1 short title: the tomato slmixta-like transcription factor 2 · 6.10.2015 · 1 1 short title:...

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Short title: The Tomato SlMIXTA-like Transcription Factor 1

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Corresponding author: Asaph Aharoni 3

Tel: +972 8 934 3643 4

Email: [email protected] 5

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The Tomato MIXTA-like Transcription Factor Coordinates Fruit Epidermis Conical 7

Cell Development and Cuticular Lipid Biosynthesis and Assembly 8

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Justin Lashbrooke1,2,4, Avital Adato1, Orfa Lotan1, Noam Alkan1,6, Tatiana Tsimbalist1, Katya 10

Rechav5, Josefina-Patricia Fernandez-Moreno1,7, Emilie Widemann3, Bernard Grausem3, 11

Franck Pinot3, Antonio Granell7, Fabrizio Costa2 and Asaph Aharoni1 12

13 1Department of Plant Sciences, Weizmann Institute of Science, PO Box 26, Rehovot, 76100, 14

Israel 15 2Research and Innovation Centre, Foundation Edmund Mach, Via Mach 1, I-38010 San 16

Michele all’Adige, Trento, Italy 17 3Département Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des 18

Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, 19

Université de Strasbourg, 67083, Strasbourg Cedex, France 20 4Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch, 7602, South Africa 21 5Department Of Chemical Research Support, Weizmann Institute of Science, PO Box 26, 22

Rehovot, 76100, Israel 23 6Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural 24

Research Organization, Bet Dagan, 50250, Israel. 25 7Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular 26

de Plantas (CSIC-UPV), Ingeniero Fausto elio s/n, 46022- Valencia, Spain 27

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One sentence summary: 29

A MIXTA-like transcription factor from tomato regulates fruit cutin biosynthesis, and forms 30

part of a regulatory network linking epidermal cell development with cuticle formation. 31

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Plant Physiology Preview. Published on October 6, 2015, as DOI:10.1104/pp.15.01145

Copyright 2015 by the American Society of Plant Biologists

https://plantphysiol.orgDownloaded on December 14, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

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Abstract 33

The epidermis of aerial plant organs is the primary source of building blocks forming the 34

outer surface cuticular layer. To examine the relationship between epidermal cell 35

development and cuticle assembly in the context of fruit surface, we investigated the tomato 36

SlMIXTA-like gene. MIXTA/MIXTA-like proteins, initially described in snapdragon petals, 37

are known regulators of epidermal cell differentiation. Fruit of transgenically silenced 38

SlMIXTA-like tomato plants displayed defects in patterning of conical epidermal cells. They 39

also showed altered postharvest water loss and resistance to pathogens. Transcriptome and 40

cuticular lipids profiling, coupled with comprehensive microscopy, revealed significant 41

modifications to cuticle assembly and suggested SlMIXTA-like to regulate cutin biosynthesis. 42

Candidate genes likely acting downstream of SlMIXTA-like included cytochrome P450s of 43

the SlCYP77A and SlCYP86A subfamilies, SlLACS2, SlGPAT4 and the SlABCG11 cuticular 44

lipids transporter. As part of a larger regulatory network of epidermal cell patterning and L1-45

layer identity, we found that SlMIXTA-like acts downstream of SlSHINE3 and possibly co-46

operates with homeodomain-leucine zipper IV transcription factors. Hence, SlMIXTA-like is 47

a positive regulator of both cuticle and conical epidermal cell formation in tomato fruit, 48

acting as a mediator of the tight association between fruit cutin polymer formation, cuticle 49

assembly and epidermal cell patterning. 50

Key words: Cuticle, epidermal cell, fruit, L1-layer, MIXTA, tomato, transcriptional 51

regulation. 52

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3

Introduction 54

The epidermal layer of plants is a multifunctional and diverse tissue. Epidermal cells interact 55

directly with the surrounding environment, and as such are involved in a number of 56

processes, including osmotic regulation, defense and pollinator attraction (Glover, 2000; 57

Martin and Glover, 2007; Whitney et al., 2009). In order to optimally perform these 58

functions, cells of the epidermis are differentiated into a variety of cell types. For the above 59

ground parts of plants this typically includes pavement cells, trichomes and stomata guard 60

cells. Each of these cell types may be further differentiated, resulting in a range of more 61

subtle variations and morphological shapes. An excellent example of this subtle variation can 62

be seen in the conical cell shape of petal epidermal cells (Whitney et al., 2009; Whitney et al., 63

2011). The widespread occurrence of these conical petal epidermal cells in nature has been 64

associated with petal color, petal reflection, scent production, petal wettability and pollinator 65

grip on the flower surface (Neinhuis and Barthlott, 1997; Riederer and Muller, 2006; 66

Whitney et al., 2009). 67

One of the major evolutionary developments of land plants was the formation of the 68

cuticular membrane (or cuticle) found to the exterior of the source of its building blocks, the 69

epidermis layer. The cuticle provides a waterproof barrier between epidermal cells and the 70

comparatively dry external environment (Riederer and Muller, 2006). It also plays an 71

important role in the protection of plants against biotic and abiotic stresses such as pathogen 72

attack and damaging UV light (Bargel et al., 2006). Recent research has highlighted the 73

cuticle as an important element in the plant’s detection and transmission of osmotic stress 74

signals (Wang et al., 2011). The cuticle is comprised of a polymerized cutin matrix embedded 75

with waxes (Kolattukudy, 2001). In many fleshy fruit, including Solanum lycopersicum 76

(tomato), the major monomer of the cutin matrix is the C16-9/10, 16-dihydroxy fatty acid 77

(DiHFA) (Mintz-Oron et al., 2008). A number of the enzymatic steps for the biosynthesis, 78

extracellular transport and polymerization of the cutin matrix have been described in 79

Arabidopsis, and to some extent in tomato. In short, free fatty acids (FFA) are synthesized in 80

the chloroplast, transported to the endoplasmic reticulum, and subsequently modified. 81

Modification includes mid- and terminal-chain hydroxylation and CoA-activation followed 82

by transfer to a glycerol moiety. Enzymes responsible for these steps include long-chain acyl-83

CoA synthetases (LACSs), (Schnurr et al., 2004; Jessen et al., 2011), oxidases (CYP86A and 84

CYP77A), (Li-Beisson et al., 2009; Pinot and Beisson, 2011; Shi et al., 2013) and 85

acyltransferases (GPATs and likely DCR), (Panikashvili et al., 2009; Rani et al., 2010; Yang 86



4

et al., 2010; Yang et al., 2012). The resultant monoacylglycerols undergo extracellular 87

transport and finally polymerization to form the cutin matrix. Enzymes responsible for these 88

steps include ATP-binding-cassette (ABC) transporters (Bird et al., 2007; Bessire et al., 2011; 89

Panikashvili et al., 2011) and cutin synthases (GDSL/CUSs and BDG (Kurdyukov et al., 90

2006; Girard et al., 2012; Yeats et al., 2012; Yeats et al., 2014). 91

Interestingly, the characterization of mutants and transgenic plants altered in cuticle 92

assembly revealed a major effect on the patterning of epidermis cells. Arabidopsis mutants 93

for cyp77a6 and gpat6 both exhibit a lack of cuticular nanoridges as well as petals with flatter 94

epidermal cells (Li-Beisson et al., 2009). The lack of cuticular nanoridges was also observed 95

in dcr Arabidopsis mutants (Panikashvili et al., 2009), while Arabidopsis mutants for genes 96

possibly responsible for cutin synthesis, bdg and gdsl, show changes to epidermal cell shape 97

(Kurdyukov et al., 2006). Study of transcriptional regulators further revealed a tight 98

relationship between the cuticle and epidermal cell. It appears that a number of reported 99

regulators of epidermal cell differentiation and cuticle biosynthesis are closely related 100

proteins belonging to the same gene families (Hen-Avivi et al., 2014). Of particular interest 101

in this regard are transcription factors from the SHN1/WIN1 clade of the APETELA2 (AP2)-102

domain superfamily, the homeodomain-leucine zipper IV (HD-ZIP IV) and R2-R3 MYB 103

factors families. Members of the HD-ZIP IV family were shown to regulate cuticle 104

metabolism in tomato and maize including CUTIN DEFICIENT2 (CD2), (Isaacson et al., 105

2009; Nadakuduti et al., 2012) and OUTER CELL LAYER1 (OCL1), (Javelle et al., 2010; 106

Depège-Fargeix et al., 2011), respectively. Other HD-ZIP IV proteins including AtGL2 107

(Rerie et al., 1994; Ishida et al., 2007; Tominaga-Wada et al., 2009; Tominaga-Wada et al., 108

2013), AtPDF2 (Abe et al., 2003), AtHDG11 (Nakamura et al., 2006), ATML1 (Abe et al., 109

2003; Takada et al., 2013), and GhHD-1 (Walford et al., 2012), were demonstrated to be 110

involved in the regulation of epidermal cell differentiation. Two members of the 111

SHN1/WIN1 clade of transcription factors from Arabidopsis and tomato (AtSHN1 and 112

SlSHN3, respectively), have been shown to be required for both cutin biosynthesis as well as 113

epidermal cell patterning (Aharoni et al., 2004; Broun et al., 2004; Shi et al., 2011; Shi et al., 114

2013). Finally, members of the R2R3 MYB transcription factor superfamily, AtMYB41 and 115

AtMYB96, have also been shown to regulate wax deposition during abiotic stress (Cominelli 116

et al., 2008; Seo et al., 2011), although more recent results suggest that AtMYB41 likely 117

promotes suberin biosynthesis and deposition (Kosma et al., 2014). 118

Members of the MYB protein family termed MIXTA or MIXTA-like were shown to 119

be key regulators of epidermal cell differentiation across multiple plants species (Martin and 120



5

Glover, 2007; Brockington et al., 2013). Orthologs of the MIXTA/MIXTA-like clade have 121

been reported specifically to act as positive regulators of conical epidermal cell formation 122

(Noda et al., 1994; Baumann et al., 2007; Di Stilio et al., 2009), trichome development 123

(Perez-Rodriguez et al., 2005; Gilding and Marks, 2010; Plett et al., 2010) and cotton fiber 124

development (Machado et al., 2009; Walford et al., 2011). Recently Arabidopsis MIXTA-like 125

orthologs, AtMYB16 and AtMYB106, were demonstrated to regulate cuticle development 126

(Oshima et al., 2013). To date however, MIXTA/MIXTA-like clade genes were not 127

characterized with relation to fleshy fruit surface. In a recent work characterizing SlSHN3 128

activity in tomato, it was suggested that this transcription factor may exert its influence on 129

epidermal cell patterning through HD-ZIP IV and/or MIXTA transcription factors (Shi et al., 130

2013). While expression of a tomato MIXTA-like gene (i.e. SlMIXTA-like) was shown earlier 131

to be enriched in the epidermal tissue throughout tomato fruit development (Mintz-Oron et 132

al., 2008), its functional role in tomato fruit surface was not examined. 133

In this work we functionally characterize the tomato SlMIXTA-like gene through the 134

detailed investigation of lines with transgenically silenced SlMIXTA-like expression. Our 135

findings show that SlMIXTA-like not only promotes conical epidermal cell development in 136

tomato fruit, but is a major positive regulator of cuticular lipids, more specifically cutin 137

monomer biosynthesis as well as cuticle assembly. This is apparent from the wide range of 138

down-regulated cutin biosynthetic genes in tomato lines silenced for SlMIXTA-like 139

expression, as well as the notable correlation between SlMIXTA-like expression and the 140

deposition of cuticle. Thus, this study further advances the understanding of co-regulation 141

between epidermal cell patterning and cuticle biosynthesis during organ formation. 142

143

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6

Results 145

The Tomato Genome Contains a Single Expressed Member of the MIXTA/MIXTA-like 146

Gene Family that is Predominantly Expressed in the Fruit Epidermal Layer 147

Analysis of the tomato genome via BLAST searches using well characterized MIXTA and 148

MIXTA-like proteins from Antirrhinum majus and Petunia hybrida (AmMIXTA (Noda et al., 149

1994) and PhMYB1 (Baumann et al., 2007), respectively) as input, identified a number of 150

potential tomato orthologs of this clade. Molecular phylogenetic analysis of the best hits 151

revealed that the tomato genome retains seven potential orthologs to the clade containing 152

MIXTA and MIXTA-like proteins (R2R3-MYB group 9) (Supplemental Fig. S1) (Stracke et 153

al., 2001; Brockington et al., 2013). This group of MYB factors also includes MYB17 154

proteins, with which two of the tomato candidates (Solyc01g094360 and Solyc05g048830) 155

group. These candidates can therefore be ruled out as potential MIXTA/MIXTA-like 156

orthologs (Supplemental Fig. S1). Of the remaining five candidates, four group separately 157

from both the MYB17 and the MIXTA/MIXTA-like branch (Solyc01g010910, 158

Solyc04g005600, Solyc05g007690 and Solyc05g007710) and may be considered a novel 159

group (Supplemental Fig. S1). These four genes show no expression in previously generated 160

large scale multi-organ expression data (Itkin et al., 2013) and thus were not investigated 161

further. The final identified candidate (Solyc02g088190) groups in the MIXTA-like branch of 162

the phylogenetic tree (Supplemental Fig. S1). This protein termed SlMIXTA-like, shares 75% 163

and 80% amino acid identity with the well characterized MIXTA-like epidermal cell 164

differentiation factors, AmMYBML2 and PhMYB1, respectively (Baumann et al., 2007). A 165

molecular phylogenetic tree for all previously characterized MIXTA and MIXTA-like 166

proteins showed that SlMIXTA-like groups with MIXTA-like orthologs (Fig. 1A). Previous 167

results have demonstrated that SlMIXTA-like has enriched transcript levels in the surface 168

layers of fruit (Mintz-Oron et al., 2008; Shi et al., 2013). Quantitative Real Time-PCR (qRT-169

PCR) analysis of SlMIXTA-like expression in five stages of tomato fruit development in skin 170

(epidermal enriched) and flesh tissues revealed that while expression levels were highest in 171

the skin at the immature green stage of fruit development, expression remained high in this 172

tissue throughout development (Mintz-Oron et al., 2008). SlMIXTA-like transcripts in the skin 173

were found to be at least 16-fold higher than in flesh at all measured stages of development. 174

Examination of publically available large-scale gene expression data for various fruit cell-175

types (Matas et al., 2011), revealed that SlMIXTA-like expression is predominantly detected 176

in the outer- and inner-epidermis of the fruit, albeit to a lesser extent in the latter (Fig. 1B). 177



7

The inner epidermal layer of tomato fruit separates the locular region from the pericarp. A 178

very low level of SlMIXTA-like expression was detected in the collenchyma tissue and none 179

in the vasculature and parenchyma. Additionally, the expression profile of SlMIXTA-like 180

across 20 tomato tissues (Itkin et al., 2013) showed that while fruit transcripts were enriched 181



8

in the skin (at all 5 stages of fruit development examined), significant expression could be 182

detected in petals, buds and pollen (Fig. 1C). 183

184

Silencing of SlMIXTA-like Results in the Flattening of Epidermal Cells and a Thinner 185

Cuticle in Tomato Fruit 186

To investigate the function of SlMIXTA-like in tomato fruit surface development, silenced 187

(SlMIXTA-RNAi) lines were generated (Fig. 2). SlMIXTA-RNAi tomato lines exhibited a 188

variety of phenotypes at the vegetative stage, including retarded growth and smaller, crinkled 189

and curled leaves (Fig. 2, B and C). Fruit of the SlMIXTA-RNAi plants appeared glossier than 190

wild-type fruits, and were subsequently subject for detailed investigation. 191

A variety of microscopy techniques were employed to investigate the changes in the 192

surface morphology of the tomato lines with reduced SlMIXTA-like expression. Initial 193

observations by light microscopy and lipid staining (using Sudan IV stain) revealed 194

significantly less cuticle deposition in the fruit of SlMIXTA-RNAi lines throughout 195

development and what appeared to be flatter epidermal cells (Fig. 3). While in wild type 196

tomato the cuticle frequently surrounds the entire epidermal cell (Mintz-Oron et al., 2008; 197

Matas et al., 2011), SlMIXTA-RNAi fruit displayed almost no sub-epidermal staining (Fig. 3, 198

A and B). Cryo-scanning electron microscopy (Cryo-SEM) and atomic force microscopy 199

(AFM) confirmed the change in cell shape and a concomitant change in the surface 200

morphology of the tomato fruit (Fig. 3, C and D). Analysis by AFM revealed a disrupted and 201

rough micro-surface (Fig. 3D; Supplemental Fig. S3). Transmission electron microscopy 202

(TEM) illustrated the typical conical shape of tomato fruit epidermal cells in wild-type and 203

confirmed that lines silenced for SlMIXTA-like expression possessed flatter cells (Fig. 3E). 204

In order to more deeply investigate cell shape, Focused Ion Beam Scanning Electron 205

Microscopy (FIB-SEM) was employed. This technique is able to produce a three-dimensional 206

(3D) image with the resolution typical of electron microscopy. Briefly, a biological sample is 207

repeatedly milled (via the FIB) and then imaged (via the SEM), producing hundreds of SEM 208

images from a few microns of tissue. These images can then be stacked (in silico) and the 3D 209

structure of the observed specimen elucidated. In the case of the analysis of epidermal cells 210

from ripe tomato fruit, wild-type fruit clearly possessed conical epidermal cells while the 211

epidermal cells from SlMIXTA-RNAi lines were considerably flatter (Fig. 4; Supplemental 212

Movie S1; Supplemental Movie S2). 213

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9

SlMIXTA-like Expression is Positively Correlated with the Accumulation of Cutin 215

Monomers in Tomato Fruit Cuticle 216



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Analysis of enzymatically isolated cuticles from fruit altered in SlMIXTA-like expression 217

revealed a positive correlation between SlMIXTA-like expression and cuticle mass (Table 1; 218

Supplemental Dataset S2). Cuticles isolated from SlMIXTA-RNAi fruit displayed a lower 219

mass compared to wild-type cuticles. Deeper chemical analysis via gas chromatography-mass 220



11

spectrometry (GC-MS) was performed to determine which elements of the cuticle were 221

contributing to the observed change in mass. The overall cutin monomer abundance was 222

significantly altered in the SlMIXTA-RNAi lines (down 27%; Table 1). Quantification of the 223

total cuticular waxes from the tomato lines revealed no significant change (Supplemental 224



12

Table S1). The change in cutin monomers was underlined by the significant reduction of 225

aromatics, dicarboxylic fatty acids (DFA), and mid-chain and terminal-hydroxylated fatty 226

acids (ω-HFA) in the SlMIXTA-RNAi lines (Fig. 5; Table 1). No significant change was 227



13

observed in the accumulation of the saturated fatty acids in the different genotypes examined 228

(Table 1). 229

230

Silencing of SlMIXTA-like Results in the Down-regulation of a Wide Spectrum of Cutin 231

Biosynthesis and Assembly Genes 232

Further investigation of the SlMIXTA-like RNAi lines identified a pertinent array of gene 233

expression changes in the fruit skin. Global expression analysis via microarrays and 234

quantitative real time-PCR (qRT-PCR) assays for validation revealed a considerable down-235

regulation of cutin biosynthesis genes in the skin of SlMIXTA-RNAi fruit at the mature green 236

stage (Table 2; Supplemental Dataset S1; Supplemental Fig. S4). The mature green stage of 237

fruit development was selected for gene expression analysis as at this stage the skin and flesh 238

are more easily separated when compared with the earlier stages of development, and cuticle 239

biosynthesis genes are still strongly enriched (Mintz-Oron et al., 2008). Mining the 240

microarray data to identify genes with at least 2-fold change (p-value ≤ 0.05), generated a 241

relatively concise list of 93 down-regulated and 153 up-regulated genes in the SlMIXTA-242

RNAi fruit skin as compared to wild-type (Supplemental Dataset S1). Gene ontology (GO) 243

enrichment analysis of the 93 down-regulated genes revealed significant enrichment for lipid 244

metabolism, specifically fatty acid and lignin biosynthesis (p-value < 0.01). Among the 93 245

down-regulated genes, 13 orthologs of genes previously functionally characterized and 246

associated with cuticle assembly were annotated (Fig. 5; Table 2). Due to the fact that 247

SlSHN3 has been shown via promotor binding assays to act upstream of SlMIXTA-like (Shi et 248

al., 2013), the initial list of down-regulated genes was further extended via qRT-PCR analysis 249

of candidates previously shown to be down-regulated in SlSHN3-RNAi lines (Shi et al., 250

2013) but not detected in the SlMIXTA-RNAi microarray experiment either due to not being 251

present on the array or due to expression levels below the background of detection. In total 17 252

genes putatively involved in cuticle biosynthesis and assembly were identified to be down-253

regulated in SlMIXTA-RNAi lines (Table 2). It is also important to note that qRT-PCR 254

confirmed no significant change in expression of SlSHN3, SlCD2, SlPDF2d, SlDCR and 255

SlCD1 (Supplemental Fig. S4). 256

Of the 17 cuticle-associated down-regulated genes, fourteen could be linked to 257

various steps of cutin biosynthesis and assembly (Fig. 5). These consisted of two long chain 258

acyl-CoA synthase coding genes (SlLACS2 and SlLACS4) putatively involved in the acyl 259

activation of fatty acids (Fig. 5). Orthologs to these genes have been demonstrated to be 260



14

required for normal cuticle development in Arabidopsis: AtLACS1, AtLACS2 and AtLACS4 261

(Schnurr et al., 2004; Jessen et al., 2011). Three CYP450s were identified, SlCYP77A1 and 262

SlCYP77A2 and SlCYP86A68 (Fig. 5; Table 2). Orthologs of CYP77A have been 263

demonstrated to be responsible for the mid-chain hydroxylation of C16 fatty acids during 264

cutin biosynthesis (Li-Beisson et al., 2009) while CYP86A orthologs have been shown to 265

catalyze the terminal hydroxylation of free fatty acids (Han et al., 2010; Shi et al., 2013). 266

Another candidate for the modification of fatty acids is the down-regulated SlHTH gene. The 267

Arabidopsis ortholog, AtHTH, has been shown to be crucial for the formation of dicarboxylic 268

fatty acids (Kurdyukov et al., 2006). The final step in the biosynthesis of cutin monomers is 269

acyl transfer of the activated fatty acid to a glycerol moiety. This reaction is catalyzed by 270

AtGPAT4 and BnGPAT4 in Arabidopsis (Li et al., 2007) and Brassica napus (Chen et al., 271

2011), respectively. The tomato ortholog to these genes (SlGPAT4) was down-regulated in 272

SlMIXTA-RNAi lines (Fig. 5; Table 2). The monoacylglycerols formed through the action of 273

the enzymes described above are subsequently transported to the exterior of the cell before 274

polymerization occurs (Pollard et al., 2008). SlMIXTA-RNAi lines showed down-regulation 275

of two extracellular transporter genes: SlABCG11 and SlABCG32. SlABCG11 is orthologous 276

to the characterized cutin and wax monomer transporter in Arabidopsis, AtABCG11 (Bird et 277

al., 2007; Panikashvili et al., 2007), while SlABCG32 is the tomato ortholog to AtABCG32 an 278

extracellular transporter of cuticle components (Bessire et al., 2011). Finally, five genes 279

potentially involved in the extracellular polymerization of the cutin matrix were found to be 280

down-regulated in the SlMIXTA-RNAi lines (Fig. 5; Table 2). Three orthologs to the tomato 281

CD1 gene, recently reported to be an extracellular cutin polymerase (Girard et al., 2012; 282

Yeats et al., 2012), were also down-regulated in the SlMIXTA-RNAi lines (Solyc07g049440 283

Solyc03g121180 and Solyc04g081770), as well as two α/β-hydrolases (Solyc09g075140 and 284

Solyc05g054330), orthologous to the Arabidopsis AtBDG suggested to be an extracellular 285

synthase required for cutin formation (Kurdyukov et al., 2006). 286

Only two out of the 17 cuticle-associated genes down-regulated in the SlMIXTA-287

RNAi lines could putatively be linked to wax biosynthesis (Solyc03g117800 and 288

Solyc11g072990). The Arabidopsis ortholog of Solyc03g117800, AtCER3, has been reported 289

to be catalyze the conversion of very long chain acyl-CoAs to very long chain alkanes 290

(Bernard et al., 2012), while the ortholog of Solyc11g072990, AtKCS3, catalyzes the first 291

step of fatty acid elongation (Millar et al., 1999). 292

293



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Putative SlMIXTA-like Downstream Targets Display an L1 Layer-specific Enrichment 294

In silico promoter analysis of the genes identified to be down-regulated in SlMIXTA-RNAi 295

lines revealed a significant enrichment (p < 0.01) for the L1-box motif -TAAATGYA- (Table 296

2; Supplemental Dataset S1). This motif has previously been demonstrated to be the binding 297

site for two L1-specific HD-ZIP transcriptional regulators in Arabidopsis, AtPDF2 and 298

ATML1 (Abe et al., 2003; Takada et al., 2013). In the SlMIXTA-RNAi lines an ortholog to 299

these genes, SlGL2 (Solyc03g120620), was demonstrated to be down-regulated (Table 2). 300

The 93 down-regulated genes were also analyzed for their L1 layer specificity by comparison 301

with a recently generated data set (Filippis et al., 2013). In this work 255 genes out of the 302

13,277 examined were identified to exhibit L1 layer-specific tomato expression. Of the 303

reported 255 L1 layer-specific gene set, 18 genes were found to be down-regulated in the 304

SlMIXTA-RNAi lines (Table 2; Supplemental Dataset S1). Hypergeometric analysis 305

demonstrates this is an extremely strong enrichment (p < 0.01), and further suggests a role for 306

SlMIXTA-like in L1 layer-specific gene control. By comparison, of the 153 up-regulated 307

genes in the SlMIXTA-RNAi lines only three are reportedly L1 layer-specific, showing no 308

enrichment (p = 0.57). 309

The previous observation that SlMIXTA-like possessed a fruit skin associated 310

expression profile (Mintz-Oron et al., 2008; Shi et al., 2013), was further confirmed by the 311

data extracted from recently generated large scale transcriptomic analysis of multiple tomato 312

tissues (Itkin et al., 2013), (Fig. 1C). The hypothesis that putative downstream targets of 313

SlMIXTA-like will likely exhibit a similar L1 layer-specific expression pattern was tested by 314

extracting the expression patterns of the SlMIXTA-RNAi down-regulated genes in skin and 315

flesh tissues from the dataset, and performing hierarchical clustering (Fig. 6). Data for 91 316

genes was collected and four major clusters were identified, the largest cluster (Cluster IV) 317

contained SlMIXTA-like and 40 other genes (Fig. 6; Table 2; Supplemental Dataset S1). 318

Cluster IV had a high homogeneity (r-value = 0.81), and displayed skin enriched (or L1 319

layer-specific) expression pattern particularly in the early stages of fruit development (Fig. 6). 320

All of the 16 genes described as potential SlMIXTA-like targets involved in cuticle 321

biosynthesis were found to be part of Cluster IV. The expanded expression profiles (including 322

seed, leaf, flower and root expression data) of genes described in this report can be seen in 323

Supplemental Fig. S5. 324

Finally, of the 143 genes found to be up-regulated in the microarray analysis, one 325

gene was of particular interest and displayed a dramatic up-regulation in SlMIXTA-RNAi 326



16

lines. An HD-ZIP IV transcription factor, SlANL2b (Solyc06g035940), was up-regulated 327

43-fold (Supplemental Dataset S1). SlANL2b is a close ortholog in tomato to the cuticle 328

regulating SlCD2 gene (Isaacson et al., 2009; Nadakuduti et al., 2012), and significantly also 329

an ortholog to the epidermis and L1 layer related transcription factors, PROTODERMAL 330



17

FACTOR 2 (AtPDF2) and ARABIDOPSIS THALIANA MERISTEM LAYER 1 (ATML1) 331

(Supplemental Fig. S6). 332

333

Putative SlMIXTA-like Downstream Target Genes Encode Members of the Cytochrome 334

P450 CYP77A and CYP86A Subfamilies Catalyzing the Formation of Major Cutin 335

Monomers in Tomato 336

Members of the cytochrome P450 CYP77A and CYP86A subfamilies have been reported 337

previously to be involved in cutin monomers biosynthesis (largely in Arabidopsis), 338

performing mid-chain and terminal oxidation of fatty acids, respectively (Li-Beisson et al., 339

2009). As three members of these subfamilies were identified here as putative SlMIXTA-like 340

downstream targets (Fig. 5; Table 2; Supplemental Fig. S7) we explored the activity of the 341

corresponding recombinant enzymes through expression in yeast cells. Initial incubation of a 342

variety of fatty acids with microsomes of yeast expressing the three CYPs (SlCYP77A1, 343

SlCYP77A2 and SlCYP86A68) confirmed that they were all active enzymes able to catalyze 344

hydroxylation of fatty acids (Fig. 7; Supplemental Fig. S8). More extensive analysis of 345

SlCYP77A1 demonstrated the enzyme was able to hydroxylate C16:0 fatty acids (Fig. 7). To 346

determine the position of the hydroxylation, we performed mass spectrometry analysis on the 347

recombinant SlCYP77A1 assay products and revealed a mixture of 11,16-; 10,16-; 9,16- and 348

8,16-dihydroxyhexadecanoic acids (Fig. 7C). This result corresponds strongly with the 349

reduced levels of 9/10,16-dihydroxyhexadecanoic acid in fruit of the SlMIXTA-RNAi lines. 350

351

Silencing of SlMIXTA-like Increased Postharvest Fruit Water Loss and Susceptibility to 352

Postharvest Fungal Infection 353



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Post-harvest analysis of SlMIXTA-RNAi fruit revealed that reduced expression of SlMIXTA-354

like resulted in an increase in postharvest water loss as well as increased susceptibility to 355

fungal infection (Fig. 8). Fruit of SlMIXTA-RNAi lines lost 80% more water than those from 356

WT lines over 30 days after harvest (Fig. 8A). Similarly, the susceptibility to post harvest 357

fungal infection was significantly higher in SlMIXTA-RNAi lines. Fruit at the breaker stage 358



19

were inoculated with the tomato fruit pathogen Colletotrichum coccodes, which causes black 359

dot anthracnose disease (Dillard, 1989). Despite no significant difference in the rate of 360

conidia germination and appressoria formation on the surface of WT and SlMIXTA-RNAi 361

fruit (Supplemental Fig. S9), a 5-fold increase in the decay diameter after 1 week of 362

inoculation was observed on SlMIXTA-RNAi fruit (Fig. 8B). 363



20

364

365



21

Discussion 366

SlMIXTA-like Forms Part of a Transcriptional Network Regulating the Development of 367

Conical Epidermal Cells in Tomato Fruit 368

To date, MIXTA orthologs across a variety of plant species have been reported to be involved 369

in the regulation of epidermal cell differentiation (Brockington et al., 2013). The earliest 370

characterized MIXTA ortholog (AmMIXTA) was shown to promote conical epidermal cell 371

development in the petals of Antirrhinum majus (Noda et al., 1994; Brockington et al., 2013). 372

Subsequently, members of the MIXTA transcription factor clade from Arabidopsis, 373

Thalictrum thalictroides and Petunia hybrida were also reported to regulate conical 374

epidermal cell development (Baumann et al., 2007; Di Stilio et al., 2009), while orthologs 375

from Arabidopsis, Populus trichopoda, Mimulus guttatus, A. majus, Medicago trunculata and 376

Dendrobium crumenatum have been shown to be positive regulators of trichome 377

development (Perez-Rodriguez et al., 2005; Gilding and Marks, 2010; Plett et al., 2010; 378

Scoville et al., 2011). Phylogenetic analysis showed that the SlMIXTA-like protein 379

characterized here is most closely related to the Petunia PhMYB1 ortholog which has been 380

reported to regulate conical epidermal cell differentiation in petals (Baumann et al., 2007) 381

(Fig. 1A). Four additional tomato proteins were identified through genome analysis and 382

appeared related to the MIXTA/MIXTA-like clade, however phylogenetic analysis found 383

these proteins to be distinct from MIXTA/MIXTA-like orthologs (Supplemental Fig. S1). 384

This relationship was not investigated in more detail as no expression was detected for these 385

genes in previously published large-scale expression studies (Itkin et al., 2013). It is possible 386

that these genes are non-expressed pseudogenes that are no longer under selective pressure to 387

maintain activity. 388

The prevalence of conical epidermal cells in flower petals suggests an important role 389

for this particular morphology, likely the attraction of pollinators; however, the mode of 390

action for this attraction is not obvious. Research into this question has shown that the 391

reflection of light by the epidermal cells of petals is significantly altered by cell morphology 392

(Gorton and Vogelmann, 1996), and this likely plays a role in pollinator attraction, however 393

more recent research has shown that pollinators are able to discriminate between petal 394

surfaces via tactile sensation (Whitney et al., 2009). The conical epidermal cells of petals 395

likely facilitate the physical interaction between pollinators and flowers (Whitney et al., 396

2009). In contrast to petals, the abundance of this morphology in fleshy fruit surface has 397

received less attention. As in the case of petals, the conical cells in fruit likely play a role in 398



22

the reflection of light, and therefore may be involved in the attraction of seed dispersal 399

agents. Recent studies confirm earlier reports that change in epidermal cell morphology can 400

dramatically alter the human perceived glossiness of tomato fruit (Isaacson et al., 2009; 401

Mahjoub et al., 2009; Nadakuduti et al., 2012; Shi et al., 2013; Petit et al., 2014), although 402

how these fruit are viewed by seed dispersers is still not known. While no epidermal specific 403

petal phenotype was observed, leaves of SlMIXTA-RNAi lines were small and folded, while 404

fruit were glossier than corresponding wild-type fruit, despite the reduction in cuticle 405

deposition seen in these lines. Morphological examination of tomato fruit silenced for 406

SlMIXTA-like expression revealed a flattening of the epidermal cells which likely leads to the 407

glossier surface as light reflects from the surface with less scattering. 408

The observed enrichment of the L1-box promoter motif (Abe et al., 2001) in the 409

promoters of the genes down-regulated in the SlMIXTA-RNAi lines together with the 410

enrichment of L1 layer-specific genes implicate SlMIXTA-like as a possible central regulator 411

of L1 layer cell identity. This might occur through co-regulation with the HD-ZIP IV 412

transcription factor SlGl2, which is significantly down-regulated in lines silenced for 413

SlMIXTA-like expression and therefore may occur downstream of SlMIXTA-like in this 414

regulatory pathway. The ortholog of SlGL2 in Arabidopsis, AtGL2, is a well characterized 415

regulator of epidermal cell differentiation (Tominaga-Wada et al., 2009). The L1-box motif 416

has been found to be an important binding site for HD-ZIP IV transcription factors regulating 417

epidermal cell differentiation in both Arabidopsis and cotton (Gossypium barbadense), (Abe 418

et al., 2003; Ohashi et al., 2003; Zhang et al., 2010). Significantly, an HD-ZIP IV ortholog 419

from cotton GbML1, was shown to not only bind the L1-box motif but also a cotton MIXTA 420

family protein, GbMYB25 (Zhang et al., 2010). In SlMIXTA-RNAi lines, the HD-ZIP IV 421

transcription factor SlANL2b (Supplemental Fig. S6) was massively up-regulated (40-fold; 422

Supplemental Dataset S1). If a similar mechanism found in cotton exists in tomato and 423

SlANL2b can be regarded as having the orthologous function to GbML1 (i.e. binding both 424

the L1-box motif and SlMIXTA-like), then the massive increase in SlANL2b expression in 425

SlMIXTA-RNAi lines may represent a compensating mechanism for the loss of SlMIXTA-like 426

expression. 427

These results suggest that the influence of SlMIXTA-like (and possibly MIXTA 428

orthologs in general) on epidermal cell differentiation may be mediated through a regulatory 429

network with L1-box motif binding HD-ZIP IV transcription factors (such as SlGL2 and 430

SlANL2b). This view of such a network between MIXTA and HD-ZIP IV transcription 431

factors in relation to epidermal cell differentiation identity can be expanded when a recent 432



23

work on the AP2 domain SlSHN3 transcription factor is considered (Shi et al., 2013). The 433

results of this earlier study suggested that SlSHN3 was able to regulate epidermal cell 434

patterning in tomato via SlGL2 and/or SlMIXTA-like activities. SlGL2 and SlMIXTA-like 435

were both down-regulated in SlSHN3-RNAi tomato lines and LUC reporter assays showed 436

that SlSHN3 acted on the promoters of both genes (Shi et al., 2013). This, together with the 437

fact that SlSHN3 displayed no change in expression in SlMIXTA-RNAi lines suggests that in 438

tomato fruit, SlSHN3 appears to act above SlMIXTA-like in the regulatory pathway 439

controlling epidermal cell patterning (Fig. 9). 440

Finally, it should be noted that while strong evidence is presented for the involvement 441

of L1 layer-specific genes as the mediators of SlMIXTA-like activity in relation to epidermal 442

cell shape it may be that this morphological alteration is in fact a secondary effect caused by 443

the observed reduction in cuticle deposition. Specifically, tomato fruit epidermal cells are 444

either totally, or partially, enveloped by the cuticle, which likely contributes to the cell 445



24

structure. Recent results have indeed found that the fruit surface structure is influenced by 446

cutin deposition; however in this work a change in cutin deposition was not necessarily 447

shown to result in a change in epidermal cell shape (Petit et al., 2014). Further, silencing of 448

CHALCONE SYNTHASE expression (a gene responsible for the inclusion of naringenin 449

chalcone in the tomato cuticle), results in a stiffer, less elastic cuticle, surrounding flatter 450

epidermal cells (Schijlen et al., 2007; España et al., 2014). These results hint at a potential 451

dependence on the surrounding cuticle with regard to epidermal cell structure. Further 452

investigations into the relationship between cuticular lipid composition and epidermal cell 453

development will prove invaluable to our understanding of plant surface formation. 454

455

SlMIXTA-like is a Positive Regulator of Tomato Fruit Cutin Biosynthesis and Assembly 456

Expression analysis of SlMIXTA-like in developing tomato fruit revealed a skin enriched 457

expression profile (predominantly at the early green stages of fruit development), while 458

transcriptome analysis across multiple tissues and developmental stages revealed that 459

SlMIXTA-like was also significantly expressed in the petals and pollen. This expression 460

profile is typical of genes involved in cuticle biosynthesis (Mintz-Oron et al., 2008). 461

Moreover, laser-micro dissection coupled to transcriptomic analysis of tomato fruit cell types 462

showed that SlMIXTA-like is expressed in the inner, as well as outer, epidermal layers but not 463

collenchyma, parenchyma or vascular tissues (Matas et al., 2011; Hen-Avivi et al., 2014) 464

(Fig. 1B). The inner epidermal layer of tomato fruit produces a waxy cuticle separating the 465

fleshy endocarp from the locular region of the fruit (Mintz-Oron et al., 2008; Matas et al., 466

2011) and thus, it seems likely that SlMIXTA-like plays a role in the regulation of this inner 467

cuticle as well as the outer fruit cuticle. It is interesting to note that the previously 468

characterized tomato cuticle regulators, SlSHN3 and SlCD2, are also expressed in both the 469

inner and outer epidermis (Hen-Avivi et al., 2014). 470

Analysis of the tomato lines altered in SlMIXTA-like expression demonstrated a 471

significant correlation between cuticle deposition and SlMIXTA-like expression. This was 472

evident in the microscopic analysis which displayed a significantly thinner cuticle in the 473

SlMIXTA-like RNAi lines and the chemical analysis, which highlighted that this change can 474

be predominantly attributed to a modification in cutin monomer biosynthesis. In fact, the 475

change in cutin levels in the transgenics correlated strongly with the change in the overall 476

weight of the isolated cuticle. Significant differences in the cutin composition were 477

particularly evident in the highly abundant modified C16 fatty acid, more specifically C16 478



25

9/10,16 DiHFA, the dominant cutin monomer of tomato fruit, as well as DFAs and ω-HFAs. 479

The saturated fatty acids, however, showed few significant changes in plants exhibiting 480

modified SlMIXTA-like expression, suggesting that SlMIXTA-like exerts its activity at the 481

downstream modification steps of the cutin biosynthetic pathway. This hypothesis was 482

confirmed through the transcriptional analysis of the transgenic plants. Numerous genes that 483

are directly responsible for the biosynthesis of specific modified fatty acids were down 484

regulated in plants with reduced SlMIXTA-like expression. In addition, genes involved in the 485

extracellular transport and the polymerization of the cutin matrix were also found to display 486

similar, SlMIXTA-like-dependent, expression patterns. In most cases the enzymatic activity of 487

the proteins coded by these various genes was inferred through the homology with 488

characterized orthologs, but for a number of the candidate enzymes, assays were performed 489

to confirm these activities. Thus, for a few of the steps in the cutin metabolic pathway, 490

namely the terminal hydroxylation of activated fatty acids by SlCYP86A68 and the mid-chain 491

hydroxylation of fatty acids by both SlCYP77A1 and SlCYP77A2, we are able to present 492

cohesive data for SlMIXTA-like regulated gene expression, enzyme activity and the resultant 493

metabolite change in the fruit skin (Fig. 5; Fig. 7; Table 1). Previously, SlCYP86A69 was 494

shown to be directly regulated by SlSHN3, and the resultant activity responsible for cutin 495

biosynthesis (Shi et al., 2013). While SlCYP86A69 does not appear to be regulated in an 496

SlMIXTA-like dependent manner, we show that SlCYP77A1 action is responsible for the 497

formation of the major cutin monomer found in tomato skin, namely C16-9/10, 16-DiHFA, 498

and that SlCYP77A1 is regulated in an SlMIXTA-like dependent manner. 499

The broad spectrum of influence exerted through SlMIXTA-like activity strongly 500

suggests a central role for SlMIXTA-like in the positive regulation of cuticle deposition 501

(particularly cutin). Significantly, recent work has shown that the Arabidopsis orthologs of 502

SlMIXTA-like, AtMYB16 and AtMYB106, also play a role in the regulatory network of cuticle 503

assembly (Oshima et al., 2013), although their effect is less specific as they regulate both the 504

wax and cutin biosynthetic pathways. Interestingly, one of the orthologs, AtMYB106, is able 505

to regulate the expression of AtSHN1, which appears to be an inversion of the relationship 506

seen between these two orthologs in tomato (Fig. 9), pointing to a complex evolutionary 507

relationship between these proteins. 508

509

SlMIXTA-like Regulates Postharvest Water Loss Prevention and Resistance to Fungal 510

Infection 511



26

Previous studies demonstrated the important role of the cuticle in protecting plants from 512

biotic and abiotic stresses, and that abnormal cuticle formation can lead to plants with altered 513

susceptibility to dehydration stress and fungal infection (Bargel et al., 2006; Riederer and 514

Muller, 2006; Isaacson et al., 2009). In the case of SlMIXTA-RNAi lines an increase in 515

susceptibility to both fungal infection and postharvest water loss was observed. It seems 516

likely that the significantly thinner cuticle allows easier penetration of the epidermal cells by 517

C. coccodes and thus faster proliferation of the fungus. This conclusion was supported by the 518

fact that C. coccodes fungus had similar rate of germination and appressoria formation but 519

the decay area was significantly larger. However, the increased postharvest water loss is more 520

difficult to explain. Previous research has suggested that cuticular waxes rather than the cutin 521

matrix are responsible for the water-proofing of the plant (Vogg et al., 2004; Isaacson et al., 522

2009). However, in the case of tomato lines reduced in SlMIXTA-like expression there 523

appears to be limited changes to the total (epi and intra-) cuticular wax composition. It may 524

be that severity of reduction in the cutin polymer provided a reduced matrix to which the 525

intra-cuticular waxes may be attached and embedded. Therefore it is possible that altered 526

cuticular structure and arrangement is the main factor responsible for the increase in water 527

loss. 528

Recent work showed that the cuticle is involved in the transmission of osmotic stress 529

signals via ABA biosynthesis (Wang et al., 2011). The fact that SlMIXTA-RNAi lines 530

displayed down-regulation of the ABA biosynthesis gene NINE-CIS-EPOXYCAROTENOID 531

DIOXYGENASE1 (SlNCED1) (Sun et al., 2012; Ji et al., 2014) suggests that the reason for 532

the increased susceptibility to dehydration may be due to the impairment of a signal 533

originating from the cuticle (Supplemental Fig. S4; Supplemental Dataset S1). Further, 534

increased cuticle permeability in ABA deficient mutants has been reported (Curvers et al., 535

2010), suggesting a feedback loop connecting ABA biosynthesis and cuticle formation that 536

might be regulated via the action of SlMIXTA-like. Furthermore, ABA biosynthesis was 537

recently shown to be up-regulated in tomato fruit’s resistance response to Colletotricum 538

(Alkan et al., 2015). This, therefore, may further contribute to the enhanced fungal 539

colonization of SlMIXTA-RNAi fruit surface. 540

541

Conclusions 542

The evolution of land plants resulted in a number of important changes to the epidermal layer 543

of aerial organs including of fleshy fruit. Over time, epidermal cells began to differentiate to 544

form a variety of cell types while concurrently developing the specialized cuticular 545



27

membrane necessary for overcoming the challenges of life on land. It is thus anticipated that 546

the co-evolution of the epidermis cell layer and the cuticle coating it should intersect, 547

particularly at the regulatory level. Here we provide evidence that SlMIXTA-like 548

transcriptionally modulates epidermal cell patterning as well as cuticle assembly and forms 549

part of a transcriptional regulatory network that mediates the patterning of fruit surface. 550

Hence, this work highlights the strong evolutionary and regulatory relationship between plant 551

epidermal cell development and cuticle deposition and points to SlMIXTA-like as a major 552

player in this relationship. 553

554

Materials and Methods 555

Plant Materials and Transformation 556

Silencing of SlMIXTA-like (Solyc02g088190) was performed in S. lycopersicum L. cv. 557

MicroTom (MT). The construct for the post transcriptional silencing (SlMIXTA-RNAi) was 558

generated by PCR, isolating a 273 bp fragment of SlMIXTA from cv. MT cDNA and cloning 559

into pENTR/D-TOPO (Invitrogen). LR Clonase (Invitrogen) was used to recombine this 560

fragment into the pH7GWIWG2(II) binary vector (Karimi et al., 2002). The primers used in 561

the creation of the constructs in this study are listed in Supplemental Table S2. Cotyledon 562

transformation of MT tomato was performed as previously described (Dan et al., 2006). 563

Subsequent gene expression analysis, chemical characterization and fungal infection and 564

water loss assays were performed using at least three independently transformed lines. 565

566

In Silico Analysis 567

Nucleotide and protein sequence retrieval from the SOL Genomics Network database was 568

performed via BLAST (Fernandez-Pozo et al., 2015). Protein alignments were performed 569

with ClustalW (Larkin et al., 2007) and the resultant molecular phylogenetic trees visualized 570

using MEGA6 (Tamura et al., 2013). Neighbor-joining trees were constructed with 571

bootstrapping calculated from 1000 instances. Promoter regions consisting of 1 Kb of 572

upstream sequence from the start codons were analyzed for binding motifs using the PLACE 573

database (Higo et al., 1999). Determination of enrichment of promoter motifs and of L1 574

layer-specific genes was performed using the hypergeometric distribution analysis provided 575

by GeneProf (Halbritter et al., 2014). Promoter motif presence was compared to 6000 kb of 576

randomly extracted genomic DNA spanning all 12 tomato chromosomes (Fernandez-Pozo et 577

al., 2015). Hierarchical clustering of genes based on available large scale expression data 578



28

(Itkin et al., 2013), was performed using EXPANDER (Ulitsky et al., 2010) with the default 579

parameters. 580

581

Gene expression Analysis 582

Total RNA extractions were performed with Trizol Reagent (Invitrogen) from manually 583

dissected skin and flesh tissues pooled from five to six tomato fruits. Skin tissue can be 584

thought of enriched for epidermal cells. RNA was extracted from mature green peel tissue 585

from three independently transformed tomato lines and wild type lines. The cDNA was 586

synthesized using Invitrogen’s SuperScript II reverse transcriptase kit. Quantitative real-time 587

PCR (qRT-PCR) analysis was performed using gene-specific oligonucleotides on an ABI 588

7300 instrument (Applied Biosystems, Norwalk, CT, USA) with the Platinum SYBR 589

SuperMix (Invitrogen) under default parameters. Mean expression values were calculated for 590

three independent transformation events. Applied Biosystems software was used to generate 591

expression data. Sequences of gene-specific oligonucleotides are provided in Supplemental 592

Table S2. Microarray analysis was performed using the 34,000 gene EUTOM3 exon array 593

(http://www.eu-sol.net/science/bioinformatics/data-and-databases/all-databases) as described 594

previously (Powell et al., 2012). 595

596

Light-, Electron- and Atomic Force- Microscopy 597

Samples for electron microscopy were prepared and analyzed as described previously 598

(Panikashvili et al., 2009). Samples prepared for TEM analysis were also used for FIB-SEM 599

analysis. The FIB-SEM tomography of the region of interest, containing a number of 600

epidermal cells, was performed with the FEI Slice and View software™. Milling was done at 601

an acceleration voltage of 30 kV and current of 2.7 nA. SEM images of the milled surface 602

were acquired with the through-the-lens detector (TLD, SE mode) in immersion mode and an 603

electron beam of 2 kV, 340 pA and 30 μs of dwell time. Subsequent 3D reconstruction was 604

performed by AVIZO software application. For light microscopy, skin tissue samples were 605

fixed and embedded in wax as described previously (Mintz-Oron et al., 2008). Sections were 606

cut to 5–10 µm on a Leica 2000 microtome, and placed on glass slides. The slides were 607

stained with Sudan IV (Buda et al., 2009) or toluidine blue (Tanaka et al., 2004) and then 608

observed with a Olympus CLSM500 microscope. Freshly harvested skin samples were used 609

for AFM imaging. Samples were mounted on a stub, and transferred to the AFM for imaging. 610

All imaging was performed on a NT-MDT NTEGRA instrument, employing the SMENA 611

scanning head. Imaging was performed either in contact mode using Bruker DNP-S probes or 612



29

Olympus ORC-PS-W probes with nominal spring constant of 0.1 N.m-1, or in semi-contact 613

mode using Olympus AC240TS probes with nominal frequency of 70 kHz and spring 614

constant of 2 N.m-1. There was no difference in images obtained by the two modes with 615

exception of one sample with some contamination that was swept aside in contact mode. The 616

raw data were processed only by 2D leveling. 617

618

Cuticular Lipid Analyses 619

Fruit skin discs were prepared for cuticular lipid extraction as previously described (Shi et al., 620

2013). Cuticular waxes were then extracted and analyzed as previously described 621

(Kurdyukov et al., 2006; Kurdyukov et al., 2006), followed by cutin extraction and analysis 622

as described previously (Franke et al., 2005). 623

624

Enzyme Activity Assays 625

Enzyme activity assays were performed using heterologously expressed SlCYP77A1, 626

SlCYP77A2 and SlCYP68A68 according to methods previously described (Grausem et al., 627

2014). Briefly, the genes under investigation were cloned and expressed in a yeast expression 628

system specifically developed for the expression of P450 enzymes (Pompon et al., 1996) 629

(Supplemental Table S2). Expression of the tomato P450s was induced, microsomes were 630

extracted, microsomal proteins were incubated with radiolabeled substrate and the enzyme 631

assay initiated by the addition of NADPH. Only three cytochromes P450 are encoded by the 632

yeast genome, and are not expressed or expressed at a negligible level during the applied 633

growth conditions. Further, none of them are able to metabolize fatty acids (Kandel et al., 634

2005; Sauveplane et al., 2009), ensuring that the metabolism described results from 635

enzymatic reactions catalyzed by the heterologously expressed cytochrome P450s. 636

Completed assays were directly spotted on TLC plates for the separation of possible products 637

formed. Plates were scanned with a radioactivity detector and the areas corresponding to the 638

metabolites were identified for subsequent GC-MS analysis. GC-MS analysis was carried out 639

and analyzed as described previously (Eglinton et al.; Grausem et al., 2014). Metabolites 640

generated from 16-hydroxypalmitic acid were identified as described previously (Li-Beisson 641

et al., 2009). As no standards are available, position of hydroxyl group is given by 642

fragmentation on both sides of the derivatized hydroxyl. This results in ions that allow one to 643

distinguish between products. 644

645

Fungal Infection and Dehydration Assays 646



30

Colletotrichum coccodes isolate 138 (Alkan et al., 2008) was used to inoculate fruit of freshly 647

harvested breaker stage tomato fruits. The fruits were surface-sterilized in 0.3% (v/v) 648

hypochlorite for 3 min, rinsed thoroughly with sterile water and dried. Drop inoculation was 649

performed directly on the fruit cuticle by applying a 7 µl of a conidia suspension (106 650

conidia.ml-1). Each line had 30 biological inoculation repeats. Following inoculation, fruits 651

were incubated at humid chambers, 22°C and approximately 95% relative humidity. At 19 652

hours post inoculation percentage of C. coccodes conidia germination and appressorium 653

formation was evaluated under a light-microscope. Disease evaluation of inoculated tomato 654

fruits was performed by measuring the decay diameter, over 7 days post inoculation. The 655

experiment was repeated three times. For water loss measurement assays red stage fruit was 656

harvested and stored at room temperature for forty days. Fruit mass was periodically recorded 657

and water loss percentage calculated. 658

Supplemental Data 659

The following materials are available in the online version of this article. 660

Supplemental Figure S1. Identification of potential tomato MIXTA/MIXTA-like 661

orthologs. 662

Supplemental Figure S2. Protein alignments used to construct molecular phylogenetic 663

trees. 664

Supplemental Figure S3. Atomic Force Microscopy (AFM) images of immature green 665

tomato surface of wild-type and SlMIXTA-like silenced plants. 666

Supplemental Figure S4. Validation of microarray-based differential gene expression 667

results by means of quantitative RT-PCR (qRT-PCR) analysis. 668

Supplemental Figure S5. Normalized expression across 20 tomato tissues of selected 669

genes described in this study to be down regulated in the SlMIXTA-RNAi tomato lines. 670

Supplemental Figure S6. Molecular phylogeny of the HD-ZIP IV family proteins 671

associated with epidermal cell patterning and ones identified in this study. 672

Supplemental Figure S7. Molecular phylogeny of the HD-ZIP IV family proteins 673

associated with epidermal cell patterning and ones identified in this study. 674

Supplemental Figure S8. Radiochromatographic resolution by Thin Layer 675

Chromatography (TLC) of metabolites generated in incubations of dodecanoic acid 676

with microsomes from yeast expressing SlCYP86A68 or SlCYP77A2. 677



31

Supplemental Figure S9. Germination rate and appressoria formation of Colletotrichum 678

coccodes is unchanged on SlMIXTA-like silenced fruit surface. 679

Supplemental Table S1. Quantification of cuticular waxes in fruit of SlMIXTA-like 680

silenced lines. 681

Supplemental Table S2. Oligonucleotides used in this study. 682

Supplemental Dataset S1. Significantly down-regulated and up-regulated genes in skin 683

tissue of SlMIXTA-RNAi lines identified via microarray analysis. 684

Supplemental Dataset S2. Generation and analysis of tomato lines over expressing 685

SlMIXTA-like. 686

Supplemental Dataset S3. Microarray gene expression data of SlMIXTA-RNAi lines and 687

Wildtype lines. 688

Supplemental Movie S1. Three-dimensional reconstruction from FIB-SEM acquisition 689

of an epidermal cell from wild type tomato fruit. 690

Supplemental Movie S2. Three-dimensional reconstruction from FIB-SEM acquisition 691

of an epidermal cell from tomato fruit silenced for SlMIXTA-like expression. 692

Acknowledgements 693

This work was supported by the Israel Science Foundation (ISF) personal grant to A.A. (ISF 694

Grant No. 646/11). We thank the Adelis Foundation, Leona M. and Harry B. Helmsley 695

Charitable Trust, Jeanne and Joseph Nissim Foundation for Life Sciences, Tom and Sondra 696

Rykoff Family Foundation Research and the Raymond Burton Plant Genome Research Fund 697

for supporting the AA lab activity. AA is the incumbent of the Peter J. Cohn Professorial 698

Chair. We thank Sidney Cohen for assistance in performing the AFM analysis. We thank 699

Gilgi Friedlander for the assistance in the analysis of the microarray data. 700

Author Contributions 701

J.L. designed and performed research, analyzed data, and co-wrote the article. A.A. designed 702

and performed research and analyzed data. O.L., N.A., T.T., K.R., J-P. F., B.G., F.P. and 703

A.G. performed research and analyzed data. F.C. analyzed data, and co-wrote the article. 704

A.A. designed research, analyzed data and co-wrote the article. All authors read, made 705

relevant suggestions and approved the final manuscript. 706



32

707



33

Tables 708

Table 1. Quantification of cutin monomer composition in fruit of SlMIXTA-like 709

silenced lines and wild-type lines. 710

Cutin monomers quantified after BF3 depolymerization of enzymatically isolated, 711 dewaxed tomato fruit cuticles (red stage fruit). Concentrations (µg/cm-2) shown for 712 lines silenced for SlMIXTA-like (SlMIXTA-RNAi) and the corresponding wild type 713 (WT). Extractions were performed on three independently transformed lines. 714 Monomers that show significant changes (Student’s t-test) from the wild type are 715 indicated with an ** (p < 0.01), or * (p < 0.05). 716 717

Wild type SlMIXTA-RNAi Cutin Monomers Average SE Average SE Aromatic cis-Coumaric acid 0.92 0.23 0.55 0.17 trans-Coumaric acid 50.52 1.57 11.26** 3.01 Subtotal 51.44 1.44 11.81** 2.84 Saturated fatty acids (FA) C16:0 FA 2.84 0.14 2.45 0.21 C18:0 FA 5.51 0.26 4.89 0.2 Subtotal 8.35 0.4 7.33 0.41 Dicarboxylic fatty acids (DFA) C16:0 DFA 24.92 1.34 11.22** 1.14 C16-9,10 hydroxy-DFA 67.53 4.73 40.57** 4.3 Subtotal 92.46 4.78 51.79** 5.37 Mid chain hydroxylated fatty acids (HFA) C16-9/10,16 DiHFA 797.66 43.11 640.48** 35.58 C18-9,18 DiHFA 2.97 0.33 2.77 0.2 C18:1-9,10,18-TriHFA 1.0 0.27 0.32* 0.03 C18-9,10 DiHFA 43.69 3.72 30.18** 2.32 Subtotal 845.31 47.32 673.75** 37.7 Terminal hydroxylated fatty acids (ω HFA) C16:1-ω HFA 7.37 0.6 4.13** 0.93 C16-ω HFA 142.55 1.82 77.46** 6.75 Subtotal 149.91 2.28 81.59** 7.58 Epoxy fatty acids C18:1-9,10-epoxy-18- ω -HFA 2.34 0.24 2.38 0.07 C18-9,10-epoxy-18- ω -HFA 3.44 0.31 3.69 0.23 Subtotal 5.78 0.55 6.08 0.27 Other Naringenin 22.58 4.89 27.66 13.45 Naringenin dimer 23.88 0.49 13.86* 4.37 Subtotal 46.46 4.66 41.52 12.8 Unknown Subtotal 187.38 6.46 134.1** 19.26 Total 1387.09 53.86 1012.65** 70.94



34

Table 2. Genes putatively involved in cuticle assembly showing down-regulation in the SlMIXTA-RNAi lines. 718

Gene ID Gene Name Putative Function Fold-change p-value Cluster Characterized ortholog Reference

Solyc05g054330 α/β-hydrolase cutin polymerization -7.8 0.001 IV.iib AtBDG (At1g64670) Kurdyukov et al. (2006a)

Solyc03g117800L1 CER3 alkane biosynthesis -7.7 0.014 IV.iia AtCER3 (At5g57800) Bernard et al. (2012)

Solyc08g080190L1 HTH dicarboxylic-acid biosynthesis -6.8 0.001 IV.iia AtHTH (At1g72970) Kurdyukov et al. (2006b)

Solyc03g121180L1 GDSL esterase/lipase cutin polymerization -4.3 0.040 IV.i SlCD1 (Solyc11g006250) Girard et al. (2012);

Yeats et al. (2012)

Solyc01g109180LB,L1 LACS2 acyl activation -3.7 (-8.3) 0.001 (0.033) IV.iia AtLACS2 (At1g49430) Schnurr et al. (2004); Jessen et al. (2011)

Solyc09g075140LB α/β-hydrolase cutin polymerization -3.7 0.001 IV.iia AtBDG (At1g64670) Kurdyukov et al. (2006a)

Solyc01g095750LB,L1 LACS4 acyl activation -3.6 (-4.3) 0.003 (0.011) IV.iia AtLACS4 (At4g23850) Schnurr et al. (2004); Jessen et al. (2011)

Solyc03g019760LB,L1 ABCG11 cuticular lipids transport -3.1 0.009 IV.iia AtABCG11 (At1g17840) Bird et al. (2007); Panikashvili et al. (2007)

Solyc11g072990LB,L1 KCS3 fatty acid elongation -3.0 0.003 IV.iia AtKCS3 (At1g07720) Millar et al. (1999)

Solyc05g055400LB,L1 CYP77A2 midchain fatty-acid oxidation* -2.5 (-20.7) 0.038 (0.022) IV.iia AtCYP77A4 (At5g04660) Li-Beisson et al. (2009)

Solyc06g065670LB,L1 PDR4/ABCG32 cuticular lipids transport -2.1 0.043 IV.iib AtABGC32 (At2g26910) Bessire et al. (2011)

Solyc04g081770LB,L1 GDSL esterase/lipase cutin polymerization -2.0 0.025 IV.iia SlCD1 (Solyc11g006250) Girard et al. (2012);

Yeats et al. (2012) Solyc01g094700LB,L1 GPAT4 acyl transfer (-38.1) (0.013) IV.iia AtGPAT4 (At1g01610) Li et al. (2007)

Solyc11g007540LB,L1 CYP77A1 midchain fatty-acid oxidation* (-13.3) (0.045) IV.iia AtCYP77A4 (At5g04660) Li-Beisson et al. (2009)

Solyc01g094750LB CYP86A68 terminal fatty-acid oxidation* (-4.8) (0.039) IV.iia SlCYP86A69 (Solyc08g081220) Shi et al. (2013)

Solyc07g049440LB,L1 GDSLa cutin polymerization (-4.2) (0.003) IV.iia SlCD1 (Solyc11g006250) Girard et al. (2012); Yeats et al. (2012)

Solyc03g120620LB GL2 cuticle regulation (-3.6) (0.037) IV.iia SlCD2 (Solyc01g091630) Isaacson et al. (2009); Nadakuduti et al. (2012)

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A 2-fold change cut off and p-value ≤ 0.05 were used. Majority of values are derived from microarray experiment, however values in brackets 719 are derived from quantitative real time-PCR (qRT-PCR) analysis. LB = Contains the L1-box promoter motif (Abe et al., 2001). L1 = L1 layer 720 specific expression (Filippis et al., 2013). * = putative function confirmed in this paper. 721 722

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Figure Legends 723

Figure 1. The tomato MIXTA-like gene is predominantly expressed in fruit epidermal 724

layers. 725

A, Molecular phylogenetic analysis of the functionally characterized members of the 726

MIXTA/MIXTA-like protein clade are shown together with the assigned functional roles. 727

ClustalW and the MEGA6 software were used to align the proteins and compute the 728

neighbor-joining tree with significance percentages (bootstrap values out of 1000). The scale 729

bar represents the relative amino acid difference. Alignments can be viewed in Supplemental 730

Fig. S2. Gossypium hirsuta (Gh), Populus trichopoda (Pt), Antirrhinum majus (Am), Solanum 731

lycopersicum (Sl), Petunia hybrida (Ph), Medicago truncatula (Mt), Arabidopsis (At), 732

Dendrobium crumenatum (Dc) and Thalictrum thalictroides (Tt). B, An epidermal specific 733

expression pattern is observed for the SlMIXTA-like gene. Normalized expression of 734

SlMIXTA-like in immature green fruit tissues showed outer and inner epidermal expression 735

(data was extracted from previously published results (Matas et al., 2011)). outepi, outer 736

epidermis; collen, collenchyma; vascu, vascular tissue; paren, parenchyma; inepi, inner 737

epidermis. C, Normalized expression of SlMIXTA-like across 20 tomato tissues highlights 738

skin enriched expression in developing tomato fruit as well as significant expression in the 739

petals and pollen (data extracted from previously published work (Itkin et al., 2013)). IG, 740

immature green; MG, mature green; Br, breaker; Or, orange; Re, red; Y, young. 741

742

Figure 2. Growth and developmental phenotypes of tomato plants with altered 743

SlMIXTA-like expression. 744

A, Confirmation of SlMIXTA-like gene silencing confirmed by quantitative Real Time-PCR 745

(qRT-PCR) analysis of transgenic tomato plants (cv. MicroTom). Data shows mean and 746

standard error for three individually transformed lines. n = 3, ** = p-value < 0.01. B, 747

Silencing of the SlMIXTA-like gene resulted in smaller, crinkled and curled leaves. C, Altered 748

expression of the SlMIXTA-like gene in tomato results in changes to plant architecture. Lines 749

silenced for SlMIXTA-like gene expression were smaller and displayed stunted growth. WT, 750

wild type; RNAi, lines silenced for SlMIXTA-like expression. 751

752

Figure. 3. Epidermal cell patterning and cuticle deposition in fruit surface of SlMIXTA-753

like silenced tomato plants. 754



37

A, Light microscopy observations of Sudan IV stained tomato skin sections showing reduced 755

cuticle deposition and flatter epidermal cells at the mature green fruit stage. ec, epidermal cell. 756

B, As in A but in the red stage of development. C, Cryo- Scanning Electron Microscopy 757

(SEM) of the surface of tomato fruit at the mature green stage illustrates the effect of cell 758

shape on surface morphology. Note the flat cells in the SlMIXTA-like silenced fruit. D, 759

Atomic Force Microscopy (AFM) images of red, ripe tomato fruit surface displaying a flatter, 760

more irregular and rough surface in the SlMIXTA-RNAi sample. Scale bars for the x- and y-761

axis represent 20µm, while the z-axis scale bar represents 2µm. Images are mixed light-762

shaded to contrast the small features on the overall large topography. E, Transmission 763

Electron Microscopy (TEM) observations of tomato fruit epidermal cells (red fruit stage). A 764

thinner cuticle as well as a distinct cell shape can be observed in the SlMIXTA-RNAi sample. 765

pcw, primary cell wall; cl, cuticular layer. 766

767

Figure 4. Three-dimensional reconstruction from Focused Ion Beam Scanning Electron 768

Microscopy (FIB-SEM) acquisition shows that fruit of tomato lines silenced for 769

SlMIXTA-like expression possess flatter epidermal cells. 770

A, B, C and D, Images acquired from the fruit skin of wild-type tomato display conical 771

epidermal cell shape. E, F, G, and H, Images of an epidermal cell from SlMIXTA-RNAi 772

tomato fruit display a considerably flattened shape. I and J, The observations above were 773

corroborated by in silico construction of three-dimensional models of epidermal cells for both 774

wild-type (I) and SlMIXTA-RNAi (J). Scale bars indicate 20 µm. See also Supplemental 775

Movie S1 and Supplemental Movie S2 for three-dimensional model construction. 776

777

Figure 5. SlMIXTA-like is required for cutin biosynthesis and deposition of the cuticle. 778

A generic cutin biosynthetic pathway using the most abundant C16 fatty acid moiety as a 779

substrate. Transcriptomic analysis pertaining to the pathway is displayed in the form of graphs 780

indicating relative gene expression. Values are a mean of three independently transformed 781

lines ± standard error (n=3), see Table 2 for specific fold change values. Relative changes to 782

major cutin monomers are also shown (green arrows; n = 3). 783

784

Figure 6. Hierarchical clustering of genes down-regulated in SlMIXTA-RNAi lines. 785

The fruit development expression profiles of 91 genes identified as down-regulated in 786

SlMIXTA-RNAi lines were extracted from a previously published large scale expression 787



38

dataset (Itkin et al., 2013), and hierarchical clustering was performed. Four major clusters 788

were identified and their mean representative expression profiles are shown adjacent to the 789

heat map (marked I to IV). Pearson correlation coefficients illustrating the homogeneity of the 790

clusters are displayed below the cluster number. The expression profile of SlMIXTA-like 791

located in cluster IV is highlighted by a yellow outline. Additional genes potentially involved 792

in cuticle biosynthesis are labeled and detailed in Table 2. For remaining genes see 793

Supplemental Dataset S1. Red and green colors represent pairwise distances for transcript 794

expression from the mean (black). IG, Immature Green; MG, Mature Green; Br, Breaker; Or, 795

Orange; R, Red. 796

797

Figure 7. Recombinant SlCYP77A1 catalyzes the formation of dihydroxyhexadecanoic 798

acids. 799

A and B, Microsomes of yeast cells expressing SlCYP77A1 were incubated with 100 μM of 800

hexadecanoic acid in the absence (A) or in the presence (B) of NADPH. Reactions products 801

were extracted with diethyl ether, derivatized and subjected to GC/MS analysis. C, 802

Fragmentation pattern of the dihydroxyhexadecanoic acid peak is presented and identified to 803

be a mixture of 8,16-; 9,16-; 10,16- and 11,16-dihydroxyhexadecanoic acids. The molecular 804

structure of the most abundant tomato cuticle fatty acid, 9,16-dihydroxyhexadecanoic acid, is 805

displayed. 806

807

Figure 8. Reduced SlMIXTA-like expression impacts post-harvest water loss and 808

susceptibility to fungal infection. 809

A, Water loss progression in fruit of wild-type and SlMIXTA-RNAi lines was measured over 810

40 days of postharvest incubation at room temperature. B, Decay area rates of Colletotrichum 811

coccodes colonization were measured after inoculation of breaker stage tomato fruit cuticle 812

during 7 days. Error bars represent standard error (n=30). 813

814

Figure 9. The SlMIXTA-like regulatory network controls cuticle assembly and cell 815

patterning. 816

The SlSHN and SlMIXTA-like proteins directly or indirectly regulate cuticle deposition in 817

tomato fruit skin as part of a larger program of epidermal cell patterning. This network likely 818

involves interaction with additional regulators such as members of the HD-ZIP IV family of 819

transcription factors. 820



39

821

822



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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Characterization%5BTitle%5D%29 AND 11%5BVolume%5D AND an ATP binding cassette %28ABC%29 transporter that is required for cuticular lipid secretion%2E Plant J 52%3A 485%5BPagination%5D AND Bird D%2C Beisson F%2C Brigham A%2C Shin J%2C Greer S%2C Jetter R%2C Kunst L%2C Wu X%2C Yephremov A%2C Samuels L%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bird&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Biol Evol%5BTitle%5D%29 AND 30%5BVolume%5D AND 526%5BPagination%5D AND Brockington SF%2C Alvarez%2DFernandez R%2C Landis JB%2C Alcorn K%2C Walker RH%2C Thomas MM%2C Hileman LC%2C Glover BJ%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Brockington SF, Alvarez-Fernandez R, Landis JB, Alcorn K, Walker RH, Thomas MM, Hileman LC, Glover BJ (2013) Evolutionary analysis of the MIXTA gene family highlights potential targets for the study of cellular differentiation. Mol Biol Evol 30: 526-540

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28WIN%5BTitle%5D%29 AND 1%5BVolume%5D AND a transcriptional activator of epidermal wax accumulation in Arabidopsis%2E Proc Natl Acad Sci U S A 101%3A 4706%5BPagination%5D AND Broun P%2C Poindexter P%2C Osborne E%2C Jiang CZ%2C Riechmann JL%5BAuthor%5D&dopt=abstract

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scanning laser microscopy. Plant J 60: 378-385Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Chen X, Truksa M, Snyder CL, El-Mezawy A, Shah S, Weselake RJ (2011) Three homologous genes encoding sn-glycerol-3-phosphate acyltransferase 4 exhibit different expression patterns and functional divergence in Brassica napus. Plant Physiol 155:851-865


Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cellexpansion and leaf surface permeability. Plant J 53: 53-64


Curvers K, Seifi H, Mouille G, de Rycke R, Asselbergh B, Van Hecke A, Vanderschaeghe D, Höfte H, Callewaert N, Van BreusegemF, Höfte M (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomatoresistance to Botrytis cinerea. Plant Physiol 154: 847-860


Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, Armstrong CL (2006) MicroTom--a high-throughput model transformation system forfunctional genomics. Plant Cell Rep 25: 432-441


Depège-Fargeix N, Javelle M, Chambrier P, Frangne N, Gerentes D, Perez P, Rogowsky PM, Vernoud V (2011) Functionalcharacterization of the HD-ZIP IV transcription factor OCL1 from maize. J Exp Bot 62: 293-305


Di Stilio VS, Martin C, Schulfer AF, Connelly CF (2009) An ortholog of MIXTA-like2 controls epidermal cell shape in flowers ofThalictrum. New Phytol 183: 718-728


Dillard HR (1989) Effect of temperature, wetness duration, and inoculum density on infection and lesion development ofColletotrichum coccodes on tomato fruit. Phytopathology: 1063-1066


Eglinton G, Hunneman DH, McCormick A Gas chromatographic—mass spectrometric studies of long chain hydroxy acids.—III.1The mass spectra of the methyl esters trimethylsilyl ethers of aliphatic hydroxy acids. A facile method of double bond location.

España L, Heredia-Guerrero JA, Reina-Pinto JJ, Fernández-Muñoz R, Heredia A, Domínguez E (2014) Transient silencing ofCHALCONE SYNTHASE during fruit ripening modifies tomato epidermal cells and cuticle properties. Plant Physiol 166: 1371-1386


Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, Bombarely A, Fisher-York T, Pujar A, Foerster H, Yan A,Mueller LA (2015) The Sol Genomics Network (SGN)-from genotype to phenotype to breeding. Nucleic Acids Res 43: D1036-1041


Filippis I, Lopez-Cobollo R, Abbott J, Butcher S, Bishop GJ (2013) Using a periclinal chimera to unravel layer-specific geneexpression in plants. Plant J 75: 1039-1049


Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L (2005) Apoplastic polyesters in Arabidopsissurface tissues--a typical suberin and a particular cutin. Phytochemistry 66: 2643-2658


Gilding EK, Marks MD (2010) Analysis of purified glabra3-shapeshifter trichomes reveals a role for NOECK in regulating earlytrichome morphogenic events. Plant J 64: 304-317

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 60%5BVolume%5D AND 378%5BPagination%5D AND Buda GJ%2C Isaacson T%2C Matas AJ%2C Paolillo DJ%2C Rose JK%5BAuthor%5D&dopt=abstract

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Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T (2007)Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved inregulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19: 2531-2543


Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R, Tikunov Y, Bovy A,Chikate Y, Singh P, Rogachev I, Beekwilder J, Giri AP, Aharoni A (2013) Biosynthesis of antinutritional alkaloids in solanaceouscrops is mediated by clustered genes. Science 341: 175-179


Javelle M, Vernoud V, Depège-Fargeix N, Arnould C, Oursel D, Domergue F, Sarda X, Rogowsky PM (2010) Overexpression of theepidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involvedin lipid metabolism and cuticle biosynthesis. Plant Physiol 154: 273-286


Jessen D, Olbrich A, Knüfer J, Krüger A, Hoppert M, Polle A, Fulda M (2011) Combined activity of LACS1 and LACS4 is required forproper pollen coat formation in Arabidopsis. Plant J 68: 715-726 https://plantphysiol.orgDownloaded on December 14, 2020. - Published by


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http://scholar.google.com/scholar?as_q=The cytochrome P450 CYP86A22 is a fatty acyl-CoA omega-hydroxylase essential for Estolide synthesis in the stigma of Petunia hybrida&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Han&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Isaacson&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jessen&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28SlNCED%5BTitle%5D%29 AND 2%5BVolume%5D AND key genes involved in ABA metabolism during tomato fruit ripening%2E J Exp Bot 65%3A 5243%5BPagination%5D AND Ji K%2C Kai W%2C Zhao B%2C Sun Y%2C Yuan B%2C Dai S%2C Li Q%2C Chen P%2C Wang Y%2C Pei Y%2C Wang H%2C Guo Y%2C Leng P%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=There's more than one way to skin a fruit: formation and functions of fruit cuticles&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://scholar.google.com/scholar?as_q=Tissue- and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matas&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Panikashvili&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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Petit J, Bres C, Just D, Garcia V, Mauxion JP, Marion D, Bakan B, Joubès J, Domergue F, Rothan C (2014) Analyses of tomato fruitbrightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase. PlantPhysiol 164: 888-906


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http://scholar.google.com/scholar?as_q=Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Perez-Rodriguez&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 164%5BVolume%5D AND 888%5BPagination%5D AND Petit J%2C Bres C%2C Just D%2C Garcia V%2C Mauxion JP%2C Marion D%2C Bakan B%2C Joub�s J%2C Domergue F%2C Rothan C%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Petit&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Analyses of tomato fruit brightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Analyses of tomato fruit brightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Petit&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28FEBS J%5BTitle%5D%29 AND 278%5BVolume%5D AND 195%5BPagination%5D AND Pinot F%2C Beisson F%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pinot&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Plett&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Plett&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Building lipid barriers: biosynthesis of cutin and suberin&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Building lipid barriers: biosynthesis of cutin and suberin&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pollard&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Methods Enzymol%5BTitle%5D%29 AND 272%5BVolume%5D AND 51%5BPagination%5D AND Pompon D%2C Louerat B%2C Bronine A%2C Urban P%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Yeast expression of animal and plant P450s in optimized redox environments&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Yeast expression of animal and plant P450s in optimized redox environments&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pompon&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Science%5BTitle%5D%29 AND 336%5BVolume%5D AND 1711%5BPagination%5D AND Powell AL%2C Nguyen CV%2C Hill T%2C Cheng KL%2C Figueroa%2DBalderas R%2C Aktas H%2C Ashrafi H%2C Pons C%2C Fern�ndez%2DMu�oz R%2C Vicente A%2C Lopez%2DBaltazar J%2C Barry CS%2C Liu Y%2C Chetelat R%2C Granell A%2C Van Deynze A%2C Giovannoni JJ%2C Bennett AB%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Powell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Powell&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 285%5BVolume%5D AND 38337%5BPagination%5D AND Rani SH%2C Krishna TH%2C Saha S%2C Negi AS%2C Rajasekharan R%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rani&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Defective in cuticular ridges (DCR) of Arabidopsis thaliana, a gene associated with surface cutin formation, encodes a soluble diacylglycerol acyltransferase&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Defective in cuticular ridges (DCR) of Arabidopsis thaliana, a gene associated with surface cutin formation, encodes a soluble diacylglycerol acyltransferase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rani&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genes Dev%5BTitle%5D%29 AND 8%5BVolume%5D AND 1388%5BPagination%5D AND Rerie WG%2C Feldmann KA%2C Marks MD%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rerie&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

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Scoville AG, Barnett LL, Bodbyl-Roels S, Kelly JK, Hileman LC (2011) Differential regulation of a MYB transcription factor iscorrelated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol 191: 251-263


Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesisunder drought conditions in Arabidopsis. Plant Cell 23: 1138-1152


Shi JX, Adato A, Alkan N, He Y, Lashbrooke J, Matas AJ, Meir S, Malitsky S, Isaacson T, Prusky D, Leshkowitz D, Schreiber L,Granell AR, Widemann E, Grausem B, Pinot F, Rose JK, Rogachev I, Rothan C, Aharoni A (2013) The tomato SlSHINE3 transcriptionfactor regulates fruit cuticle formation and epidermal patterning. New Phytol 197: 468-480


Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, Schreiber L, Aharoni A (2011) SHINE transcription factors act redundantlyto pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 7: e1001388


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Sun L, Sun Y, Zhang M, Wang L, Ren J, Cui M, Wang Y, Ji K, Li P, Li Q, Chen P, Dai S, Duan C, Wu Y, Leng P (2012) Suppression of9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenictomato. Plant Physiol 158: 283-298


Takada S, Takada N, Yoshida A (2013) ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140:1919-1923


Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. MolBiol Evol 30: 2725-2729


Tanaka T, Tanaka H, Machida C, Watanabe M, Machida Y (2004) A new method for rapid visualization of defects in leaf cuticlereveals five intrinsic patterns of surface defects in Arabidopsis. Plant J 37: 139-146


Tominaga-Wada R, Iwata M, Sugiyama J, Kotake T, Ishida T, Yokoyama R, Nishitani K, Okada K, Wada T (2009) The GLABRA2homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J 60: 564-574


Tominaga-Wada R, Nukumizu Y, Sato S, Wada T (2013) Control of plant trichome and root-hair development by a tomato (Solanumlycopersicum) R3 MYB transcription factor. PLoS One 8: e54019


Ulitsky I, Maron-Katz A, Shavit S, Sagir D, Linhart C, Elkon R, Tanay A, Sharan R, Shiloh Y, Shamir R (2010) Expander: fromexpression microarrays to networks and functions. Nat Protoc 5: 303-322


Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M (2004) Tomato fruit cuticular waxes and their effects ontranspiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoAsynthase. J Exp Bot 55: 1401-1410

Pubmed: Author and TitleCrossRef: Author and Title


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http://scholar.google.com/scholar?as_q=The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://scholar.google.com/scholar?as_q=Expander: from expression microarrays to networks and functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ulitsky&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 55%5BVolume%5D AND 1401%5BPagination%5D AND Vogg G%2C Fischer S%2C Leide J%2C Emmanuel E%2C Jetter R%2C Levy AA%2C Riederer M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoA synthase. J Exp Bot 55: 1401-1410



Walford SA, Wu Y, Llewellyn DJ, Dennis ES (2011) GhMYB25-like: a key factor in early cotton fibre development. Plant J 65: 785-797Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Walford SA, Wu Y, Llewellyn DJ, Dennis ES (2012) Epidermal cell differentiation in cotton mediated by the homeodomain leucinezipper gene, GhHD-1. Plant J 71: 464-478


Wang ZY, Xiong L, Li W, Zhu JK, Zhu J (2011) The plant cuticle is required for osmotic stress regulation of abscisic acidbiosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23: 1971-1984


Whitney HM, Bennett KM, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (2011) Why do so many petals have conicalepidermal cells? Ann Bot 108: 609-616


Whitney HM, Chittka L, Bruce TJ, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foragingefficiency. Curr Biol 19: 948-953


Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, Ohlrogge J (2010) A distinct type of glycerol-3-phosphate acyltransferase withsn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc Natl Acad Sci U S A 107: 12040-12045


Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB (2012) A land-plant-specific glycerol-3-phosphateacyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol 160: 638-652


Yeats T, Martin L, Viart H, Isaacson T, He Y, Zhao L, Matas A, Buda G, Domozych D, Clausen M, Rose J (2012) The identification ofcutin synthase: formation of the plant polyester cutin. Nature Chemical Biology 8: 609-611


Yeats TH, Huang W, Chatterjee S, Viart HM, Clausen MH, Stark RE, Rose JK (2014) Tomato Cutin Deficient 1 (CD1) and putativeorthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J 77: 667-675


Zhang F, Zuo K, Zhang J, Liu X, Zhang L, Sun X, Tang K (2010) An L1 box binding protein, GbML1, interacts with GbMYB25 tocontrol cotton fibre development. J Exp Bot 61: 3599-3613



http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Vogg&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoA synthase&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoA synthase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vogg&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 65%5BVolume%5D AND 785%5BPagination%5D AND Walford SA%2C Wu Y%2C Llewellyn DJ%2C Dennis ES%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walford SA, Wu Y, Llewellyn DJ, Dennis ES (2011) GhMYB25-like: a key factor in early cotton fibre development. Plant J 65: 785-797

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Walford&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=GhMYB25-like: a key factor in early cotton fibre development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=GhMYB25-like: a key factor in early cotton fibre development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walford&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 71%5BVolume%5D AND 464%5BPagination%5D AND Walford SA%2C Wu Y%2C Llewellyn DJ%2C Dennis ES%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walford SA, Wu Y, Llewellyn DJ, Dennis ES (2012) Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. Plant J 71: 464-478

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Walford&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walford&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 23%5BVolume%5D AND 1971%5BPagination%5D AND Wang ZY%2C Xiong L%2C Li W%2C Zhu JK%2C Zhu J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang ZY, Xiong L, Li W, Zhu JK, Zhu J (2011) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23: 1971-1984

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Ann Bot%5BTitle%5D%29 AND 108%5BVolume%5D AND 609%5BPagination%5D AND Whitney HM%2C Bennett KM%2C Dorling M%2C Sandbach L%2C Prince D%2C Chittka L%2C Glover BJ%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Whitney HM, Bennett KM, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (2011) Why do so many petals have conical epidermal cells? Ann Bot 108: 609-616

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Whitney&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Why do so many petals have conical epidermal cells&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Why do so many petals have conical epidermal cells&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Whitney&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Biol%5BTitle%5D%29 AND 19%5BVolume%5D AND 948%5BPagination%5D AND Whitney HM%2C Chittka L%2C Bruce TJ%2C Glover BJ%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Whitney HM, Chittka L, Bruce TJ, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19: 948-953

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Whitney&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Conical epidermal cells allow bees to grip flowers and increase foraging efficiency&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Conical epidermal cells allow bees to grip flowers and increase foraging efficiency&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Whitney&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci U S A%5BTitle%5D%29 AND 107%5BVolume%5D AND 12040%5BPagination%5D AND Yang W%2C Pollard M%2C Li%2DBeisson Y%2C Beisson F%2C Feig M%2C Ohlrogge J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, Ohlrogge J (2010) A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc Natl Acad Sci U S A 107: 12040-12045

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 160%5BVolume%5D AND 638%5BPagination%5D AND Yang W%2C Simpson JP%2C Li%2DBeisson Y%2C Beisson F%2C Pollard M%2C Ohlrogge JB%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB (2012) A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol 160: 638-652

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature Chemical Biology%5BTitle%5D%29 AND 8%5BVolume%5D AND 609%5BPagination%5D AND Yeats T%2C Martin L%2C Viart H%2C Isaacson T%2C He Y%2C Zhao L%2C Matas A%2C Buda G%2C Domozych D%2C Clausen M%2C Rose J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yeats T, Martin L, Viart H, Isaacson T, He Y, Zhao L, Matas A, Buda G, Domozych D, Clausen M, Rose J (2012) The identification of cutin synthase: formation of the plant polyester cutin. Nature Chemical Biology 8: 609-611

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yeats&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The identification of cutin synthase: formation of the plant polyester cutin&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The identification of cutin synthase: formation of the plant polyester cutin&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yeats&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 77%5BVolume%5D AND 667%5BPagination%5D AND Yeats TH%2C Huang W%2C Chatterjee S%2C Viart HM%2C Clausen MH%2C Stark RE%2C Rose JK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yeats TH, Huang W, Chatterjee S, Viart HM, Clausen MH, Stark RE, Rose JK (2014) Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J 77: 667-675

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yeats&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yeats&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28An%5BTitle%5D%29 AND 1%5BVolume%5D AND interacts with GbMYB25 to control cotton fibre development%2E J Exp Bot 61%3A 3599%5BPagination%5D AND Zhang F%2C Zuo K%2C Zhang J%2C Liu X%2C Zhang L%2C Sun X%2C Tang K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang F, Zuo K, Zhang J, Liu X, Zhang L, Sun X, Tang K (2010) An L1 box binding protein, GbML1, interacts with GbMYB25 to control cotton fibre development. J Exp Bot 61: 3599-3613

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1


1 short title: the tomato slmixta-like transcription factor 2 · 6.10.2015 · 1 1 short title:...

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