galis I (2012) Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulatesjasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores The Plant Journal 72 (5) 758-767
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wu J and Baldwin IT (2009) Herbivory-induced signalling in plants perception and action Plant cell amp environment 32 (9)1161-1174
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xin Z Yu Z Erb M Turlings TCJ Wang B Qi J Liu S and Lou Y (2012) The broad-leaf herbicide 2 4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp New Phytologist 194 (2) 498-510
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xu S Zhou W Pottinger S and Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific amongclosely related Nicotiana species BMC plant biology (1) 2
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yamaguchi H Tanaka H Hasegawa M Tokuda M Asami T and Suzuki Y (2012) Phytohormones and willow gall induction bya gall-inducing sawfly New Phytologist 196 (2) 586-595
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang D-L Yao J Mei C-S Tong X-H Zeng L-J Li Q Xiao L-T Sun T-p Li J and Deng X-W (2012) Plant hormonejasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade Proceedings of the National Academyof Sciences 109 (19) E1192-E1200
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang F Song Y Yang H Liu Z Zhu G and Yang Y (2014) An auxin-responsive endogenous peptide regulates rootdevelopment in Arabidopsis Journal of integrative plant biology 56 (7) 635-647
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-
Zhang P-J Li W-D Huang F Zhang J-M Xu F-C and Lu Y-B (2013) Feeding by whiteflies suppresses downstreamjasmonic acid signaling by eliciting salicylic acid signaling Journal of Chemical Ecology 39 (5) 612-619
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon June 1 2020 - Published by Downloaded from Copyright copy 2016 American Society of Plant Biologists All rights reserved
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
- Foliennummer 1
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- Parsed Citations
- Article File
- Figure 1
- Figure 2
- Figure 3
- Figure 4
- Figure 5
- Figure 6
- Figure 7
- Figure 8
- Parsed Citations
-