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The Plant Cell, October 2015 © 2015The American Society of Plant Biologists

10/26/2015

www.plantcell.org/cgi/doi/10.1105/tpc111.tt0411 1

© 2015 American Society of Plant Biologists

STRIGOLACTONES

www.plantcell.org/cgi/doi/10.1105/tpc.109.tt0411


Strigolactones contribute to a devastating form of plant parasitism

Striga are parasitic plants that are the single largest biotic cause of reduced crop yields throughout Africa(> $10 billion per year in yield losses)

StrigaHost

Root parasites

Striga germination is induced by

strigolactones produced by host plant roots

Striga hermonthica

Image source: USDA APHIS PPQ Archive


Strigolactones (SLs) regulate seemingly unrelated events

Striga

Host

Root

AM fungi

SLs inhibit shoot branching

SLs promote associations with arbuscular mycorrhizal

(AM) fungi

SLs promote germination of parasitic Striga plants


Strigolactones inhibit shoot branching

Image courtesy RIKEN

Wild type SL-deficient

In mutant plants unable to make SLs, many more shoot branches grow out


Strigolactones promote beneficial symbiotic interactions

Image courtesy of Mark Brundrett

Symbiotic AM fungi

SLs promotes the symbiotic association with AM fungi. This symbiosis occurs in 80% of land plants and helps them assimilate nutrients from the soil

Arbuscular is derived from Latin for tree (arbor). Mycorrhiza means “fungus root”


Strigolatones promote germination of parasitic Striga seeds

Striga-infested maize field

Their common name is witchweed because the plants appear to be cursed. Typically Striga infestation causes reductions in crop yields of 50 – 100%

Image source USDA APHIS PPQ Archive


Image courtesy RIKEN

What is the

connection between:

•Shoot branching

•Root parasitism, and

•Root symbiosis?


Three seemingly independent topics converged on SLs

Evolution of plant parasitism

Origins of plant / mycorrhizal symbiosis

> 460 mya

Search for branching factor...

1960s – 1970s Purification and

characterization of strigol from roots

1900s - Role of auxin in shoot branching described

1990s – 2000s Branching mutants

described in petunia, pea, Arabidopsis and rice

2008: Strigolactonesinhibit shoot branching

1800s - Recognition of AM fungus / plant

symbiosis

1800s - Host plant factor required for parasitic seed

germination

2005: Strigolactones promote hyphal branching


Strigolactones have been co-opted for various functions

O O

O O OOH

SL’s ancestral function may have

been communication between individuals of the same species (as

pheromones or quormones)

AM fungi

Root parasite

O

O O OH

O

SLs now contribute to communication within an individual (as hormones), and between

individuals of different species (and kingdoms) (as allelochemicals)

See for example Tsuchiya, Y. and McCourt, P. (2012). Strigolactones as small molecule communicators. Mol. BioSyst. 8: 464-469; Delaux, P.-M., et al., (2012). Origin of strigolactones in the green lineage. New Phytol. 195: 857-871; Proust, H., et al., (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development. 138: 1531-1539.


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Lecture Outline

• Synthesis

• Perception and signaling

• Strigolactones in whole-plant processes:– Shoot branching

– Other developmental effects

– Moss colony growth

– Symbiosis

– Germination

• Towards the elimination of Striga parasitism



Synthesis and transport

In a search for stimulators of Strigagermination, strigolactones were purified from cotton roots in 1966 and the chemical structure determined in 1972

Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E., and Egley, G.H. (1966). Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 154: 1189-1190; Reprinted with permission from Cook, C.E., Whichard, L.P., Wall, M., Egley, G.H., Coggon, P., Luhan, P.A., and McPhail, A.T. (1972). Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J. Am. Chem. Soc. 94: 6198-6199.


Strigolactones (SLs) are a small family of compounds

Reprinted from Humphrey, A.J., and Beale, M.H. (2006). Strigol: Biogenesis and physiological activity. Phytochemistry 67: 636-640 with permission from Elsevier; See also Boyer, F.D., et al.. and Rameau, C. (2012). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: 1524-1544.

5-Deoxystrigol

SYNTHESIS

There are many naturally occurring SLs, derived from 5-deoxystrigol


The stimulator of Striga germination derives from the carotenoid pathway

fluridone

MEP pathway

GGPP

phytoene

-carotene

5-deoxystrigol

Carotenoid-deficient mutants do not make germination stimulator

WT WT

mutant mutant

Through the use of maize mutants and enzyme inhibitors, carotenoids were demonstrated to be the precursors of SLs

Matusova, R., Rani, K., Verstappen, F.W.A., Franssen, M.C.R., Beale, M.H., and Bouwmeester, H.J. (2005). The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 139: 920-934.


Genes involved in SL biosynthesis were identified by genetic methods

Reprinted from Booker, J., et al. (2004). MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14: 1232-1238with permission from Elsevier; Morris, S.E., et al. (2001). Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 126: 1205-1213; Ishikawa, S., et al. (2005). Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46: 79-86 by permission of the Japanese Society of Plant Physiologists. Simons, J.L., et al. (2007). Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol. 143: 697-706.

WT max3 WT rms5

Strigolactone-deficient mutants in Arabidopsis,

pea, rice and petunia show similar short, branchy

phenotypes

The MORE AXILLARY GROWTH3 (MAX3), RAMOSUS5 (RMS5) , DWARF17 (D17) and DECREASED APICAL DOMINANCE3 (DAD3) genes all encode a carotenoid cleavage dioxygenase (CCD7)

WT dad3


SL biosynthesis pathway

carlactone

MAX3, D17, RMS5, DAD3:

MAX4, D10 ,RMS1, DAD1:

MAX1

STRIGOLACTONES

CCD7

CCD8

(P450)MAX; ArabidopsisD; riceRMS; peaDAD; petunia

These reactions occur

in the plastid

D27 (β-carotene-9-isomerase)

Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200.; Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. (2012) Recent advances in strigolactone research: chemical and biological aspects. (in press). Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.


D27 encodes an Fe-binding enzyme necessary for SL synthesis

Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J. and Wang, Y. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell. 21: 1512-1525.

Wild-type (Shiokari) d27

Strigolactones are detected in exudates of wild-type but not d27 roots

Standard

Wild-type exudate

d27 exudate

The rice D27 is a β-carotene-9-isomerase also

found in other plants


Rice SL biosynthesis mutants are rescued by exogenous SL

Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200;

Control

2nd leaf tiller1st leaf tiller

1 cm

1 cm

WT d10 d17

GR24(1 µM)

d10 and d17 are rescued by exogenous SL

(GR24 is a synthetic SL)WT d10 d17

D17

D10


WT max1 max3 max4

Control

GR24 (5 µM)

Arabidopsis SL biosynthesis mutants are rescued by SL

Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200; Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. (2012) Recent advances in strigolactone research: chemical and biological aspects. (in press).

MAX1

MAX4

MAX3


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MAX1 encodes a P450 enzyme involved in shoot branching

Reprinted from Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449 with permission from Elsevier.

max1WT

MAX1 is expressed throughout the plant, primarily in association with vascular tissuesMAX1


SL synthesis in root or shoot is sufficient to control shoot branching

Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449.

max3WT

max3 ScionRoot

WTmax3WT

Grafts

Reciprocal grafts, in which wild-

type tissue is either the root or

scion, have normal phenotypes;

this says that the branch-

controlling signal can be made in

either tissue, and can move from

root to shoot


Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Developmental Cell 8: 443-449; Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.

An intermediate between MAX4 and MAX1 action can move in the plant

max4max1

max1max4

MAX1

STRIGOLACTONES

MAX4

In this experiment mobile, graft-transmissible intermediate in SL synthesis is produced in max1roots, and converted into SL in max4 shoots

Carlactone is a good candidate as the SL mobile

signalling molecule


Kretzschmar, T., Kohlen, W., Sasse, J., Borghi, L., Schlegel, M., Bachelier, J.B., Reinhardt, D., Bours, R., Bouwmeester, H.J. and Martinoia, E. (2012). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature. 483: 341-344.

WT dad1 (=max4)

PDR1 has been identified as a strigolactone exporter

pdr1

SLs are present in pdr1 root extracts, but not prd1 exudates, supporting its role as a transporter

pdr1 mutants are less colonized by

AM fungi, and stimulate less parasitic seedgermination

Loss-of-function pdr1 mutant show:• increased shoot branching• decreased exudation of SLs • decreased symbiotic interactions


The distribution of PDR1 is consistent with its roles in transport

Reprinted from Sasse, J., Simon, S., Gübeli, C., Liu, G.-W., Cheng, X., Friml, J., Bouwmeester, H., Martinoia, E. and Borghi, L. (2015). Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr. Biol. 25: 647-655 and Ruyter-Spira, C., Al-Babili, S., van der Krol, S. and Bouwmeester, H. (2013). The biology of strigolactones. Trends Plant Sci. 18: 72-83 with permission from Elsevier.

SLs are transported shootward and outward from the root


Synthesis and transport - summary

Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science. 335: 1348-1351.

SLs are derived from carotenoids;Early steps occur in the plastids of root and shoot

carlactone

MAX3, RMS5, D17, DAD3

MAX4, RMS1, D10, DAD1

MAX1

STRIGOLACTONES

(CCD7)

(CCD8)

(P450)MAX; ArabidopsisRMS; peaD; riceDAD; petunia


Carlactone is an SL intermediate (and may be a mobile signal)


Perception and signaling

Reprinted by permission from Macmillan Publishers Ltd: Zhou, F., et al and Wan, J. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.

1. D14 is an α/β-fold hydrolase that

binds SLs

2. D3 is an F-box protein that promotes interaction with the proteasome

3. The interaction between SLs, D14 and D3 leads to degradation of target

proteins including D53 (SMAX)


1. D14 is an α/β-fold hydrolase that binds SLs

\

Loss-of-function d14 mutants are SL insensitive and show increased shoot branching; the orthologous gene in petunia is dad2

Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S. and Kyozuka, J. (2009). d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 50: 1416-1424; Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 22: 2032–2036

Genetic studies Biochemical studies

D14 and DAD2 are α/β-fold hydrolases similar to the GID1 protein involved in gibberellin perception


The α/β-fold hydrolase D14/DAD2 cleaves SL

Nakamura, H., Xue, Y.L., Miyakawa, T., Hou, F., Qin, H.M., Fukui, K., Shi, X., Ito, E., Ito, S., Park, S.H., Miyauchi, Y., Asano, A., Totsuka, N., Ueda, T., Tanokura, M., and Asami, T. (2013). Molecular mechanism of strigolactone perception by DWARF14. Nat Commun. 4: 2613. Seto, Y., and Yamaguchi, S. (2014). Strigolactone biosynthesis and perception. Curr. Opin. Plant Biol. 21: 1-6 with permission from Elsevier.

Hydrolysis


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SL receptors D14/DAD2 are related to the KAI2 karrikin receptors

Conn, C.E., Bythell-Douglas, R., Neumann, D., Yoshida, S., Whittington, B., Westwood, J.H., Shirasu, K., Bond, C.S., Dyer, K.A., and Nelson, D.C. (2015). Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349: 540-543. Reprinted with permission from AAAS.

Karrikins are small molecules present in

smoke that are structurally similar to SLs and can induce seed germination

D14 probably arose from a duplication of KAI2 before the evolution of seed plants


Parasitic Striga make highly-sensitive SL receptors

From Toh, S., Holbrook-Smith, D., Stogios, P.J., Onopriyenko, O., Lumba, S., Tsuchiya, Y., Savchenko, A. and McCourt, P. (2015). Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science. 350: 203-207. Reprinted with permission from AAAS.

The SL receptor gene family is amplified in Striga

ShHTL7 encodes a highly sensitive receptor protein that confers germination sensitivity to SLs in vivo


2. D3, an F-box protein, promotes interaction with the proteasome

GR24(1 µM)

Control

d3WT

MAX2, D3 and RMS4 encode F-box proteins related to those involved in auxin and jasmonate signaling

Auxin receptor

Jasmonate co-receptor

Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200. Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogne, K., Beveridge, C.A., and Rameau, C. (2006). Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol. 142: 1014-1026.


In the presence of SLs, DAD2/D14interacts with D3/MAX2

Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perceptionof the plant branching hormone, strigolactone. Curr Biol. 22: 2032–2036 ;Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A.,Ghisalberti, E.L. and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 108: 8897-8902.

SL concentration-dependent interaction between DAD2 (D14)

and MAX2 (D3)

Pro

tein

inte

ract

ion

Model of SL signal transduction

Note the similarity of this model with those for auxin, jasmonate, salicylate and gibberellin signalling

A current model is that SLs promote the interaction between DAD2/D14 receptor and MAX2/D3,

leading to degradation of a signaling repressor

(D3)


Karrikin signals are transduced in a similar manner as SLs

Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L. and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA. 108: 8897-8902.; Waters, M.T., Nelson, D.C., Scaffidi, A., Flematti, G.R., Sun, Y.K., Dixon, K.W. and Smith, S.M. (2012). Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 139: 1285-1295.

By analogy to SLs, karrikin-binding to KAI2 could promote its interaction with MAX2 and the degradation of repressor proteins

MAX2 is needed for SL

and karrikin signaling


3. Genetic approaches identified D53/SMXLs in SL signalling

Stanga, J.P., Smith, S.M., Briggs, W.R. and Nelson, D.C. (2013). SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163: 318-330. Jiang, L., and Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405. Reprinted by permission from Macmillan Publishers Ltd: Zhou, F. et al.,, and Wan, J. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.

SMAX = Suppressor of MAX2

Loss-of-function smax1mutants suppress SL mutant phenotypes

Gain-of-function dominant d53 mutants show a SL-resistant, branchy phenotype


Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., Wu, F., Mao, H., Dong, W., Gan, L., Ma, W., Gao, H., Chen, J., Yang, C., Wang, D., Tan, J., Zhang, X., Guo, X., Wang, J., Jiang, L., Liu, X., Chen, W., Chu, J., Yan, C., Ueno, K., Ito, S., Asami, T., Cheng, Z., Wang, J., Lei, C., Zhai, H., Wu, C., Wang, H., Zheng, N., and Wan, J. (2013). Reprinted by permission from Macmillan Publishers Ltd: D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.

The D53 protein is a SL signaling repressor. D53 degradation by the proteasome depends on interaction with the D14/DAD2 receptor bound to SL.

D14-SL and D3/MAX2 intermediate interaction between the D53 repressor and the SCF complex.

In Arabidopsis, D14 degradation is induced by SL via a MAX2-dependent proteasome mechanism.

Model: Strigolactone promotes D14-SCFD3-mediated degradation of the

repressor D53


Reprinted by permission from Macmillan Publishers Ltd: Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., Yi, W., Zhao, L., Ma, H., He, Y., Wu, Z., Melcher, K., Qian, Q., Xu, H.E., Wang, Y., and Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405

• D14/DAD2 is an / hydrolyze that binds SL, allowing interactions with the F-box protein D3/MAX2

• D3/MAX2 brings the SCF complex and E2 ubiquitin ligase to D53 for polyubiquitination, and further degradation by the proteasome

• D53 degradation leads to transcriptional activation of SL-target genes

Signaling summary


Strigolactones and whole-plant processes

Seto, Y., Kameoka, H., Yamaguchi, S., and Kyozuka, J. (2012). Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol. 53: 1843-1853 by permission of Oxford University Press.

Strigolactones have diverse roles in the development of vascular plants and moss

This include positive and negative effects


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Strigolactones regulate shoot /root branching and nutrient responses

Reprinted from Brewer, P.B., Koltai, H., and Beveridge, C.A. (2013). Diverse roles of strigolactones in plant development. Mol Plant. 6: 18-28 with permission of Elsevier.

SL mutants produce more shoot and root branches

In nutrient deficiency, elevated SLs repress shoot branching and promote root hair elongation


Strigolactones dampen polar auxin transport (PAT)

Reprinted from Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C., and Leyser, O. (2006). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16: 553-563 with permission from Elsevier; Crawford, S., Shinohara, N., Sieberer, T., Williamson, L., George, G., Hepworth, J., Müller, D., Domagalska, M.A., and Leyser, O. (2010). Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913 reproduced with permission.

SL-deficient plants show increased polar auxin transport

Transported auxin

Auxin

+SLPIN

In shoots, strigolactones promote internalization of PIN

auxin efflux transporters, decreasing polar auxin transport


How do strigolactones

inhibit bud outgrowth?

Goulet, C. and Klee, H.J. (2010). Climbing the branches of the strigolactones pathway one discovery at a time. Plant Physiol. 154: 493-496.


Axillary bud outgrowth is hormonally and environmentally responsive

McSteen, P. (2009). Hormonal regulation of branching in grasses. Plant Physiol. 149: 46-55; Brewer, P.B., Dun, E.A., Ferguson, B.J., Rameau, C., and Beveridge, C.A. (2009). Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol. 150: 482-493.

(Axillla means armpit)

bud• Auxin and SLs

inhibit outgrowth

• Cytokinins (CKs) promote it


SL effect on branching can occur via effects on polar auxin transport

Shinohara, N., Taylor, C., and Leyser, O. (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474.


SL effects on shoot branching can also be auxin-independent

Brewer, P.B., Dun, E.A., Gui, R., Mason, M.G. and Beveridge, C.A. (2015). Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol. 168: 1820-1829.

Transcriptional targets of SLs include BRC1, a transcription factor that represses bud outgrowth


–P+P

Phosphate-starved plants

suppress shoot growth and enhance root growth

Nutrient control of branching


Phosphorous deficiency limits plant growth in much of the world

Image courtesy CIMMYT; FAO (2008)

40 million tonnes per year of phosphate

fertilizer is mined, transported, applied to

farmlands, and in many cases run-off to

contaminate lakes and rivers-P

-P-P

-P


Strigolactones suppress shoot branching in low phosphorous

No.

of o

utgr

owin

gtil

lers

0

1

2

0

0.2

0.4

0.6

Tillering

1st tiller 2nd tiller3rd tiller

epi-5

DS

(ng

gF

W-1

)

P (µM)

600 300 120 60 30 12 06

+P –P

Strigolactone level

Strigolactone synthesis is high and shoot branching is suppressed when phosphate availability is low

Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., and Yamaguchi, S. (2010). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51: 1118-1126.


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In the SL-deficient d10 mutant, branch outgrowth is independent of [P]

(None Detected)0

0.2

0.4

0.6

0

1

2

P (µM)

600 300 120 60 30 12 06

Strigolactone level

3

d10

No.

of o

utgr

owin

g til

lers

0

1

2

0

0.2

0.4

0.6

Tillering

1st tiller 2nd tiller3rd tiller

epi-5

DS

(ng

gF

W-1

)

P (µM)

600 300 120 60 30 12 06

WT

Strigolactone level




carlactone

MAX3/D17 (CCD7)MAX4/D10 (CCD8)

MAX1 (P450)


carotenoid

Low [P] induces SL-related gene expression in shoots and roots


Kohlen, W., et al. (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol. 155: 974-987.

Low [P] lowers branch outgrowth in Arabidopsis, dependent on SLs

Low P SL synthesis

Col-0 max4-1


Furthermore, under low [P], SLs enhance root branching

Ruyter-spira, C., et al. (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another below-ground role for strigolactones? Plant Physiology. 155: 721-734.

Low P SL synthesis

In wild-type plants grown with exogenous auxin, outgrowth of lateral roots is enhanced by SL

SLs, in combination with auxin, may

control plant architecture under

nutrient limiting conditions


These interlocking networks provide for local and systemic responses

For example, hormone crosstalks coordinate shoot’s development in response to nitrogen and phosphate limitation

Low auxinLow SLHigh CK

High bud outgrowth

Low bud outgrowth

High auxinHigh SLLow CK

de Jong, M., George, G., Ongaro, V., Williamson, L., Willetts, B., Ljung, K., McCulloch, H., and Leyser, O. (2014). Auxin andstrigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiol. 166: 384-395


Strigolactones suppress development of adventitious roots

Rasmussen, A., Mason, M.G., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D., Greb, T., Goormachtig, S., Beeckman, T. and Beveridge, C.A. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158: 1976-1987.

A. SL mutants of Arabidopsis show enhanced development of adventitious roots. B. Development of adventitious roots is supressed in wild-type and mutant with SL application in a dose-dependent manner.

A. SL mutants of pea also show enhanced development of adventitious

roots. B-C. Cuttings of wild-type (B) show

development of less adventitious roots than the rms5 synthesis mutant (C).


Strigolactones stimulate auxin-dependent secondary growth

Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Sieberer, T., Sehr, E.M., and Greb, T. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. USA. 108: 20242-20247.

SL mutants show decreased lateral and longitudinal extension of interfascicular cambium-derived tissues (ICD)

WT

max1-1


Strigolactones regulate rice shoot gravitropism via auxin

Sang, D., Chen, D., Liu, G., Liang, Y., Huang, L., Meng, X., Chu, J., Sun, X., Dong, G., Yuan, Y., Qian, Q., Li, J. and Wang, Y. (2014). Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. USA. 111: 11199-11204.

The lazy lamutant is deficient in lateral auxin distribution

The sol1 mutant (suppressor of lazy), is a loss-of-function mutant of the F-box protein D3. SL-deficient mutants have enhanced shoot gravitropism, perhaps due to increased auxin synthesis


Strigolactones stimulate leaf senescence

Reprinted from Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D. and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol. 22: 2032–2036, with permission from Elsevier. Snowden, K.C., Simkin, A.J., Janssen, B.J., Templeton, K.R., Loucas, H.M., Simons, J.L., Karunairetnam, S., Gleave, A.P., Clark, D.G., and Klee, H.J. (2005). The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: 746-759; Ueda, H. and Kusaba, M. (2015). Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol. doi:10.1104/pp.15.00325.

SL mutants show delayed leaf

senescence in petunia and Arabidopsis Exogenous

SLs accelerate senescence


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Strigolactone mutants are more sensitive to abiotic stress

Ha, C.V., Leyva-González, M.A., Osakabe, Y., Tran, U.T., Nishiyama, R., Watanabe, Y., Tanaka, M., Seki, M., Yamaguchi, S., Dong, N.V., Yamaguchi-Shinozaki, K., Shinozaki, K., Herrera-Estrella, L., and Tran, L.S. (2014). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA. 111: 851-856

These results suggest that strigolactones play a positive role in abiotic stress tolerance

control drought


Strigolactones are present in non-vascular plants and some green algae

See Ruyter-Spira, C. and Bouwmeester, H. (2012). Strigolactones affect development in primitive plants. The missing link between plants and arbuscular mycorrhizal fungi? New Phytologist. 195: 730-733. Delaux, P.M., Xie, X., Timme, R.E., Puech-Pages, V., Dunand, C., Lecompte, E., Delwiche, C.F., Yoneyama, K., Becard, G. and Sejalon-Delmas, N. (2012). Origin of strigolactones in the green lineage. New Phytol. 195: 857-871. Tirithel; Christian Fischer

Bryophytes –mosses, liverworts

Lycopods –club mosses

Ferns Gymnosperms Angiosperms

Charales

Chlorophyceae

Plants

Green

algae


Strigolactones regulate moss colony growth

Reproduced with permission from Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogué, F., and Rameau, C. (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539.

In wild-type moss, colony size decreases with increasing colony density

In SL-deficient moss, colony size is insensitive to colony density

SLs act like a quorum-sensing molecule


Model – SLs are diffusible signals that reveal moss density

WT – signals repress growth ccd8∆ – NO signal, no growth repression WT moss at periphery send

signal, ccd8∆ moss in center perceives it and restricts growth

Reproduced with permission from Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogué, F., and Rameau, C. (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539.


SLs in whole plant responses -summary

Reprinted from Smith, Steven M. and Waters, Mark T. (2012). Strigolactones: Destruction-dependent perception? Curr. Biol. 22: R924-R927, with permission from Elsevier.

SLs have pleiotropic effects on plant

development, mediated in part by auxin and

other hormones


Strigolactones promote branching in arbuscular mycorrhizal fungi

Reprinted by permission from Macmillan Publishers Ltd: Akiyama, K., Matsuzaki, K.-i., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827 copyright 2005.

SL

SL

SL

SL

Time Zero Time 24 hours

SLs promote hyphal branching


When AM fungi perceive SLs, they initiate symbiosis with the host plant

Reprinted by permission from Macmillan Publishers Ltd: Parniske, M. (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat. Rev. Microbiol. 6: 763 – 775 copyright 2008.


Both partners benefit from the symbiosis

The fungus gets sugars produced by photosynthesis

The plant gets nitrogen and phosphorus from the soil by way of the symbiotic fungal association

The arbuscule provides a large surface area for nutrient exchange


0 500 1000 1500 2000 25005-deoxystrigol (pg/plant/5 days)

Low Mg

Low Ca

Low K

Low P

Low N

control

SL levels are elevated in sorghum root exudates under low P and N

Courtesy of K. Yoneyama and adapted from Yoneyama, K., Xie, X., Kusumoto, D., Sekimoto, H., Sugimoto, Y., Takeuchi, Y., and Yoneyama, K. (2007). Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227: 125-132.


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The nutrient-effect on SL production is plant-specific

Some non-AM host plant

Leguminous plant

Non leguminous,AM host plant (e.g sorghum)

Low P

Low N

Instead, in low N, leguminous plants enter a symbiosis with

nitrogen-fixing bacteria

SL

SL

SL Or SLOr


–P+P

AM fungi

In nutrient-poor soils: •SL synthesis increases•Shoot branching decreases and root branching increases •AM symbiosis increases

These responses enhance plant

survival under low nutrient conditions


Strigolactones promote germination in parasitic and other plants

Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200 Dörr, I. (1997). How Striga parasitizes its host: a TEM and SEM study. Annals of Botany. 79: 463-472, by permission of Oxford University Press;

O O

O O OOH

Strigolactones were first characterized as inducers of Strigagermination (1960s)


Strigolactones also promote Arabidopsis germination in some conditions

Tsuchiya, Y., Vidaurre, D., Toh, S., Hanada, A., Nambara, E., Kamiya, Y., Yamaguchi, S. and McCourt, P. (2010). A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat .Chem. Biol. 6: 741-749.

Striga seeds show stronger seed dormancy and enhanced germination dependency on SLs

Germination response can be studied in Arabidopsis


Striga species (witchweeds) are serious agricultural pests

•Major cereal crops are infested: corn, sorghum, millet and rice

•70 million hectares are infested

•Food productions for 300 million people are affected

•Financial loss is estimated to be approximately 10 billion USD

•No effective control measure has been developed

Adapted from Ejeta, G. and Gressel, J. (eds) (2007) Integrating new technologies for striga control: towards ending the witch-hunt. World Scientific Publishing, Singapore; Image sources: USDA APHIS PPQ Archive, Florida Division of Plant Industry Archive, Dept Agriculture and Consumer Services.

Witchweed infestation

HeavyModerateLight

Striga asiaticaStriga hermonthica


Parasitism has evolved recently and several times

Reprinted from Westwood, J.H., Yoder, J.I., Timko, M.P., and dePamphilis, C.W. (2010) The evolution of parasitism in plants. Trends Plant Sci. 15: 227-235 with permission from Elsevier.

Some plants are facultative parasites; others, like Striga, obligate parasites. Strigaroots cannot grow normally. The primary root tip forms a haustorium specialized to penetrate host plant roots.


Once attached to the host root, the plant grows and reproduces

Dörr, I. (1997). How Striga parasitizes its host: a TEM and SEM study. Annals of Botany. 79: 463-472, by permission of Oxford University Press; USDA APHIS PPQ Archive; USDA APHIS PPQ Archive

Seedling Flowering Tiny seeds

Mustard

Tobacco

Striga


How can we move towards Striga-resistant crops?

Agricultural practices:•Field treatments•Allelopathic approaches

Genetic approaches: •Modify SL structure: encrypt the signal•Suppress branching in SL-deficient plants

Image courtesy of International Institute of Tropical Agriculture (IITA)


Orobanche (broomrape)-infested carrot field

Photo credit Shmuel Golan courtesy of Yaakov Goldwasser


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Striga asiatica

Image courtesy of Prof. Julie Scholes & Mamadou Cissoko

Rice field infested with Striga


Parasitic plants infect 60% of farmlands in sub-Saharan Africa



Agricultural practices can reduce crop losses from Striga

Photo courtesy Ken Hammond (USDA)

• Before planting, apply germination stimulants to promote “suicidal germination” (no host = no survival)

• Apply fertilizers to reduce SL production by crop plants.

• These methods are prohibitively expensive in many parts of the developing world.


Intercropping with beneficial plants can reduce Striga infestation

Maize intercropped with Desmodium uncinatum

Desmodium is a nitrogen-fixing legume that enriches the soil, and also produces allelopathic chemicals that interfere with Striga parasitism

Hassanali, A., Herren, H., Khan, Z.R., Pickett, J.A. and Woodcock, C.M. (2008). Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Phil. Trans. R. Soc. B 363: 611-621 copyright 2008 The Royal Society.

Desmodium uncinatum


Do all SLs promote Strigagermination and affect branching?

5-Deoxystrigol Orobanchol 2’-epi-orobanchol

Sorgomol SolanacolOrobachyl acetate

Strigyl acetateStrigolSorgolactone

Fabacyl acetate7-oxoorobanchyl acetate

Orobanchyl acetate

A BC

D

There are many different naturally occurring SLs –how does their structure affect their function?


Saturated (3,6'-dihydro-) GR24 isomers do not induce Striga germination

O

O O O

O O

O O O

O O

O O O

O O

O O O

O

Isomer I Isomer II Isomer III Isomer IV

GR24

Enol etherO O

O O O

Isomers of saturated GR24


…but an isomer of saturated GR24 promotes interactions with AM fungi

Adapted from Akiyama, K., Ogasawara, H., Ito, S. and Hayashi, H. (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol., 51: 1104-1117 see also Boyer, F.D., de Saint Germain, A., Pillot, J.P., Pouvreau, J.B., Chen, V.X., Ramos, S., Stevenin, A., Simier, P., Delavault, P., Beau, J.M. and Rameau, C. (2012). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol. 159: 1524-1544.

Can we make synthetic SLs with beneficial but not detrimental effects? YESCan we engineer plants to make these? MAYBE

AM fungi Striga

+++ –O

O O O

O

Saturated GR24

O O

O O O+++ +++GR24


Can we engineer Striga resistance? Rice d10 SL-deficient mutant...

(1) Parasitism

(2) Symbiosis

Root parasite

(3) Shoot branching

O

O O OH

O

O O

O OO

(1) No germination of Strigaseeds around the root

(2) Reduced AM fungi symbiosis（but not fully inhibited）

(3) Too many shoot branches

Are these effects separable?

AM fungi


Can we engineer Striga resistance? Rice d10 SL-deficient mutant...

(1) Parasitism

(2) Symbiosis

Root parasite

(3) Shoot branching

O

O O OH

O

O O

O OO

Modify downstream component

（e.g. d10 suppressor mutants）

Can we normalize shoot branching in SL-deficient mutants?

These experiments are in progress with a goal to producing Striga-resistant plants

(1) No germination of Strigaseeds around the root

(2) Reduced AM fungi symbiosis（but not fully inhibited）

(3) Too many shoot branches

AM fungi


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Summary (1) Perception and signaling

de Saint Germain, A., Bonhomme, S., Boyer, F.D., and Rameau, C. (2013). Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol. 16: 583-589.


Conclusions and future directions

AM fungi

O

O O OH

O

O O

O OO

Strigolactones are synthesized in roots of nutrient-limited plants

SLs enhance AM fungi symbiosis

SLs repress shoot branching and adventitious root formation

SLs stimulate primary root growth, root hair elongation, secondary growth, and leaf senescence


AM fungi

O

O O OH

O

O O

O OO


How do SLs integrate with other hormones and signals to control shoot, root branching and leaf senescence?

Can we modify the SL biosynthesis pathway to alter the types and activities of SLs produced?

What are the evolutionary origins and ancestral functions of SLs?



Photo courtesy CIMMYT

“Striga has a disproportionately large impact on those least equipped to control it, as it thrives in low-fertility soil”- International Maize and Wheat Improvement Center (CIMMYT)

Knowledge of the

production and

effects of SLs gives

us the power to

work towards

eliminating the

devastation of

parasitic Striga

the plant cell, october 2015 © 2015 10/26/2015 the ... · the american society of plant biologists...

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