1 biochemistry and metabolism 2 - plant physiology · 54 biochemical analyses coupled with...

1

Biochemistry and Metabolism 1

2

Short title: BAHD Activity in Petunia Trichomes 3

4

For Correspondence: 5

6

Cornelius S. Barry, 7

Department of Horticulture, 8

Michigan State University, 9

East Lansing, 10

MI 48824, 11

USA, 12

Phone: (1) 517 884 6959 13

Fax: (1) 517 353 0890 14

Email: [email protected] 15

16

Plant Physiology Preview. Published on July 12, 2017, as DOI:10.1104/pp.17.00538

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

Characterization of trichome-expressed BAHD acyltransferases in Petunia 17

axillaris reveals distinct acylsugar assembly mechanisms within the Solanaceae1 18

19

Satya Swathi Nadakuduti, Joseph B. Uebler, Xiaoxiao Liu, A. Daniel Jones and 20

Cornelius S. Barry* 21

Department of Horticulture (S.S.N., J.B.U., C.S.B.), Department of Chemistry (X.L., 22

A.D.J.), and Department of Biochemistry and Molecular Biology (A.D.J.), Michigan State 23

University, East Lansing, MI 48824, USA 24

25

26

27

One Sentence Summary: The assembly of plant defense-related acylsugars in Petunia 28

axillaris trichomes requires four acyltransferase activities that are distinct from those 29

catalyzing acylsugar biosynthesis in tomato 30

31 Author Contributions: C.S.B. conceived the original research plans; S.S.N. performed 32

the majority of the experiments; J.B.U. and X.L. provided assistance for some 33

experiments. A.D.J. contributed to data analyses and interpretation. C.S.B. and S.S.N. 34

wrote the manuscript with input from all the authors. 35

36 1 This research was supported by NSF IOS-1025636 and NSF IOS-1546617. C.S.B. 37

and A.D.J. are supported in part by Michigan AgBioResearch and through USDA 38

National Institute of Food and Agriculture, Hatch project numbers MICL02265 and 39

MICL02143. 40

*Address correspondence to [email protected] 41

42



3

ABSTRACT 43

Acylsugars are synthesized in the glandular trichomes of the Solanaceae family and are 44

implicated in protection against abiotic and biotic stress. Acylsugars are comprised of 45

either sucrose or glucose esterified with varying numbers of acyl chains of differing 46

length. In tomato (Solanum lycopersicum), acylsugar assembly requires four acylsugar 47

acyltransferases (ASATs), of the BAHD super family. Tomato ASATs catalyze the 48

sequential esterification of acyl-CoA thioesters to the R4, R3, R3ʹ, and R2 position of 49

sucrose, yielding a tetra-acylsucrose. Petunia spp. synthesize acylsugars that are 50

structurally distinct to those of tomato. To explore the mechanisms underlying this 51

chemical diversity, a P. axillaris transcriptome was mined for trichome preferentially 52

expressed BAHDs. A combination of phylogenetic analyses, gene silencing, and 53

biochemical analyses coupled with structural elucidation of metabolites revealed that 54

acylsugar assembly is not conserved between tomato and petunia. In P. axillaris, tetra-55

acylsucrose assembly occurs through the action of four ASATs, which catalyze 56

sequential addition of acyl groups to the R2, R4, R3 and R6 positions. Notably in P. 57

axillaris, PaxASAT1 and PaxASAT4 catalyze acylation of the R2 and R6 positions of 58

sucrose, respectively, and no clear orthologs exist in tomato. Similarly, petunia 59

acylsugars lack an acyl group at the R3ʹ position and congruently an ortholog of 60

SlASAT3, which catalyzes acylation at the R3ʹ position in tomato, is absent in P. 61

axillaris. Furthermore, where putative orthologous relationships of ASATs are predicted 62

between tomato and petunia, these are not supported by biochemical assays. Overall, 63

these data demonstrate the considerable evolutionary plasticity of acylsugar 64

biosynthesis. 65

66

67

68



4

INTRODUCTION 69

Plants synthesize an array of specialized metabolites that contribute to fitness through 70

their roles in defense against pathogens and herbivory or promotion of reproduction 71

through attraction of pollinators and seed dispersing fauna (Tewksbury and Nabhan, 72

2001; Klahre et al., 2011; Mithofer and Boland, 2012; Dudareva et al., 2013). 73

Specialized metabolites are often synthesized at a specific stage of development or in 74

response to environmental stimuli and their biosynthesis may be restricted to a single 75

tissue or cell type (Bird et al., 2003; Murata et al., 2008; Arimura et al., 2009; Bedewitz 76

et al., 2014; Rambla et al., 2014). Glandular trichomes are epidermal cell appendages 77

present on the surface of many plant species that serve as the location for the 78

synthesis, storage and secretion of diverse classes of specialized metabolites, including 79

phenylpropanoids, terpenoids, and acylsugars (Schilmiller et al., 2008; Tissier, 2012). 80

These compounds act directly as toxins or repellants to deter herbivory or serve as 81

signaling molecules in tritrophic interactions to attract predators and have also been co-82

opted by humans for use as medicines, narcotics, aromatics and flavorings (Schilmiller 83

et al., 2008; Weinhold and Baldwin, 2011; Bleeker et al., 2012). The glandular trichomes 84

of members of the Solanaceae family are structurally and chemically diverse and 85

synthesize specialized metabolites that are often restricted to individual species or 86

specific accessions (Luckwill, 1943; Shapiro et al., 1994; Fridman et al., 2005; 87

Gonzales-Vigil et al., 2012; Kim et al., 2012; Kim et al., 2014). This chemical diversity is 88

manifest through tremendous genetic variation that includes gene duplication and loss, 89

expression variation, and amino acid substitutions that alter enzyme activity (Schilmiller 90

et al., 2010; Kim et al., 2012; Matsuba et al., 2013; Kang et al., 2014; Kim et al., 2014). 91

Together, these studies illustrate the plasticity and rapid evolution of glandular trichome-92

derived specialized metabolites, supporting their role as primary defense mechanisms 93

that likely facilitate plant adaptation to differing environments. 94

95

Acylsugars are synthesized in the glandular trichomes of several Solanaceous species 96

and are particularly abundant in Nicotiana spp., Petunia spp., and the wild tomato 97

species, Solanum pennellii, which can synthesize acylsugars up to 20% of leaf dry 98

weight (Fobes et al., 1985; Severson et al., 1985; Arrendale et al., 1990; Chortyk et al., 99



5

1997). Secretion of acylsugars creates a sticky exudate that covers the aerial surfaces 100

of plants that is implicated in direct defense against herbivores, tritrophic interactions, 101

and possesses antimicrobial activity (Goffreda et al., 1989; Chortyk et al., 1993; Hare, 102



6

2005; Weinhold and Baldwin, 2011; Luu et al., 2017). Acylsugars consist of either a 103

sucrose or glucose backbone onto which acyl groups of differing lengths, typically C2-104

C12, are esterified at various positions (King et al., 1986; King et al., 1988; Halinski and 105

Stepnowski, 2013; Ghosh et al., 2014). Acyl groups can be straight chain (n) or 106

branched chain, with the latter present in the iso (i) and anteiso (ai) configurations 107

(Ghosh et al., 2014; Liu et al., 2017). A combination of ultrahigh performance liquid 108

chromatography mass spectrometry (UHPLC-MS) followed by purification and structural 109

characterization by nuclear magnetic resonance (NMR) spectroscopy revealed that 110

trichomes of cultivated tomato (Solanum lycopersicum) synthesize a relatively simple 111

mixture of approximately 15 tri- and tetra-acylsucroses (Ghosh et al., 2014). This 112

acylsugar profile is dominated by the compound S4:17 (2,5,5,5) which consists of a 113

sucrose (S) molecule esterfied with four (S4) acyl groups that includes a C2 chain and 114

three C5 chains to give a total number of carbons in the acyl groups of 17 (Schilmiller et 115

al., 2010; Ghosh et al., 2014) (Fig. 1A). In addition to the short chain acyl groups, 116

several acylsugars from S. lycopersicum contain a single acyl group ranging from C10 117

to C12 in length that is either esterified at the R3 or R3ʹ position of sucrose (Fig. 1A). 118

Additional chemical complexity is manifest through isomers, which have the same 119

elemental formulae and mass but varied positions of esterification (Ghosh et al., 2014). 120

In contrast, to the relatively simple acylsugar profile of S. lycopersicum, diverse 121

accessions of the wild tomato species S. habrochaites collectively synthesize at least 34 122

acylsucroses and two acylglucoses, although these numbers are likely an 123

underestimate once isomers are considered (Kim et al., 2012; Ghosh et al., 2014). 124

Diversity also exists between accessions of S. pennellii, some of which preferentially 125

accumulate acylglucoses rather than acylsucroses (Shapiro et al., 1994). Overall, these 126

data illustrate that although acylsugars are fairly simple molecules, considerable 127

diversity can occur as a result of acylation pattern and the length and structure of the 128

acyl donors. 129

130

Until recently, genes required for the assembly of acylsugars remained elusive. 131

However, a combination of metabolite profiling of introgression lines of tomato, coupled 132

with positional cloning and RNAi screens of trichome expressed genes, identified four 133



7

acylsugar acyltransferases (SlASAT1 - SlASAT4) that belong to the BAHD 134

acyltransferase superfamily (Schilmiller et al., 2012; Schilmiller et al., 2015; Fan et al., 135

2016). Biochemical characterization revealed that these ASATs sequentially catalyze 136

the esterification of acylchains at the R4, R3, R3´, and R2 positions of sucrose to 137

generate a tetra-acylsucrose and their activities with different substrates is sufficient to 138

explain the structures of S. lycopersicum acylsugars (Fig. 1A) (Ghosh et al., 2014; Fan 139

et al., 2016). Furthermore, a combination of gene duplication, gene loss and allelic 140

variation at the asat2, asat3 and asat4 loci determine much of the chemical diversity 141

observed in the wild tomato species S. habrochaites and S. pennellii (Kim et al., 2012; 142

Schilmiller et al., 2012; Schilmiller et al., 2015; Fan et al., 2016). 143

144

The trichomes of Petunia spp. synthesize large quantities of acylsugars and UHPLC-MS 145

analysis identified >100 acylsucroses in P. axillaris, P. exserta and P. integrifolia (Liu et 146

al., 2017). Twenty-nine of these acylsugars were purified and their structures 147

determined by NMR. Together, these approaches revealed that petunia synthesizes a 148

mixture of neutral and malonated acylsugars. Each acylsugar contains four acyl chains 149

esterified to the pyranose ring at the R2, R3, R4 and R6 positions and, depending on 150

the species, a single malonate ester can be formed on the furanose ring at either the 151

R1´ or R6´ position (Fig. 1B; Liu et al., 2017). In petunia, the length of the acyl groups 152

ranges from C4 to C8, and NMR analyses revealed that the structures of these groups 153

were a mixture of iC4, iC5, iC6, iC7, and iC8 together with aiC5 and aiC6 (Fig. 1B). 154

However, these acyl groups are not equally represented across the acylsugars as aiC5 155

predominates, whereas iC4, iC5 and aiC6 are relatively minor components. NMR 156

analyses also revealed that the medium chain length acyl groups (C6-C8) are almost 157

exclusively esterified to the R3 position of sucrose whereas the shorter chain acyl 158

groups (C4 and C5) are located on the R2, R4 and R6 positions. Thus, petunia 159

synthesizes a suite of acylsugars that are completely distinct to those found in tomato 160

and these differences are manifest through acyl chains of different lengths and 161

conformation that are esterified to different positions of sucrose. 162

163



8

With the exception of tomato and closely related wild relatives, the enzymes required for 164

acylsugar assembly remain unknown. As petunia synthesizes a completely different 165

suite of acylsugars than tomato, with acyl chains of different lengths that are esterified 166

at alternative positions on the sucrose molecule, it was hypothesized that the 167

mechanism of acylsugar assembly would differ between the two species. This 168

hypothesis was tested and confirmed through the identification and characterization of 169

four ASATs that are required for assembly of tetra-acylsucroses in P. axillaris. Notably, 170

the order of acylsugar assembly differs between tomato and petunia and the 171

orthologous relations and biochemical activities of tomato and petunia ASATs are not 172

conserved, suggesting that acylsugar biosynthesis has differentially evolved within 173

diverse members of the Solanaceae family. 174

175

176



9

RESULTS 177

Identification of putative ASATs from P. axillaris 178

The four ASATs from S. lycopersicum, SlASAT1 (Solyc12g006330), SlASAT2 179

(Solyc04g012020), SlASAT3 (Solyc11g067270) and SlASAT4 (Solyc01g105580) were 180

used as query sequences in tBLASTN searches against a de novo transcriptome 181

assembly of P. axillaris that includes transcripts generated from trichomes (Guo et al., 182

2015). Two P. axillaris unigenes, Pax36474 and Pax31629 were recovered that share 183

68 and 61% amino acid identity to SlASAT1 and SlASAT2, respectively. Examination of 184

their expression patterns derived from the transcriptome data, which included callus, 185

whole seedlings, shoot apices, flowers of mixed developmental stages, and trichomes 186

revealed that both Pax36474 and Pax31629, like SlASAT1 and SlASAT2 (Fan et al., 187

2016), are preferentially expressed in trichomes (Supplemental Table S1). Confirmation 188

of trichome enriched expression of Pax36474 and Pax31629 was obtained by real time 189

quantitative reverse transcription PCR (qRT-PCR) in whole petioles, shaved petioles 190

and trichomes, which indicated ~100-fold enrichment in trichomes for both genes when 191

compared to shaved petioles (Fig. 2). A phylogeny of ASAT-related BAHDs constructed 192

using available sequences from across the Solanaceae family confirmed the close 193

relationship between both SlASAT1 and Pax36474 and SlASAT2 and Pax31629 (Fig. 194

3). Furthermore, comparison of approximately ~120 Kb of genomic sequence 195

surrounding the SlASAT1 and Pax36474 loci (Tomato Genome Consortium, 2012; 196

Bombarely et al., 2016) revealed considerable synteny between tomato and P. axillaris 197

within this region suggesting that the genes are orthologous (Supplemental Figure S1). 198

However, no syntenic relationship was observed between the genomic regions of 199

SlASAT2 and Pax31629. Together, these data suggest that Pax36474 and Pax31629 200

P. axillaris unigenes represent candidate ASATs. Two additional P. axillaris unigenes, 201

Pax21699 and Pax39119 were also recovered in tBLASTn searches using SlASAT1 as 202

the query sequence (Fig. 3). These unigenes are more divergent to SlASAT1 than 203

Pax36474, each sharing approximately 38% amino acid identity with the query 204

sequence. In particular, Pax21699 does not appear to possess a putative ortholog in 205

any of the Solanaceae genomes investigated (tomato, potato, pepper) and while a small 206

amount of synteny exists between the corresponding genomic region of petunia and two 207



10

regions of tomato chromosome 2, the latter do not contain any predicted BAHD 208

acyltransferases (Supplemental Figure S2). Similarly, although there is synteny 209

between tomato and petunia in a genomic region that flanks the Pax39119 locus, 210



11

tomato does not contain a putative ortholog of this petunia BAHD acyltransferase 211

(Supplemental Figure S3). Analyses of expression by qRT-PCR revealed that both 212

Pax21699 and Pax39119 are strongly preferentially expressed in trichomes, relative to 213

shaved petioles (Fig. 2). 214

215



12

In tomato, SlASAT3 catalyzes the addition of acyl groups to the 3´ position of the 216

furanose ring, a position that is not acylated in petunia acylsugars (Schilmiller et al., 217

2015; Liu et al., 2017). Reciprocal BLASTP searches and phylogenetic analysis 218

indicated that SlASAT3 is 53% identical, and most closely related to the P. axillaris 219

unigene, Pax16120. However, Pax16120 is not expressed in trichomes (Supplemental 220

Table S1), suggesting that this unigene is unlikely to be involved in acylsugar assembly. 221

Tandem gene duplications are a feature of many plant genes and are particularly 222

prevalent in genes involved in specialized metabolism (Matsuba et al., 2013; Chae et 223

al., 2014; Boutanaev et al., 2015). In tomato, SlASAT4 resides at a locus on 224

chromosome 1 that contains two additional BAHD acyltransferases (Schilmiller et al., 225

2012) and similar clustering of tandem duplicates of SlASAT4-related BAHDs occurs in 226

the potato and pepper genomes (Potato Genome Sequencing Consortium, 2011; Kim et 227

al., 2014). In P. axillaris, several unigenes were identified that share approximately 50% 228

amino acid identity to SlASAT4 (Fig. 3) and three of these, Pax24741, Pax28156, and 229

Pax35115 are preferentially expressed in trichomes (Supplemental Table S1). However, 230

qRT-PCR analyses revealed that the transcript abundance of Pax24741, Pax28156, 231

and Pax35115 is enriched between 5 and 18-fold in trichomes compared to shaved 232

petioles, which is in contrast to at least the 100-fold enriched expression of Pax21699, 233

Pax31629, Pax36474, and Pax39119 in P. axillaris trichomes (Fig. 2). Phylogenetic 234

analyses revealed that the SlASAT4-related proteins form a separate clade to those 235

more closely related to SlASAT1, SlASAT2 and SlASAT3 (Fig. 3). 236

237

Silencing of putative ASATs in P. axillaris 238

Based on phylogenetic analyses and their highly enriched (≥100-fold) expression in 239

trichomes (Fig. 2 and 3), the role of four putative ASATs; Pax21699, Pax31629, 240

Pax36474, and Pax39119, in acylsugar biosynthesis was investigated using virus-241

induced gene silencing (VIGS) in P. axillaris. The four candidate P. axillaris ASATs are 242

highly divergent at the nucleotide level and it was possible to identify fragments of each 243

gene ranging from 247 to 375 nucleotides in length that are highly specific for each 244

target. For example, BLASTN searches against P. axillaris transcriptome and genome 245

assemblies (Guo et al., 2015; Bombarely et al., 2016) failed to identify any additional 246



13

nucleotide sequences longer than 19 bp that share 100% identity with each VIGS 247

fragment, indicating that there is very limited potential for off target silencing. Upon 248

silencing, the abundance of each target transcript was reduced by approximately 80-249

90% in silenced lines when compared to those of TRV2 empty vector controls 250

(Supplemental Figure S4). 251

252

Prior analyses using mass spectrometry and NMR spectroscopy revealed that P. 253

axillaris acylsugars contain four acyl groups on the pyranose ring and often possess a 254

malonate ester on the furanose ring (Fig. 1B; Liu et al., 2017). In agreement with these 255

prior findings, the acylsugar profile of petioles of P. axillaris TRV2 empty vector control 256

plants is comprised of approximately 10 compounds and is dominated by the S5 ester 257

S(m)5:26 (m,5,5,5,8) (Fig. 4A and B). Furthermore, the molecular formulae of the 258

acylsugars identified in TRV2 empty vector control plants (Fig. 4A) match those of a 259

number of structurally resolved acylsugars from P. axillaris (Supplemental Table S2). 260

261

Silencing of Pax21699 resulted in qualitative and quantitative changes to the acylsugar 262

profile (Fig. 4A and B). Total acylsugars were reduced in Pax21699 silenced lines by 263

approximately 60%, which was manifest by a reduction in all of the acylsugars detected 264

in TRV2 empty vector lines. In addition, several acylsugars were apparent in the 265

Pax21699 silenced lines that were undetectable in the empty vector lines and each 266

lacks a single C5 acyl group. For example, S(m)5:26 (m,5,5,5,8) is reduced in the 267

silenced lines while S(m)4:21 (m,5,5,8) and S3:18 (5,5,8) increase (Fig. 4A and B and 268

Supplemental Figure S5). These data suggest that Pax21699 possesses ASAT activity 269

and may be responsible for adding a C5 acyl group to the pyranose ring of P. axillaris 270

acylsugars (Fig. 1B). Similarly, silencing of Pax31629 also resulted in an overall 271

reduction in acylsugar levels of approximately 50% and this was accompanied by 272

increased abundance of minor acylsugars containing only C4 or C5 acyl groups, 273

including S4:20 (5,5,5,5) and S4:19 (4,5,5,5) (Fig. 4A and C). These data indicate a shift 274

from the C6-C8 acyl groups in favor of shorter acyl chains. Notably, in structurally 275

resolved acylsugars of P. axillaris, the C6-C8 acyl groups are predominantly esterified 276

to the R3 position of the pyranose ring (Liu et al., 2017). In contrast to silencing 277



14

Pax21699 and Pax31629, which resulted in both qualitative and quantitative changes to 278

the acylsugar profile of P. axillaris trichomes, only quantitative changes were observed 279

following silencing of both Pax36474 and Pax39119 with an overall reduction in 280



15

acylsugar levels of between 50-60% (Fig. 5). Overall, these data suggest the four highly 281

trichome enriched unigenes, Pax21699, Pax31629, Pax36474, and Pax39119, each 282

encoding predicted BAHD acyltransferases, are involved in acylsugar assembly. 283



16

284

Biochemical characterization of P. axillaris ASATs 285

In tomato, SlASAT1 (Solyc12g006330) catalyzes the first step in acylsucrose assembly 286

through the acylation of sucrose at the R4 position, using several acyl-CoA donors (Fan 287

et al., 2016). As the P. axillaris unigene, Pax36474, is the putative ortholog of SlASAT1 288

(Fig. 3 and Supplemental Figure S1), it was hypothesized that this enzyme would also 289

catalyze the initial acylation of sucrose. However, Pax36474 failed to catalyze acylation 290

of sucrose using several acyl-CoA donors (C4–C8 in length), including aiC5, which 291

represents the most frequent acyl group esterified to the R4 position of P. axillaris 292

acylsugars (Fig.1B and Supplemental Table S3; Liu et al., 2017). The failure of 293

Pax36474 to utilize sucrose as a substrate indicated that this enzyme does not possess 294

ASAT1 activity, suggesting that the assembly of acylsugars differs between tomato and 295

petunia and prompting investigation of the activity of the additional putative P. axillaris 296

ASATs, Pax21699, Pax31629, and Pax39119. Only Pax39119 was active with sucrose 297

as an acyl acceptor and led to the synthesis of various monoacylsucroses when 298

supplied with acyl-CoA donors ranging from C5-C8 in length but not with iC4-CoA 299

(Supplemental Figure S6 and Supplemental Table S3). These data suggest that 300

Pax39119 catalyzes a reaction consistent with ASAT1 activity in P. axillaris and we 301

therefore renamed this protein PaxASAT1. Notably, different retention times were 302

observed for the S1:5 products generated by SlASAT1 and PaxASAT1, using either iC5 303

or aiC5 as acyl donors, suggesting that the acyl groups are not esterified to the same 304

position of sucrose (Fig. 6). To determine the position at which PaxASAT1 acylates 305

sucrose, a reaction using sucrose and aiC5 was scaled up to generate sufficient 306

material for purification and structural determination by NMR spectroscopy. Subsequent 307

heteronuclear single-quantum correlation spectroscopy (HSQC) together with 308

correlation spectroscopy (COSY) NMR spectra revealed that PaxASAT1 catalyzes the 309

addition of the acyl group to the R2 position of sucrose, which is in contrast to SlASAT1 310

that catalyzes addition at the R4 position (Fan et al., 2016; Fig. 6E and Supplemental 311

Table S4). 312

313



17

To define the second step in acylsucrose assembly, the S1:5 (aiC5R2) product 314

generated with PaxASAT1 was utilized as a substrate together with acyl-CoA donors, 315

ranging from C4 – C8 in length, in sequential reactions with one of the additional 316



18

putative P. axillaris ASATs, Pax21699, Pax31629, or Pax36474. Only Pax36474 317

acylated S1:5 (aiC5R2) and the enzyme was active with iC4-CoA, iC5-CoA, aiC5-CoA, 318

and iC6-CoA acyl donors, indicating that it possesses PaxASAT2 activity (Fig. 7A and 319



19

Supplemental Table S3). Synthesis of S2:10 (aiC5R2, aiC5), formed through sequential 320

reactions of sucrose and aiC5-CoA catalyzed by PaxASAT1 and PaxASAT2, was 321

scaled up and the product purified by preparative HPLC and its structure determined by 322

NMR spectroscopy. The resulting NMR spectra (Supplemental Table S5) revealed that 323

the two acyl groups of S2:10 are esterified to the R2 and R4 positions of sucrose, 324

yielding S2:10 (aiC5R2, aiC5R4). This is consistent with structural characterization of 325

acylsucroses from P. axillaris indicating that while aiC5 is the predominant acyl group at 326

the R4 position, iC4-CoA can also be incorporated (Liu et al., 2017). However, enzyme 327

activity assays (Supplemental Table S3) suggest that, at least in vitro, PaxASAT2 328

possesses greater catalytic promiscuity with respect to the acyl-donor substrate than is 329

observed in the acylsugar profile in planta. 330

331

Sequential reactions were subsequently performed with PaxASAT1 and PaxASAT2 and 332

either Pax21699 or Pax31629. These reactions revealed that tri-acylsucroses were only 333

formed in the presence of Pax31629 using iC6, iC7 and iC8 as acyl-CoA donors but not 334

iC4, or aiC5 CoAs, suggesting that this enzyme corresponds to PaxASAT3 (Fig. 7B and 335

Supplemental Table S3). In P. axillaris, these medium chain length acyl groups (C6-C8) 336

are predominantly esterified to the R3 position of acylsucroses and are not present at 337

the R6 position (Liu et al., 2017), the remaining open position on the pyranose ring that 338

can serve as an acyl acceptor once the R2 and R4 positions are occupied in S2:10 339

(aiC5R2, aiC5R4). These data suggest that PaxASAT3 catalyzes the addition of acyl 340

groups to the R3 position of a diacylsucrose, a hypothesis supported by reduced levels 341

of acylsugars containing C6 - C8 groups in Pax31629 VIGS lines (Fig. 4). Furthermore, 342

SlASAT2 (Solyc04g012020), which is phylogenetically closely related to PaxASAT3 343

(Fig. 3), also catalyzes acylation at the R3 position in tomato (Fan et al., 2016). 344

345

P. axillaris acylsugars possess four acyl groups on the pyranose ring (Fig. 1B; Liu et al., 346

2017) and the current biochemical analysis indicates that as the R2, R4, and R3 347

positions are substituted by the activities of Pax39119, Pax36474, and Pax31629, 348

respectively. Thus, the R6 position is the final position of the pyranose ring to be 349

acylated. Silencing of Pax21699 led to an overall reduction in acylsugars that was also 350



20

associated with the accumulation of acylsucroses that lack a C5 chain suggesting that 351

Pax21699 possesses ASAT activity (Fig. 4 and Supplemental Figure S5). Although 352

Pax21699 was inactive with sucrose, S1:5 (aiC5R2) and S2:10 (aiC5R2, aiC5R4) as 353

substrates, tetra-acylsucroses were formed following incubation of Pax21699 with 354

triacylsucroses, generated by the sequential action of PaxASAT1, PaxASAT2, and 355

PaxASAT3, and either iC4 or aiC5-CoAs (Fig. 7C and Supplemental Table S3). These 356

data are congruent with structural characterization of P. axillaris acylsucroses (Fig. 1B; 357

Liu et al., 2017). Pax21699 was also active with S3:16 and S3:17 to yield S4:21 and 358

S4:22 when supplied with aiC5 as an acyl donor (Supplemental Table S3). Together, 359

these data indicate that Pax21699 possesses PaxASAT4 activity and overall all four of 360

the trichome expressed candidate BAHD enzymes demonstrate ASAT activity. 361

362

363



21

DISCUSSION 364

The tremendous chemical diversity observed in plant specialized metabolites is 365

mediated in part by the formation of ester linkages between starter molecules that result 366

in the formation of increasingly complex phytochemicals (D'Auria, 2006; Mugford et al., 367

2009; Nishizaki et al., 2013). Acylsugars are plant specialized metabolites that are 368

synthesized in the glandular trichomes of members of the Solanaceae family and are 369

formed through the direct coupling of primary metabolites or their immediate breakdown 370

products. Glucose or sucrose serve as the backbone of the acylsugar molecule and 371

ester linkages are formed at the various hydroxyl groups of these sugars through the 372

addition of acyl groups derived from metabolism of branched chain amino acids (Kandra 373

et al., 1990; Walters and Steffens, 1990; Slocombe et al., 2008; Ning et al., 2015) and in 374

the case of Petunia spp., the presence of a malonate ester derived from malonyl-CoA, a 375

precursor of fatty acid biosynthesis (Liu et al., 2017). Hence, relative to more structurally 376

complex specialized metabolites, including many alkaloids and terpenoids that are 377

synthesized by multistep pathways involving several enzyme classes (Winzer et al., 378

2012; Lange and Turner, 2013; Bedewitz et al., 2014; Duge de Bernonville et al., 2015), 379

acylsucrose assembly is seemingly simple as only four acylation steps catalyzed by the 380

same class of enzyme, BAHD acyltransferases, are required in S. lycopersicum 381

trichomes to synthesize the characteristic tetra-acylsucroses (Fan et al., 2016). 382

However despite this apparent simplicity and metabolic proximity to primary 383

metabolism, acylsugars with structures depicted in Fig. 1 are not widely distributed 384

across the plant kingdom and thus far are only found in the glandular trichomes of the 385

Solanaceae where expression data indicates their synthesis is restricted to the single 386

glandular cell at the tip of type I and IV trichomes (Schilmiller et al., 2012; Ning et al., 387

2015; Schilmiller et al., 2015; Fan et al., 2016). 388

389

Although acylsugars are structurally simple, chemical complexity is apparent between 390

and within species and this is mediated by varied lengths and conformation of acyl 391

chains (C2-C12) that are esterified to different positions of the sugar backbone, together 392

with catalytic promiscuity of the BAHD acyltransferases that possess the ability to utilize 393

multiple acyl-CoA donors (Ghosh et al., 2014; Schilmiller et al., 2015; Fan et al., 2016; 394



22

Liu et al., 2017). Plant specialized metabolism is highly variable and evolves rapidly, a 395

phenomenon attributed to reduced evolutionary constraints compared to those imposed 396

upon primary metabolism (Milo and Last, 2012). This rapid evolution frequently involves 397

gene duplication, gene loss, and allelic variation that subsequently alter enzyme activity 398

and these phenomena are apparent within the Solanaceae and contribute to the 399

acylsugar phenotype. For example, deletion at the asat4 locus (formerly asat2) in S. 400

pennellii and select accessions of S. habrochaites alters the acylsugar phenotype (Kim 401

et al., 2012; Schilmiller et al., 2012). Similarly, variation at the asat3 locus in the tomato 402

clade also contributes to acylsugar diversity. For example, while the allele from S. 403

lycopersicum acylates a di-acylsucrose on the furanose ring to form a tri-acylsucrose, 404

the allele from S. pennellii acylates a mono-acylsucrose on the pyranose ring to form a 405

di-acylsucrose (Schilmiller et al., 2015). Furthermore, duplication of the asat3 locus in 406

multiple accessions of S. habrochaites coupled with neofunctionalization creates ASATs 407

with altered acyl donor and acyl acceptor specificities that explain much of the acylsugar 408

diversity observed in the species (Kim et al., 2012; Schilmiller et al., 2015). 409

410

Petunia and S. lycopersicum diverged from a common ancestor ~30 million years ago 411

(Sarkinen et al., 2013) and the acylsugar profile of Petunia spp. is completely different 412

to that of Solanum spp. due to the structure of the acyl donors and their locations on the 413

sugar backbone (Ghosh et al., 2014; Liu et al., 2017). This chemical diversity prompted 414

the examination of whether acylsugar assembly is conserved across the Solanaceae 415

and involves putative orthologs of the tomato ASATs or whether additional enzymes 416

have evolved ASAT function in P. axillaris. Utilizing a combination of transcriptome 417

guided candidate gene identification, gene silencing, and biochemical analyses, four 418

trichome expressed BAHD enzymes designated PaxASAT1 - 4 were identified from P. 419

axillaris that are required for acylsugar assembly and whose activities are congruent 420

with the acylsugar profile of the species. For example, Pax39119 / PaxASAT1 can 421

utilize C5, C6, C7 and C8 acyl donors to acylate the R2 position of sucrose 422

(Supplemental Figure S6 and Supplemental Table S4) and NMR based structural 423

characterization of P. axillaris acylsugars indicates that while aiC5 is the most frequent 424

acyl group at this position, iC6 and iC8 acyl groups are present in S4:24[1] (iC6R2, 425



23

iC8R3, aiC5R4, aiC5R6) and S4:24[2] (iC8R2, aiC6R3, aiC5R4, aiC5R6) (Liu et al., 2017). In 426

all structurally resolved P. axillaris acylsugars characterized to date, either an iC4 or 427

aiC5 group is present at the R4 position (Liu et al., 2017) and PaxASAT2, which 428

catalyzes addition to the R4 position, is active with acyl donors up to C6 in length. 429

Silencing of Pax31629 / PaxASAT3 leads to a reduction in acylsugars with C6-C8 acyl 430

chains, which are primarily esterified at the R3 position of the pyranose ring (Fig. 4; Liu 431

et al., 2017). This is accompanied by a small increase in very minor acylsugars that 432

contain four short acyl chains, including S4:18 (4,4,5,5), S4:19 (4,5,5,5), and S4:20 433

(5,5,5,5) (Fig. 4C). In agreement with the hypothesis that PaxASAT3 adds C6-C8 acyl 434

groups to the R3 position of the pyranose ring, recombinant PaxASAT3 was active with 435

iC6, iC7, and iC8 acyl donors but inactive with C4 and C5 acyl donors (Fig. 7B and 436

Supplemental Table S3). Similarly, silencing of Pax21699 / PaxASAT4 leads to a 437

reduction in total acylsugars together with the accumulation of several tri-acylsucroses 438

that lack a C5 acyl group and this enzyme is active with C4 and C5 acyl donors (Fig. 4 439

and Supplemental Table S3). Together, these data indicate a general consensus 440

between the known structures of P. axillaris acylsugars and the observed silencing and 441

biochemical phenotypes. However, the assays performed using recombinant enzymes 442

illustrate broader catalytic potential among the P. axillaris ASATs than is currently 443

observed among the structurally resolved acylsugars from this species. For example, 444

recombinant PaxASAT2 possesses activity with acyl donors up to C6 in length 445

(Supplemental Table S3) whereas only iC4 and aiC5 acyl groups are present at the R4 446

position in structurally resolved P. axillaris acylsugars (Liu et al., 2017). Such 447

discrepancies may simply reflect acylsugar abundance in the species, which typically 448

drives the selection of targets for purification and NMR structural elucidation. 449

Alternatively, a restricted in planta acylsugar profile compared to that obtained from in 450

vitro biochemical activity of a recombinant enzyme may reflect reduced availability of an 451

acyl donor or lower levels of ASAT activity with specific substrates. 452

453

Silencing of each petunia ASAT transcript led to a quantitative reduction in total 454

acylsugar abundance (Fig. 4 and 5). This reduction would be expected, particularly for 455

early steps in the pathway such as that catalyzed by Pax39119 / PaxASAT1, and 456



24

indeed, was previously observed in SlASAT1 silenced lines (Fan et al., 2016). However, 457

in general, metabolic precursors did not accumulate to levels that might be expected 458

based on the extent of reduction of some of the individual acylsugars. For example, 459

while the most abundant petunia acylsucrose, S(m)5:26 (m,5,5,5,8) is reduced by 460

approximately 70% in Pax21699 / PaxASAT4 silenced lines (Fig. 4B), there is only a 461

slight increase in abundance of the predicted precursors S3:18 (5,5,8) and S(m)4:21 462

(m,5,5,8). Similarly, when Pax36474 / PaxASAT2 and Pax31629 / PaxASAT3 were 463

silenced, accumulation of either mono-acylsucroses or di-acylsucroses would be 464

predicted, respectively. However, these intermediary metabolites were not detected in 465

any of the silenced lines. While the underlying reasons for this remain unknown, it is 466

possible that when ASAT activity is reduced by silencing, precursors may be turned 467

over by acylsugar hydrolases or further metabolized to compounds undetected by our 468

metabolite analyses. Together, these processes may contribute to the overall reduction 469

in acylsugars observed in VIGS lines. 470

471

Notable differences exist between the P. axillaris and S. lycopersicum ASATs and their 472

orthologous relationships and acyl acceptor preferences are not fully conserved, leading 473

to altered order of tetra-acylsucrose assembly between the two species (Fig. 8). For 474

example, based on phylogeny (Fig. 3) it was hypothesized that Pax36474 would, like 475

SlASAT1, encode an enzyme with ASAT1 activity that utilizes sucrose as the acyl 476

acceptor and catalyzes the addition of an acyl group to the R4 position of the pyranose 477

ring (Fig. 1A). However, Pax36474 was inactive with sucrose as an acyl acceptor and 478

every acyl donor tested (C4–C8) whereas subsequent biochemical analyses and NMR-479

based structural characterization of reaction products identified Pax39119 as 480

PaxASAT1 that catalyzes the addition of a range of acyl groups to the R2 position of the 481

pyranose ring of sucrose (Supplemental Figure S6, Supplemental Tables S3 and S4). 482

Thus, rather than initiation at the R4 position, as in tomato, acylsugar assembly in P. 483

axillaris begins with acyl chain addition at the R2 position and subsequent acylations at 484

the R4, R3 and R6 positions completes tetra-acylsucrose assembly. This is in contrast 485

to the sequence of acylsugar assembly in S. lycopersicum, which occurs through 486

sequential acylations at the R4, R3, R3ʹ, and R2 positions (Fan et al., 2016; Fig. 8). 487



25

These data indicate that primary sequence is not a good predictor of ASAT substrate 488

preference as SlASAT1 / Solyc12g006330 of tomato utilizes sucrose as an acyl 489

acceptor whereas Pax36474 has ASAT2 activity and utilizes a mono-acylsucrose 490

substrate. This shift in substrate preference is also observed between SlASAT2 / 491

Solyc04g012020 and Pax31629 / PaxASAT3 which are phylogenetically related and 492

share approximately 61% amino acid identity (Fig. 3). While SlASAT2 utilizes a mono-493

acylsucrose as an acyl acceptor (Fan et al., 2016), PaxASAT3 utilizes a di-acylsucrose 494

(Fig. 7B). Despite these changes in acyl acceptor specificity between related P. axillaris 495

and tomato ASATs, SlASAT1 and PaxASAT2 both acylate at the R4 position of the 496

pyranose ring, while SlASAT2 and PaxASAT3 each catalyze additions to the R3 497

position. These data suggest that sequence conservation between ASATs of diverse 498

species may be a useful predictor of acylation position. Indeed, structure function 499

analyses of ASATs from tomato and closely related wild species has proven to be a 500

powerful approach to identify amino acid residues that specify substrate preferences 501



26

(Fan et al., 2016). However, given the evolutionary distance between petunia and 502

tomato and the fairly low sequence identity of their ASATs, additional comparisons 503

between putative ASATs of diverse species from across the Solanaceae phylogeny will 504

likely be required to enhance the power of this approach. Alternatively, resolving the 505

structures of ASATs bound to their substrates may reveal the underlying biochemical 506

changes that have led to the ability of seemingly orthologous enzymes to evolve new 507

substrate preferences. 508

509

While sequence conservation is observed between SlASAT1 and PaxASAT2 and 510

between SlASAT2 and PaxASAT3, additional PaxASATs are less well conserved. For 511

example, P. axillaris does not appear to contain a putative ortholog of SlASAT3, which 512

is in agreement with the lack of a branched acyl group on the furanose ring of 513

acylsugars from this species (Liu et al., 2017). Similarly, additional ASATs, are not fully 514

conserved across the Solanaceae. For example, Pax39119 / PaxASAT1 is 72% 515

identical to Ca06g15270, a predicted BAHD from pepper, although no closely related 516

proteins are found in tomato or potato (Fig. 3). In addition, while putative orthologs of 517

Pax31629 / PaxASAT3 are readily identifiable in tomato, potato and pepper, putative 518

orthologs of Pax36474 / PaxASAT2 are present in tomato and potato but not pepper 519

(Fig. 3). In contrast, Pax21699 / PaxASAT4 is more divergent, sharing less than 40% 520

identity to the most closely related sequences from tomato, potato, and pepper, 521

suggesting that a putative ortholog of this gene is likely absent from these species. 522

While, the functions of the putative ASATs from potato and pepper need to be 523

characterized to determine whether they are involved in acylsugar biosynthesis, the lack 524

of complete conservation of the ASATs, and related BAHDs across the Solanaceae 525

(Fig. 3) reflects the plasticity of specialized metabolism which frequently involves gene 526

duplication and loss (Pichersky and Lewinsohn, 2011; Chae et al., 2014). 527

528

Although four P. axillaris ASATs have been identified that can explain much of the 529

acylsugar diversity within this species, there are ASAT activities in P. axillaris that 530

remain to be identified. For example, many P. axillaris acylsugars possess an unusual 531

malonate ester on the furanose ring at the R1ʹ position that has thus far not been 532



27

detected in acylsugars of other members of the Solanaceae (Liu et al., 2017). However, 533

despite our efforts to identify the ASAT activity responsible for adding this malonate 534

group, the enzyme remains unknown. Thus, it is unclear at what step in acylsugar 535

assembly the malonate group is added and whether this may affect ASAT activity. 536

However, our favored hypothesis is that malonylation is the final step in acylsugar 537

assembly in Petunia spp. as neutral and malonate ester forms of multiple acylsugars 538

coexist. For example, S(m)5:25 (m,5,5,5,7) is present with S4:22 (5,5,5,7) in P. axillaris 539

trichomes and both S(m)5:26 (m,5,5,5,8) and S4:23 (5,5,5,8) occur in the trichomes of 540

P. exserta (Liu et al., 2017). In addition, the enzyme responsible for catalyzing the 541

esterification of either a C4 or C5 acyl group to the R3 position of the low abundance 542

acylsucroses that accumulate in Pax31629 / PaxASAT3 silenced lines; S4:18 (4,4,5,5), 543

S4:19 (4,5,5,5), and S4:20 (5,5,5,5), is uncharacterized and further experimentation will 544

be required to confirm its identity. 545

546

Although there has been a longstanding interest in the role of acylsugars in plant 547

defense (Goffreda et al., 1989; Buta et al., 1993; Chortyk et al., 1997), until relatively 548

recently, the enzymes involved in trichome-derived acylsucrose assembly remained 549

unknown. A combination of genetic- and genomics-enabled biochemistry led to the 550

identification of several BAHDs from tomato and closely related wild species that are 551

involved in acylsugar assembly and chemical diversity (Kim et al., 2012; Schilmiller et 552

al., 2012; Schilmiller et al., 2015; Fan et al., 2016). The current study utilized the tomato 553

ASATs as a framework to explore the potential conservation of acylsugar assembly. 554

Acylsugar composition differs between tomato and Petunia spp. and although four 555

trichome-expressed ASATs were identified from P. axillaris that can explain much of the 556

acylsugar diversity within this species, the data indicate that the genes encoding ASATs 557

are not fully conserved across the Solanaceae and that considerable variation exists in 558

substrate preference of tomato and P. axillaris ASATs as well as the mechanism of 559

acylsucrose assembly between these two species. These data expand the existing 560

knowledge of acylsugar biosynthesis in plants, highlighting the evolutionary complexity 561

that contributes to the chemical diversity of these structurally simple specialized 562

metabolites. Additional studies are required using species from across the Solanaceae 563



28

to determine the extent of acylsugar chemical diversity, their assembly, and the 564

biochemical evolution of ASATs. 565

566

567



29

METHODS 568

Plant Material and Growth Conditions 569

Seeds of Petunia axillaris (PI667515) were obtained from the Germplasm Resources 570

Information Network. Plants were grown in four inch pots in peat-based compost 571

supplemented with half-strength Hoaglands solution in a growth room under a 16 h 572

photoperiod (145 μmol m-2 s-1) at a constant temperature of 24°C. 573

574

Multiple Sequence Alignments and Phylogenetic Analyses 575

Sequence analysis was performed using MEGA version 5 (Tamura et al., 2011). Amino 576

acid alignments were generated using MUSCLE (Edgar, 2004) and phylogenetic trees 577

constructed using the Maximum Likelihood method and the Jones-Taylor-Thornton 578

model. A bootstrap test of 2000 replicates was used to assess the reliability of the 579

phylogeny. Amino acid alignments used to construct phylogenetic trees are available in 580

Supplemental Dataset S1. 581

582

Virus-induced Gene Silencing 583

Constructs were assembled in TRV2-LIC vector as previously described (Dong et al., 584

2007) using the primers in Supplemental Table S6. VIGS experiments were performed 585

as described by (Velasquez et al., 2009). P. axillaris first true leaf was inoculated with 586

Agrobacterium tumefaciens strain GV3101 cultures. Plants inoculated with A. 587

tumefaciens carrying the TRV2-LIC empty vector were used as controls and 588

TRV2::PHYTOENE DESATURASE plants were used to monitor the progression of 589

gene silencing. Plants were grown as described above. 10 mm petiole segments were 590

harvested from the fifth true leaf of five week-old plants for acylsugar profiling and 591

trichomes for RNA extraction were harvested from frozen petioles by brushing and 592

collection directly into liquid nitrogen. 593

594

RNA Extraction, cDNA Synthesis and Quantitative RT-PCR 595

Total RNA was extracted from tissues of P. axillaris using the RNeasy Plant Mini Kit and 596

subjected to on column DNase treatment (Qiagen). cDNA was synthesized from 800 ng 597

of total RNA using the SuperScript III first-strand synthesis kit (Invitrogen). Following 598



30

synthesis, cDNAs were column purified and their quantity and quality determined by UV 599

absorbance. Gene-specific primers (Supplemental Table S6), were designed using 600

Primer Express 3.0 software (Applied Biosystems) and primers from petunia EF1α 601

(Mallona et al., 2010) were utilized for normalization. Each primer pair was validated to 602

ensure that the amplification efficiencies of each target gene were similar to the EF1α 603

endogenous control using serial dilutions of cDNA synthesized from trichome RNA. 604

Only primer pairs that had an absolute value of the slope of ΔCT versus log of the input 605

cDNA concentration of ≤ 0.1 were utilized. Experiments to determine the relative 606

expression of target genes in trichomes versus shaved stems were performed using 20 607

ng of cDNA template while those investigating the efficiency of gene silencing were 608

performed with 30 ng of cDNA template. 10 µl PCR reactions containing 2X FAST 609

SYBR Master Mix (Applied Biosystems), cDNA template and 300 nM of each primer 610

were assembled using a Biomek 3000 liquid handler and amplified using an Applied 611

Biosystems ABI Prism 7900HT Real-Time PCR System. Amplification conditions were 612

as follows: 2 min at 50°C and 10 min at 95°C, followed by 40 cycles of 15 s at 95°C and 613

1 min at 60°C. Data were analyzed using the ΔΔCT method to generate relative 614

expression values. 615

616

Acylsugar Profiling by Liquid Chromatography Mass Spectrometry 617

For acylsugar profiling, 10 mm segments of petioles were placed in 1 ml of extraction 618

solvent (acetonitrile/isopropanol/water in 3:3:2 v/v/v) containing 0.1% formic acid and 5 619

μM telmisartan as an internal standard. Samples were gently agitated for 1 min and the 620

solvent transferred to HPLC vials. The acylsugar extracts were analyzed using a 621

Shimadzu LC-20AD HPLC system connected to a Waters LCT Premier ToF-MS. 10 μL 622

of sample was injected onto a fused core Ascentis Express C18 column (2.1 mm X 10 623

cm, 2.7 μm particle size) for reverse-phase separation. Column temperature was set to 624

50°C. The flow rate was set at 0.3 mL/min and start conditions were 99% solvent A (10 625

mM ammonium formate pH 2.8) and 1% solvent B (acetonitrile). The 20 min elution 626

gradient was as follows: ramp to 60% B at 1.25 min, 90% B at 12.5 min and to 100% B 627

at 15 min. Hold at 100% B up to 19 min and return to 1% B at 19.01 min and hold up to 628

20 min. The MS parameters employed electrospray ionization and were as described in 629



31

(Schilmiller et al., 2015). Five separate acquisition functions were utilized to generate 630

spectra at different collision potentials (10, 25, 40, 55 and 80 V) providing both non-631

fragmenting and a range of fragmenting conditions. Acylsugar abundances were 632

determined using the Waters QuanLynx analysis tool to integrate extracted ion 633

chromatogram peak areas relative to the peak area of the internal standard. 634

Representative samples (Fig. 4A and Supplemental Figure S5) were analyzed using a 635

Waters Acquity UPLC system connected to Waters Xevo G2-S QToF LC/MS. 636

Chromatography conditions were identical to those described above except that the 20 637

min elution gradient was modified slightly such that 100% acetonitrile was maintained 638

from 12.5 - 18 min followed by 1% acetonitrile from 18.01 - 20 min. 639

640

Synthesis of Acyl-CoA Thioesters 641

Isobutyryl-CoA (iC4-CoA) and Isovaleryl-CoA (iC5-CoA) were purchased from Santa 642

Cruz Biotechnology and Sigma-Aldrich, respectively. Additional acyl-CoA thioesters 643

were synthesized from their cognate fatty acids using a carbonyldiimidazole method 644

(Kawaguchi et al., 1981) with modifications outlined in (Schilmiller et al., 2015). 2-645

methylbutyric acid (aiC5), 4-methylpentanoic acid (iC6), and 5-methylhexanoic acid 646

(iC7) were purchased from Sigma-Aldrich and 6-methylheptanoic acid (iC8) and 647

Coenzyme A tri-lithium salt (CoA) were obtained from BOC Sciences and Crystal Chem, 648

respectively. The concentrations of the resulting acyl-CoAs were obtained by UV 649

spectroscopy using the CoA extinction coefficient of 16,400 at 260 nm. 650

651

Recombinant Expression of BAHD Acyltransferases and Enzyme Assays 652

Full-length open reading frames of candidate ASAT enzymes were amplified from P. 653

axillaris trichome cDNA using the primers described in Supplemental Table S6. Linkers 654

containing either the NheI or NdeI together with BamHI or SalI were added to permit 655

sub-cloning of the fragments into the pET28b vector (EMD Millipore). Constructs were 656

transformed into BL21 Rosetta Cells (EMD Millipore) for recombinant protein 657

production. His-tagged protein production was induced in E. coli cultures by 0.05 mM 658

isopropyl β-D-1-thiogalactopyranoside for 16 h at 16°C. Soluble protein was partially 659

purified by nickel-affinity chromatography as previously described (Schilmiller et al., 660



32

2012). Enzyme assays were performed for 30 min at 30°C in a 30 μL volume containing 661

50 mM ammonium acetate (pH 6.0) with 100 µM of an appropriate acyl-CoA donor and 662

1 mM sucrose as the acyl acceptor. Assays were terminated by addition of 60 μL 663

acetonitrile/isopropanol/formic acid (1:1:0.001) containing 10 μM propyl-4-hydroxy 664

benzoate internal standard and centrifugation at 13,000 g for 10 min. 665

666

For sequential enzyme assays, heat inactivation of previous enzyme activity was 667

achieved by incubation at 65°C for 5 min followed by cooling on ice and the subsequent 668

addition of an appropriate acyl-CoA donor (100 µM) and a candidate ASAT enzyme. 669

Enzyme reactions were terminated as previously described (Schilmiller et al., 2015). 670

Acylsugars produced in vitro together with representative samples from plant extracts 671

were analyzed using a Waters Xevo G2-S QToF LC-MS interfaced to a Waters Acquity 672

UPLC system. 10 µL of leaf dip extract was injected onto a fused core Ascentis Express 673

C18 column (5 cm x 2.1 mm, 2.7 µm particle size) interfaced to a Waters Acquity UPLC 674

system. Column temperature was maintained at 40°C. The start conditions were 95% A 675

and 5% solvent B with flow rate set to 0.3 mL/min. The 7 min linear gradient was as 676

follows: ramp to 60% B at 1 min, then to 100% B at 5 min, hold at 100% B to 6 min, 677

return to 95% A at 6.01 min and hold until 7 min. The MS settings are identical to 678

Schilmiller et al., 2015. Three acquisition functions were set up to generate spectra at 679

different collision potentials (5, 25, and 60 V). The method and MS parameters for 680

electrospray ionization in both positive and negative-ion modes are similar except that in 681

positive-ion mode the capillary voltage was 2.61 kV. LC-MS/MS in negative-ion mode 682

was used to determine the fragmentation of selected acylsucrose products from enzyme 683

assays detected as m/z 555.2, 667.3 and 751.4 under the same conditions as above 684

but with a single acquisition function at collision potential of 6.0 V and acquisition mass 685

range from m/z 50 - 600, 700 and 800, respectively. 686

687

Collision-induced dissociation MS in negative ion mode was used to obtain acylsugar 688

structure information about the number and length of acyl chains according to the 689

carboxylate fragment ion masses whereas MS in positive ion mode was used to cleave 690

the glycosidic bond linking the sucrose pyranose and furanose rings and obtain 691



33

information on the number and length of acyl chains present on each ring as previously 692

described (Schilmiller et al., 2010; Ghosh et al., 2014). 693

694

Analysis of Monoacylsucroses 695

To analyze the shift in retention time of monoacylsucrose (S1:5) products formed by 696

PaxASAT1 and SlASAT1, reaction products were analyzed using a Waters Acquity 697

UPLC system connected to Waters Xevo G2-S QToF LC/MS. 10 µL of reaction product 698

was injected into a fused core ACQUITY UPLC Ethylene Bridged Hybrid (BEH) amide 699

column (2.1 mm X 10 cm, 2.7 μm particle size; Waters) with column oven set to 40°C. 700

The flow rate was 0.4 mL/min with initial conditions at 5% solvent A (0.15% formic acid) 701

and 95% B (acetonitrile). The 9 min elution gradient was as follows: hold at 5% A to 1 702

min, then ramp to 40% A at 6 min, ramp to 95% A at 7 min, return to 5% A at 7.01 min 703

and hold until 9 min. The MS parameters were as described in (Schilmiller et al., 2015) 704

except that the mass range was m/z 50 to 1000 and five separate acquisition functions 705

were utilized to generate spectra at different collision potentials (10, 25, 40, 55 and 80 706

V). 707

708

Purification of Acylsugars and Structural Elucidation by NMR 709

1 L cultures of E. coli expressing either PaASAT1 or PaASAT2 were induced and 710

protein was extracted and purified as described above. Enzyme assays with PaASAT1 711

to form S1:5 (aiC5) were performed in a 30 mL reaction volume containing 50 mM 712

ammonium acetate (pH 6.0), 0.66 mM sucrose and (50 μM) aiC5-CoA at 30°C for 3 713

hours. For the sequential assay with PaASAT2 to form S2:10 (aiC5, aiC5), PaASAT1 714

was inactivated at 65°C for 1 h, the reaction was cooled on ice, centrifuged, and 1.8 mL 715

of 0.5 mM aiC5-CoA (30 μM) and PaASAT2 were added and the reaction incubated for 716

3 h at 30°C. Reactions were terminated by addition of 60 mL 717

acetonitrile/isopropanol/formic acid (1:1:0.001), followed by centrifugation at 4500 rpm 718

for 10 min. Solvent was evaporated to dryness and the residue dissolved in 1 mL of 719

water. 720

721



34

S1:5 (aiC5) and S2:10 (aiC5, aiC5) purification was performed using a Waters 2795 722

HPLC and a Thermo Scientific Acclaim 120 C18 semi-preparative HPLC column (4.6 × 723

150 mm, 5.0 μm particle size). The mobile phase consisted of 0.15% formic acid in 724

water (Solvent A), and acetonitrile (Solvent B) with flow rate of 1.5 mL/min. For 725

purification of S1:5, a linear gradient consisted of 1% solvent B at 0 min, 8% solvent B 726

at 3 min, 9% solvent B at 11 min, and 100% solvent B at 12 min. Solvent composition 727

was held at 100% solvent B for 12 to 14 min and then brought back to 1% solvent B at 728

15 min and held at 1% solvent B for 15 to 16 min. For purification of S2:10, a 40 min 729

method with a linear gradient consisted of 1% solvent B at 0 min, 8% solvent B at 3 min, 730

9% solvent B at 11 min, 17% solvent B from 12 to 35 min, ramped to 18% solvent B at 731

35 min and then to 100% solvent B at 36 min and held at 100% solvent B until 38 min 732

and returned to 1% solvent B at 39 min and held till 40 min. Eluted fractions of S1:5 733

were collected in 1 min fractions for 5 injections and 8 injections for S2:10, using an 734

injection volume of 200 μL for each injection. The desired compound was collected in 7 735

to 10 min for S1:5 and 23 min for S2:10 and evaporated to dryness. The residue was 736

dissolved in 1 mL of water with sonication for 10 min followed by transfer to a 737

polypropylene centrifuge tube and centrifugation at 3000 g for 2 min at 25°C. 738

Supernatants were collected in HPLC vials with glass low-volume inserts. Purified 739

acylsugars were dissolved in 250 μL D2O and transferred into Shigemi solvent-matched 740

NMR tubes. NMR spectra were recorded using a Bruker Avance 900 NMR 741

spectrometer equipped with a TCI triple-resonance inverse detection cryoprobe at the 742

Michigan State University Max T. Rogers NMR facility. NMR experiments measured: 1H 743

(899.13 MHz), COSY and heteronuclear single-quantum correlation (HSQC) 744

spectroscopy (F1: 226.09 MHz, F2: 899.13 MHz). Acylsugar substitution patterns were 745

determined by chemical shifts of H based on 1H and HSQC. 746

747

Data Availability and Accession Numbers 748

A P. axillaris transcriptome assembly and associated sequences are available under 749

GenBank/EMBL/DDBJ BioProject PRJNA261953 (Guo et al., 2015). Sequences of P. 750

axillaris ASATs are deposited in GenBank under the following accession numbers: 751



35

PaxASAT1 (KT716258), PaxASAT2 (KT716259), PaxASAT3 (KT716260), and 752

PaxASAT4 (KT716261). 753

754

Supplemental Data 755

Supplemental Figure S1. Synteny between the SlASAT1 and Pax36474 genomic 756

regions. 757

Supplemental Figure S2. Synteny between the Pax21699 genomic region of P. 758

axillaris and two separate regions of tomato chromosome 2. 759

Supplemental Figure S3. Synteny between tomato and P. axillaris within a region that 760

flanks the Pax39119 locus. 761

Supplemental Figure S4. Transcript abundance in candidate ASAT-silenced lines. 762

Supplemental Figure S5. Mass spectra of acylsugars that accumulate in 763

TRV2::Pax21699 silenced lines. 764

Supplemental Figure S6. Activity of PaxASAT1 with multiple acyl-CoA donors. 765

Supplemental Table S1. Putative ASATs identified from P. axillaris transcriptome data. 766

Supplemental Table S2. P. axillaris acylsugars detected in petioles of P. axillaris. 767

Supplemental Table S3. In vitro activities of candidate ASAT enzymes of P. axillaris. 768

Supplemental Table S4. NMR chemical shifts of S1:5 (aiC5) produced in vitro by 769

PaxASAT1. 770

Supplemental Table S5. NMR chemical shifts of S2:10 (aiC5) produced in vitro by 771

sequential action of PaxASAT1 and PaxASAT2. 772

Supplemental Table S6. Oligonucleotide primers utilized in this study. 773

774

ACKNOWLEDGMENTS 775

We thank members of the Solanum Trichome Project (www.trichome.msu.edu), 776

particularly Matthew Bedewitz, Tony Schilmiller, and Pengxiang Fan, for sharing 777

materials and providing advice and Krystle Wiegert-Rininger for assistance with RNA 778

isolation. We also thank the MSU RTSF Mass Spectrometry and Metabolomics Core 779

Facility and Kermit Johnson and Dan Holmes of the MSU Max T. Rogers NMR facility 780

for assistance with collecting NMR spectra. 781

782 783



36

Figure Legends 784

Figure 1. Acylsucroses from S. lycopersicum and P. axillaris. A, Structures of 785

characteristic tetra-acylsucroses from S. lycopersicum. Details of the length of the acyl 786

chains typically found at each position in the most abundant metabolites are provided 787

together with the identity of the ASAT enzymes responsible for acylsucrose assembly 788

and the order in which they catalyze acylation reactions. Data represented are 789

summarized from (Ghosh, 2014; Schilmiller, 2012; Schilmiller, 2015; Fan et al., 2016). 790

B, Structures of characteristic acylsucroses from P. axillaris. Details of the length of the 791

acyl chains typically found at each position are derived from NMR-based structural 792

characterization (Liu et al., 2017). The order of assembly of P. axillaris acylsucroses 793

and the identification of the corresponding ASAT enzymes is the subject of this study. 794

795

Figure 2. Expression analysis of putative P. axillaris ASATs. Expression of candidate 796

ASATs was determined in whole petioles, shaved petioles with trichomes removed, and 797

trichomes of P. axillaris. Three biological and three technical replicates for each sample 798

were analyzed. Data are presented as the mean expression values ± SE relative to that 799

observed in shaved stems. Values labeled with different letters are significantly different 800

(least square means, P < 0.05). 801

802

Figure 3. Phylogenetic analysis of putative ASATs. An unrooted phylogenetic tree of 803

known S. lycopersicum (tomato) ASATs together with related amino acid sequences 804

from S. lycopersicum, S. tuberosum (potato), Capsicum annuum (pepper), and P. 805

axillaris was constructed using the Maximum Likelihood method from a multiple 806

sequence alignment of deduced full-length amino acid sequences. The tree was 807

constructed using MEGA V5.0 and bootstrap values ≥ 50 are shown from 2000 808

replicates. Known tomato ASATs are shown in red and putative trichome preferentially 809

expressed ASATs from P. axillaris are in blue. Subsequent functional characterization of 810

the putative P. axillaris ASATs reported herein led to the identification of four enzymes 811

involved in acylsugar assembly, PaxASAT1 – 4. The position on the sucrose molecule 812

where addition of acyl chains occurs following ASAT mediated catalysis are provided in 813

parentheses. 814



37

815

Figure 4. The P. axillaris acylsugar profile is altered by silencing of Pax21699 and 816

Pax31629. A, Comparison of the acylsugar profile of P. axillaris expressing either TRV2 817

empty vector, TRV2::Pax21699 or TRV2::Pax31629 constructs. Negative-ion mode total 818

ion current LC/MS chromatograms are shown, indicating both reduced [e.g. 819

S(m)5:26(m,5,5,5,8)] and increased [e.g. S3:18(5,5,8), S(m)4:21(m,5,5,8), 820

S4:19(4,5,5,5) and S4:20(5,5,5,5)] abundance of individual acylsugars in 821

TRV2::Pax21699 and TRV2::Pax31629 silenced lines. The peak corresponding to a 5 822

µM telmisartan internal standard is labelled IS. Details of individual acylsugars are 823

provided in Supplemental Table S2 and Supplemental Figure S5. B and C, 824

Quantification of acylsugar levels in TRV2::Pax21699 and TRV2::Pax31629 silenced 825

lines. The abundance of individual and total (inset) acylsugars in TRV2::Pax21699 and 826

TRV2::Pax31629 silenced lines relative to those in TRV2 empty vector controls are 827

shown. Data are presented as peak area normalized to dry weight and internal standard 828

peak area and represent the mean ± SE of 12 biological replicates. 829

830

Figure 5. P. axillaris acylsugar levels are reduced in Pax36474 and Pax39119 silenced 831

lines. The abundance of individual and total (inset) acylsugars in A, TRV2::Pax36474 832

and B, TRV2::Pax39119 silenced lines relative to those in TRV2 empty vector controls 833

are shown. Data are presented as peak area normalized to dry weight and internal 834

standard peak area and represent the mean ± SE of 12 biological replicates. 835

836

Figure 6. ASAT1 activity is not conserved in P. axillaris and S. lycopersicum. A, In vitro 837

formation of S1:5 by recombinant S. lycopersicum ASAT1 (SlASAT1) and P. axillaris 838

ASAT1 (PaxASAT1) using sucrose as the acyl acceptor and either iC5-CoA or aiC5-839

CoA as acyl donors. Negative-ion mode LC/MS extracted ion chromatograms for the 840

reaction product m/z 461.1 (S1:5; [M+Cl]−) are shown. The vertical dashed line 841

highlights a retention time shift of S1:5 products formed by SlASAT1 and PaxASAT1, 842

suggesting that different S1:5 isomers are formed by these enzymes. B, Structure of the 843

S1:5 reaction products formed by SlASAT1 and PaxASAT1 using iC5-CoA and aiC5-844

CoA, respectively. Data for S1:5(iC5R4) formed by SlASAT1 are based on prior 845



38

structural characterization (Schilmiller et al., 2015; Fan et al., 2016) while the structure 846

of S1:5(aiC5R2) was determined by NMR (Supplemental Table S4). 847

848

Figure 7. Identification of ASAT2, ASAT3 and ASAT4 activities of P. axillaris. A, In vitro 849

formation of S2:10 by recombinant P. axillaris ASAT2 (PaxASAT2) using S1:5 (aiC5R2) 850

as the acyl acceptor and aiC5-CoA as the acyl donor. Negative-ion mode LC/MS 851

extracted ion chromatogram for the reaction product m/z 555.2 is shown. B, In vitro 852

formation of S3:17 by recombinant P. axillaris ASAT3 (PaxASAT3) using S2:10 (aiC5R2, 853

aiC5R4) as the acyl acceptor and iC7-CoA as the acyl donor. Negative-ion-mode LC/MS 854

extracted ion chromatogram for the reaction product m/z 667.3 is shown. In vitro 855

formation of S4:22 by recombinant P. axillaris ASAT4 (PaxASAT4) using S3:17 (aiC5R2, 856

iC7R3, aiC5R4,) as the acyl acceptor and aiC5-CoA as the acyl donor. Negative-ion 857

mode LC/MS extracted ion chromatogram for the reaction product m/z 751.4 is shown. 858

D – F, Tandem mass spectra (LC-MS/MS) of the acylsucroses formed by PaxASAT2, 859

PaxASAT3, and PaxASAT4. Fragmentation of specific reaction products of m/z 555.2, 860

667.3 and 751.4 presented in A – C are shown. Fragmentation in negative mode 861

reveals the length of the acyl chains esterified to the sucrose core due to loss of acyl 862

groups as ketenes. 863

864

Figure 8. Comparison of tetra-acylsucrose assembly in tomato and P. axillaris. A, 865

Structure of a generic tetra-acylsucrose from tomato. B, Structure of a generic 866

acylsucrose from P. axillaris. The four steps required for the formation of tetra-867

acylsucroses in each species are shown. Orthologous enzymes predicted by sequence 868

analysis are indicated by the same color. Note, that the predicted orthologous 869

relationships between SlASAT1 and PaxASAT2 and SlASAT2 and PaxASAT3 are not 870

conserved at the biochemical level, and this, together with presence absence variation 871

of other ASATs between tomato and petunia, results in differential acylsucrose 872

assembly in these two species. 873

874

875

876



39

877



Parsed CitationsArimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factorsand their ultimate functions. Plant and Cell Physiology 50: 911-923

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Arrendale RF, Severson RF, Sisson VA, Costello CE, Leary JA, Himmelsbach DS, Vanhalbeek H (1990) Characterization of thesucrose ester fraction from Nicotiana glutinosa. Journal of Agricultural and Food Chemistry 38: 75-85


Bedewitz MA, Gongora-Castillo E, Uebler JB, Gonzales-Vigil E, Wiegert-Rininger KE, Childs KL, Hamilton JP, Vaillancourt B, YeoYS, Chappell J, DellaPenna D, Jones AD, Buell CR, Barry CS (2014) A root-expressed L-phenylalanine:4-hydroxyphenylpyruvateaminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna. Plant Cell 26: 3745-3762


Bird DA, Franceschi VR, Facchini PJ (2003) A tale of three cell types: Alkaloid biosynthesis is localized to sieve elements in opiumpoppy. Plant Cell 15: 2626-2635


Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012)Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proceedingsof the National Academy of Sciences of the United States of America 109: 20124-20129


Bombarely A, Moser M, Amrad A, Bao M, Bapaume L, Barry CS, Bliek M, Boersma MR, Borghi L, Bruggmann R, Bucher M,D'Agostino N, Davies K, Druege U, Dudareva N, Egea-Cortines M, Delledonne M, Fernandez-Pozo N, Franken P, Grandont L,Heslop-Harrison JS, Hintzsche J, Johns M, Koes R, Lv X, Lyons E, Malla D, Martinoia E, Mattson NS, Morel P, Mueller LA,Muhlemann J, Nouri E, Passeri V, Pezzotti M, Qi Q, Reinhardt D, Rich M, Richert-Pöggeler KR, Robbins TP, Schatz MC, SchranzME, Schuurink RC, Schwarzacher T, Spelt K, Tang H, Urbanus SL, Vandenbussche M, Vijverberg K, Villarino GH, Warner RM,Weiss J, Yue Z, Zethof J, Quattrocchio F, Sims TL, Kuhlemeier C (2016) Insight into the evolution of the Solanaceae from theparental genomes of Petunia hybrida. Nature Plants 2: 16074


Boutanaev AM, Moses T, Zi JC, Nelson DR, Mugford ST, Peters RJ, Osbourn A (2015) Investigation of terpene diversificationacross multiple sequenced plant genomes. Proceedings of the National Academy of Sciences of the United States of America 112:E81-E88


Buta JG, Lusby WR, Neal JW, Waters RM, Pittarelli GW (1993) Sucrose esters from Nicotiana gossei active against the greenhousewhitefly Trialeuroides vaporariorum. Phytochemistry 32: 859-864


Chae L, Kim T, Nilo-Poyanco R, Rhee SY (2014) Genomic signatures of specialized metabolism in plants. Science 344: 510-513Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Chortyk OT, Kays SJ, Teng Q (1997) Characterization of insecticidal sugar esters of Petunia. Journal of Agricultural and FoodChemistry 45: 270-275


Chortyk OT, Severson RF, Cutler HC, Sisson VA (1993) Antibiotic activities of sugar esters isolated from selected Nicotianaspecies. Bioscience Biotechnology and Biochemistry 57: 1355-1356


D'Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Current Opinion in Plant Biology 9: 331-340Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from

Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Arimura G%2C Matsui K%2C Takabayashi J %282009%29 Chemical and molecular ecology of herbivore%2Dinduced plant volatiles%3A Proximate factors and their ultimate functions%2E Plant and Cell Physiology 50%3A 911%2D923&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions. Plant and Cell Physiology 50: 911-923

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

http://scholar.google.com/scholar?as_q=Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions&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=Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Arimura&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Arrendale RF%2C Severson RF%2C Sisson VA%2C Costello CE%2C Leary JA%2C Himmelsbach DS%2C Vanhalbeek H %281990%29 Characterization of the sucrose ester fraction from Nicotiana glutinosa%2E Journal of Agricultural and Food Chemistry 38%3A 75%2D85&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Arrendale RF, Severson RF, Sisson VA, Costello CE, Leary JA, Himmelsbach DS, Vanhalbeek H (1990) Characterization of the sucrose ester fraction from Nicotiana glutinosa. Journal of Agricultural and Food Chemistry 38: 75-85

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

http://scholar.google.com/scholar?as_q=Characterization of the sucrose ester fraction from Nicotiana glutinosa&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=Characterization of the sucrose ester fraction from Nicotiana glutinosa&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Arrendale&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bedewitz MA%2C Gongora%2DCastillo E%2C Uebler JB%2C Gonzales%2DVigil E%2C Wiegert%2DRininger KE%2C Childs KL%2C Hamilton JP%2C Vaillancourt B%2C Yeo YS%2C Chappell J%2C DellaPenna D%2C Jones AD%2C Buell CR%2C Barry CS %282014%29 A root%2Dexpressed L%2Dphenylalanine%3A4%2Dhydroxyphenylpyruvate aminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna%2E Plant Cell 26%3A 3745%2D3762&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bedewitz MA, Gongora-Castillo E, Uebler JB, Gonzales-Vigil E, Wiegert-Rininger KE, Childs KL, Hamilton JP, Vaillancourt B, Yeo YS, Chappell J, DellaPenna D, Jones AD, Buell CR, Barry CS (2014) A root-expressed L-phenylalanine:4-hydroxyphenylpyruvate aminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna. Plant Cell 26: 3745-3762

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

http://scholar.google.com/scholar?as_q=A root-expressed L-phenylalanine:4-hydroxyphenylpyruvate aminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna&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 root-expressed L-phenylalanine:4-hydroxyphenylpyruvate aminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bedewitz&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bird DA%2C Franceschi VR%2C Facchini PJ %282003%29 A tale of three cell types%3A Alkaloid biosynthesis is localized to sieve elements in opium poppy%2E Plant Cell 15%3A 2626%2D2635&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bird DA, Franceschi VR, Facchini PJ (2003) A tale of three cell types: Alkaloid biosynthesis is localized to sieve elements in opium poppy. Plant Cell 15: 2626-2635

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

http://scholar.google.com/scholar?as_q=A tale of three cell types: Alkaloid biosynthesis is localized to sieve elements in opium poppy&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 tale of three cell types: Alkaloid biosynthesis is localized to sieve elements in opium poppy&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bird&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bleeker PM%2C Mirabella R%2C Diergaarde PJ%2C VanDoorn A%2C Tissier A%2C Kant MR%2C Prins M%2C de Vos M%2C Haring MA%2C Schuurink RC %282012%29 Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative%2E Proceedings of the National Academy of Sciences of the United States of America 109%3A 20124%2D20129&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proceedings of the National Academy of Sciences of the United States of America 109: 20124-20129

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

http://scholar.google.com/scholar?as_q=Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative&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=Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bleeker&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bombarely A%2C Moser M%2C Amrad A%2C Bao M%2C Bapaume L%2C Barry CS%2C Bliek M%2C Boersma MR%2C Borghi L%2C Bruggmann R%2C Bucher M%2C D%27Agostino N%2C Davies K%2C Druege U%2C Dudareva N%2C Egea%2DCortines M%2C Delledonne M%2C Fernandez%2DPozo N%2C Franken P%2C Grandont L%2C Heslop%2DHarrison JS%2C Hintzsche J%2C Johns M%2C Koes R%2C Lv X%2C Lyons E%2C Malla D%2C Martinoia E%2C Mattson NS%2C Morel P%2C Mueller LA%2C Muhlemann J%2C Nouri E%2C Passeri V%2C Pezzotti M%2C Qi Q%2C Reinhardt D%2C Rich M%2C Richert%2DP�ggeler KR%2C Robbins TP%2C Schatz MC%2C Schranz ME%2C Schuurink RC%2C Schwarzacher T%2C Spelt K%2C Tang H%2C Urbanus SL%2C Vandenbussche M%2C Vijverberg K%2C Villarino GH%2C Warner RM%2C Weiss J%2C Yue Z%2C Zethof J%2C Quattrocchio F%2C Sims TL%2C Kuhlemeier C %282016%29 Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida%2E Nature Plants 2%3A 16074&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bombarely A, Moser M, Amrad A, Bao M, Bapaume L, Barry CS, Bliek M, Boersma MR, Borghi L, Bruggmann R, Bucher M, D'Agostino N, Davies K, Druege U, Dudareva N, Egea-Cortines M, Delledonne M, Fernandez-Pozo N, Franken P, Grandont L, Heslop-Harrison JS, Hintzsche J, Johns M, Koes R, Lv X, Lyons E, Malla D, Martinoia E, Mattson NS, Morel P, Mueller LA, Muhlemann J, Nouri E, Passeri V, Pezzotti M, Qi Q, Reinhardt D, Rich M, Richert-P�ggeler KR, Robbins TP, Schatz MC, Schranz ME, Schuurink RC, Schwarzacher T, Spelt K, Tang H, Urbanus SL, Vandenbussche M, Vijverberg K, Villarino GH, Warner RM, Weiss J, Yue Z, Zethof J, Quattrocchio F, Sims TL, Kuhlemeier C (2016) Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nature Plants 2: 16074

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

http://scholar.google.com/scholar?as_q=Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida.&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=Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bombarely&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Boutanaev AM%2C Moses T%2C Zi JC%2C Nelson DR%2C Mugford ST%2C Peters RJ%2C Osbourn A %282015%29 Investigation of terpene diversification across multiple sequenced plant genomes%2E Proceedings of the National Academy of Sciences of the United States of America 112%3A E81%2DE88&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Boutanaev AM, Moses T, Zi JC, Nelson DR, Mugford ST, Peters RJ, Osbourn A (2015) Investigation of terpene diversification across multiple sequenced plant genomes. Proceedings of the National Academy of Sciences of the United States of America 112: E81-E88

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

http://scholar.google.com/scholar?as_q=Investigation of terpene diversification across multiple sequenced plant genomes&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=Investigation of terpene diversification across multiple sequenced plant genomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Boutanaev&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Buta JG%2C Lusby WR%2C Neal JW%2C Waters RM%2C Pittarelli GW %281993%29 Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporariorum%2E Phytochemistry 32%3A 859%2D864&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Buta JG, Lusby WR, Neal JW, Waters RM, Pittarelli GW (1993) Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporariorum. Phytochemistry 32: 859-864

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

http://scholar.google.com/scholar?as_q=Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporariorum&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=Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporariorum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Buta&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chae L%2C Kim T%2C Nilo%2DPoyanco R%2C Rhee SY %282014%29 Genomic signatures of specialized metabolism in plants%2E Science 344%3A 510%2D513&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chae L, Kim T, Nilo-Poyanco R, Rhee SY (2014) Genomic signatures of specialized metabolism in plants. Science 344: 510-513

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

http://scholar.google.com/scholar?as_q=Genomic signatures of specialized metabolism in 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=Genomic signatures of specialized metabolism in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chae&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chortyk OT%2C Kays SJ%2C Teng Q %281997%29 Characterization of insecticidal sugar esters of Petunia%2E Journal of Agricultural and Food Chemistry 45%3A 270%2D275&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chortyk OT, Kays SJ, Teng Q (1997) Characterization of insecticidal sugar esters of Petunia. Journal of Agricultural and Food Chemistry 45: 270-275

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

http://scholar.google.com/scholar?as_q=Characterization of insecticidal sugar esters of Petunia&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=Characterization of insecticidal sugar esters of Petunia&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chortyk&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chortyk OT%2C Severson RF%2C Cutler HC%2C Sisson VA %281993%29 Antibiotic activities of sugar esters isolated from selected Nicotiana species%2E Bioscience Biotechnology and Biochemistry 57%3A 1355%2D1356&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chortyk OT, Severson RF, Cutler HC, Sisson VA (1993) Antibiotic activities of sugar esters isolated from selected Nicotiana species. Bioscience Biotechnology and Biochemistry 57: 1355-1356

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

http://scholar.google.com/scholar?as_q=Antibiotic activities of sugar esters isolated from selected Nicotiana species&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=Antibiotic activities of sugar esters isolated from selected Nicotiana species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chortyk&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=D%27Auria JC %282006%29 Acyltransferases in plants%3A a good time to be BAHD%2E Current Opinion in Plant Biology 9%3A 331%2D340&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=D'Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Current Opinion in Plant Biology 9: 331-340

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

http://scholar.google.com/scholar?as_q=Acyltransferases in plants: a good time to be BAHD&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=Acyltransferases in plants: a good time to be BAHD&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=D'Auria&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1


Dong Y, Burch-Smith TM, Liu Y, Mamillapalli P, Dinesh-Kumar SP (2007) A Ligation-Independent cloning tobacco rattle virus vectorfor high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development. Plant Physiology145: 1161-1170


Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatileorganic compounds. New Phytologist 198: 16-32


Duge de Bernonville T, Clastre M, Besseau S, Oudin A, Burlat V, Glevarec G, Lanoue A, Papon N, Giglioli-Guivarc'h N, St-Pierre B,Courdavault V (2015) Phytochemical genomics of the Madagascar periwinkle: Unravelling the last twists of the alkaloid engine.Phytochemistry 113: 9-23


Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797


Fan PX, Miller AM, Schilmiller AL, Liu XX, Ofner I, Jones AD, Zamir D, Last RL (2016) In vitro reconstruction and analysis ofevolutionary variation of the tomato acylsucrose metabolic network. Proceedings of the National Academy of Sciences of theUnited States of America 113: E239-E248


Fobes JF, Mudd JB, Marsden MPF (1985) Epicuticular lipid accumulation on the leaves of (Corr.) D'Arcy and Lycopersiconesculentum Mill. Plant Physiology 77: 567-570


Fridman E, Wang JH, Iijima Y, Froehlich JE, Gang DR, Ohlrogge J, Pichersky E (2005) Metabolic, genomic, and biochemicalanalyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis ofmethylketones. Plant Cell 17: 1252-1267


Ghosh B, Westbrook TC, Jones AD (2014) Comparative structural profiling of trichome specialized metabolites in tomato (Solanumlycopersicum) and S. habrochaites: acylsugar profiles revealed by UHPLC/MS and NMR. Metabolomics 10: 496-507


Goffreda JC, Mutschler MA, Ave DA, Tingey WM, Steffens JC (1989) Aphid deterrence by glucose esters in glandular trichomeexudate of wild tomato, Lycopersicon pennellii. Journal of Chemical Ecology 15: 2135-2147


Gonzales-Vigil E, Hufnagel DE, Kim J, Last RL, Barry CS (2012) Evolution of TPS20-related terpene synthases influences chemicaldiversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant Journal 71: 921-935


Guo YF, Wiegert-Rininger KE, Vallejo VA, Barry CS, Warner RM (2015) Transcriptome-enabled marker discovery and mapping ofplastochron-related genes in Petunia spp. Bmc Genomics 16


Halinski LP, Stepnowski P (2013) GC-MS and MALDI-TOF MS profiling of sucrose esters from Nicotiana tabacum and N. rustica.Zeitschrift Fur Naturforschung Section C-a Journal of Biosciences 68: 210-222


Hare JD (2005) Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insectherbivores. Journal of Chemical Ecology 31: 1475-1491

Pubmed: Author and TitleCrossRef: Author and Title www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from


http://www.ncbi.nlm.nih.gov/pubmed?term=Dong Y%2C Burch%2DSmith TM%2C Liu Y%2C Mamillapalli P%2C Dinesh%2DKumar SP %282007%29 A Ligation%2DIndependent cloning tobacco rattle virus vector for high%2Dthroughput virus%2Dinduced gene silencing identifies roles for NbMADS4%2D1 and %2D2 in floral development%2E Plant Physiology 145%3A 1161%2D1170&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dong Y, Burch-Smith TM, Liu Y, Mamillapalli P, Dinesh-Kumar SP (2007) A Ligation-Independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development. Plant Physiology 145: 1161-1170

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

http://scholar.google.com/scholar?as_q=A Ligation-Independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral 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=A Ligation-Independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dong&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dudareva N%2C Klempien A%2C Muhlemann JK%2C Kaplan I %282013%29 Biosynthesis%2C function and metabolic engineering of plant volatile organic compounds%2E New Phytologist 198%3A 16%2D32&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytologist 198: 16-32

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

http://scholar.google.com/scholar?as_q=Biosynthesis, function and metabolic engineering of plant volatile organic compounds&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=Biosynthesis, function and metabolic engineering of plant volatile organic compounds&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dudareva&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Duge de Bernonville T%2C Clastre M%2C Besseau S%2C Oudin A%2C Burlat V%2C Glevarec G%2C Lanoue A%2C Papon N%2C Giglioli%2DGuivarc%27h N%2C St%2DPierre B%2C Courdavault V %282015%29 Phytochemical genomics of the Madagascar periwinkle%3A Unravelling the last twists of the alkaloid engine%2E Phytochemistry 113%3A 9%2D23&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Duge de Bernonville T, Clastre M, Besseau S, Oudin A, Burlat V, Glevarec G, Lanoue A, Papon N, Giglioli-Guivarc'h N, St-Pierre B, Courdavault V (2015) Phytochemical genomics of the Madagascar periwinkle: Unravelling the last twists of the alkaloid engine. Phytochemistry 113: 9-23

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

http://scholar.google.com/scholar?as_q=Phytochemical genomics of the Madagascar periwinkle: Unravelling the last twists of the alkaloid engine&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=Phytochemical genomics of the Madagascar periwinkle: Unravelling the last twists of the alkaloid engine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Duge&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Edgar RC %282004%29 MUSCLE%3A multiple sequence alignment with high accuracy and high throughput%2E Nucleic Acids Research 32%3A 1792%2D1797&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797

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

http://scholar.google.com/scholar?as_q=MUSCLE: multiple sequence alignment with high accuracy and high throughput&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=MUSCLE: multiple sequence alignment with high accuracy and high throughput&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Edgar&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fan PX%2C Miller AM%2C Schilmiller AL%2C Liu XX%2C Ofner I%2C Jones AD%2C Zamir D%2C Last RL %282016%29 In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network%2E Proceedings of the National Academy of Sciences of the United States of America 113%3A E239%2DE248&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fan PX, Miller AM, Schilmiller AL, Liu XX, Ofner I, Jones AD, Zamir D, Last RL (2016) In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network. Proceedings of the National Academy of Sciences of the United States of America 113: E239-E248

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

http://scholar.google.com/scholar?as_q=In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network&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=In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fan&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fobes JF%2C Mudd JB%2C Marsden MPF %281985%29 Epicuticular lipid accumulation on the leaves of %28Corr%2E%29 D%27Arcy and Lycopersicon esculentum Mill%2E Plant Physiology 77%3A 567%2D570&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fobes JF, Mudd JB, Marsden MPF (1985) Epicuticular lipid accumulation on the leaves of (Corr.) D'Arcy and Lycopersicon esculentum Mill. Plant Physiology 77: 567-570

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

http://scholar.google.com/scholar?as_q=Epicuticular lipid accumulation on the leaves of (Corr&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=Epicuticular lipid accumulation on the leaves of (Corr&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fobes&as_ylo=1985&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fridman E%2C Wang JH%2C Iijima Y%2C Froehlich JE%2C Gang DR%2C Ohlrogge J%2C Pichersky E %282005%29 Metabolic%2C genomic%2C and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones%2E Plant Cell 17%3A 1252%2D1267&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fridman E, Wang JH, Iijima Y, Froehlich JE, Gang DR, Ohlrogge J, Pichersky E (2005) Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones. Plant Cell 17: 1252-1267

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

http://scholar.google.com/scholar?as_q=Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones&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=Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fridman&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ghosh B%2C Westbrook TC%2C Jones AD %282014%29 Comparative structural profiling of trichome specialized metabolites in tomato %28Solanum lycopersicum%29 and S%2E habrochaites%3A acylsugar profiles revealed by UHPLC%2FMS and NMR%2E Metabolomics 10%3A 496%2D507&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ghosh B, Westbrook TC, Jones AD (2014) Comparative structural profiling of trichome specialized metabolites in tomato (Solanum lycopersicum) and S. habrochaites: acylsugar profiles revealed by UHPLC/MS and NMR. Metabolomics 10: 496-507

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

http://scholar.google.com/scholar?as_q=Comparative structural profiling of trichome specialized metabolites in tomato (Solanum lycopersicum) and S&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=Comparative structural profiling of trichome specialized metabolites in tomato (Solanum lycopersicum) and S&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ghosh&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Goffreda JC%2C Mutschler MA%2C Ave DA%2C Tingey WM%2C Steffens JC %281989%29 Aphid deterrence by glucose esters in glandular trichome exudate of wild tomato%2C Lycopersicon pennellii%2E Journal of Chemical Ecology 15%3A 2135%2D2147&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goffreda JC, Mutschler MA, Ave DA, Tingey WM, Steffens JC (1989) Aphid deterrence by glucose esters in glandular trichome exudate of wild tomato, Lycopersicon pennellii. Journal of Chemical Ecology 15: 2135-2147

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

http://scholar.google.com/scholar?as_q=Aphid deterrence by glucose esters in glandular trichome exudate of wild tomato, Lycopersicon pennellii&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=Aphid deterrence by glucose esters in glandular trichome exudate of wild tomato, Lycopersicon pennellii&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Goffreda&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gonzales%2DVigil E%2C Hufnagel DE%2C Kim J%2C Last RL%2C Barry CS %282012%29 Evolution of TPS20%2Drelated terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites%2E Plant Journal 71%3A 921%2D935&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gonzales-Vigil E, Hufnagel DE, Kim J, Last RL, Barry CS (2012) Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant Journal 71: 921-935

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

http://scholar.google.com/scholar?as_q=Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites&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=Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gonzales-Vigil&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guo YF%2C Wiegert%2DRininger KE%2C Vallejo VA%2C Barry CS%2C Warner RM %282015%29 Transcriptome%2Denabled marker discovery and mapping of plastochron%2Drelated genes in Petunia spp%2E Bmc Genomics 16&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Guo YF, Wiegert-Rininger KE, Vallejo VA, Barry CS, Warner RM (2015) Transcriptome-enabled marker discovery and mapping of plastochron-related genes in Petunia spp. Bmc Genomics 16

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

http://scholar.google.com/scholar?as_q=Transcriptome-enabled marker discovery and mapping of plastochron-related genes in Petunia spp.&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=Transcriptome-enabled marker discovery and mapping of plastochron-related genes in Petunia spp.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guo&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Halinski LP%2C Stepnowski P %282013%29 GC%2DMS and MALDI%2DTOF MS profiling of sucrose esters from Nicotiana tabacum and N%2E rustica%2E Zeitschrift Fur Naturforschung Section C%2Da Journal of Biosciences 68%3A 210%2D222&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Halinski LP, Stepnowski P (2013) GC-MS and MALDI-TOF MS profiling of sucrose esters from Nicotiana tabacum and N. rustica. Zeitschrift Fur Naturforschung Section C-a Journal of Biosciences 68: 210-222

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

http://scholar.google.com/scholar?as_q=GC-MS and MALDI-TOF MS profiling of sucrose esters from Nicotiana tabacum and N&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=GC-MS and MALDI-TOF MS profiling of sucrose esters from Nicotiana tabacum and N&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Halinski&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hare JD %282005%29 Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores%2E Journal of Chemical Ecology 31%3A 1475%2D1491&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hare JD (2005) Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores. Journal of Chemical Ecology 31: 1475-1491


Google Scholar: Author Only Title Only Author and Title

Kandra L, Severson R, Wagner GJ (1990) Modified branched-chain amino acid pathways give rise to acyl acids of sucrose estersexuded from tobacco leaf trichomes. European Journal of Biochemistry 188: 385-391


Kang JH, Gonzales-Vigil E, Matsuba Y, Pichersky E, Barry CS (2014) Determination of residues responsible for substrate andproduct specificity of Solanum habrochaites short-chain cis-prenyltransferases. Plant Physiology 164: 80-91


Kawaguchi A, Yoshimura T, Okuda S (1981) A new method for the preparation of acyl-CoA thioesters. Journal of Biochemistry 89:337-339


Kim J, Kang K, Vigil EG, Shi F, Jones AD, Barry CS, Last RL (2012) Striking natural diversity in glandular trichome acylsugarcomposition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites. Plant Physiology 160:1854-1870


Kim J, Matsuba Y, Ning J, Schilmiller AL, Hammar D, Jones AD, Pichersky E, Last RL (2014) Analysis of natural and inducedvariation in tomato glandular trichome flavonoids identifies a gene not present in the reference genome. Plant Cell 26: 3272-3285


Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim SB, LeeHY, Kim SY, Kim MS, Kang BC, Jo YD, Yang HB, Jeong HJ, Kang WH, Kwon JK, Shin C, Lim JY, Park JH, Huh JH, Kim JS, Kim BD,Cohen O, Paran I, Suh MC, Lee SB, Kim YK, Shin Y, Noh SJ, Park J, Seo YS, Kwon SY, Kim HA, Park JM, Kim HJ, Choi SB, BoslandPW, Reeves G, Jo SH, Lee BW, Cho HT, Choi HS, Lee MS, Yu Y, Do Choi Y, Park BS, van Deynze A, Ashrafi H, Hill T, Kim WT, PaiHS, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sorensen I, Lee SJ, Kim RW, Choi IY, Choi BS, Lim JS, Lee YH, Choi D (2014)Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46:270-278


King RR, Calhoun LA, Singh RP (1988) 3,4-Di-O-acylated and 2,3,4-tri-O-acylated glucose esters from the glandular trichomes ofnontuberous Solanum species. Phytochemistry 27: 3765-3768


King RR, Pelletier Y, Singh RP, Calhoun LA (1986) 3,4-di-o-isobutyryl-6-o-caprylsucrose - the major component of a novel sucroseester complex from type B glandular trichomes of Solanum berthaultii Hawkes (PI 473340). Journal of the Chemical Society-Chemical Communications: 1078-1079


Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E, Guerin PM, Kuhlemeier C (2011) Pollinator choice in Petunia dependson two major genetic loci for floral scent production. Current Biology 21: 730-739


Lange BM, Turner GW (2013) Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant BiotechnologyJournal 11: 2-22


Liu X, Enright M, Barry CS, Jones AD (2017) Profiling, isolation and structure elucidation of specialized metabolites accumulatingin trichomes of Petunia species. Metabolomics 13: 85


Luckwill L (1943) The genus Lycopersicon: A historical, biological, and taxonomic survey of the wild and cultivated tomatoes.Aberdeen University Press, Aberdeen, Scotland

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from


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

http://scholar.google.com/scholar?as_q=Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores&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=Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hare&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kandra L%2C Severson R%2C Wagner GJ %281990%29 Modified branched%2Dchain amino acid pathways give rise to acyl acids of sucrose esters exuded from tobacco leaf trichomes%2E European Journal of Biochemistry 188%3A 385%2D391&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kandra L, Severson R, Wagner GJ (1990) Modified branched-chain amino acid pathways give rise to acyl acids of sucrose esters exuded from tobacco leaf trichomes. European Journal of Biochemistry 188: 385-391

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

http://scholar.google.com/scholar?as_q=Modified branched-chain amino acid pathways give rise to acyl acids of sucrose esters exuded from tobacco leaf trichomes&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=Modified branched-chain amino acid pathways give rise to acyl acids of sucrose esters exuded from tobacco leaf trichomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kandra&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kang JH%2C Gonzales%2DVigil E%2C Matsuba Y%2C Pichersky E%2C Barry CS %282014%29 Determination of residues responsible for substrate and product specificity of Solanum habrochaites short%2Dchain cis%2Dprenyltransferases%2E Plant Physiology 164%3A 80%2D91&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kang JH, Gonzales-Vigil E, Matsuba Y, Pichersky E, Barry CS (2014) Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases. Plant Physiology 164: 80-91

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

http://scholar.google.com/scholar?as_q=Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases&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=Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kawaguchi A%2C Yoshimura T%2C Okuda S %281981%29 A new method for the preparation of acyl%2DCoA thioesters%2E Journal of Biochemistry 89%3A 337%2D339&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kawaguchi A, Yoshimura T, Okuda S (1981) A new method for the preparation of acyl-CoA thioesters. Journal of Biochemistry 89: 337-339

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

http://scholar.google.com/scholar?as_q=A new method for the preparation of acyl-CoA thioesters&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 new method for the preparation of acyl-CoA thioesters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kawaguchi&as_ylo=1981&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim J%2C Kang K%2C Vigil EG%2C Shi F%2C Jones AD%2C Barry CS%2C Last RL %282012%29 Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites%2E Plant Physiology 160%3A 1854%2D1870&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim J, Kang K, Vigil EG, Shi F, Jones AD, Barry CS, Last RL (2012) Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites. Plant Physiology 160: 1854-1870

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

http://scholar.google.com/scholar?as_q=Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites&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=Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim J%2C Matsuba Y%2C Ning J%2C Schilmiller AL%2C Hammar D%2C Jones AD%2C Pichersky E%2C Last RL %282014%29 Analysis of natural and induced variation in tomato glandular trichome flavonoids identifies a gene not present in the reference genome%2E Plant Cell 26%3A 3272%2D3285&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim J, Matsuba Y, Ning J, Schilmiller AL, Hammar D, Jones AD, Pichersky E, Last RL (2014) Analysis of natural and induced variation in tomato glandular trichome flavonoids identifies a gene not present in the reference genome. Plant Cell 26: 3272-3285


http://scholar.google.com/scholar?as_q=Analysis of natural and induced variation in tomato glandular trichome flavonoids identifies a gene not present in the reference genome&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=Analysis of natural and induced variation in tomato glandular trichome flavonoids identifies a gene not present in the reference genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim S%2C Park M%2C Yeom SI%2C Kim YM%2C Lee JM%2C Lee HA%2C Seo E%2C Choi J%2C Cheong K%2C Kim KT%2C Jung K%2C Lee GW%2C Oh SK%2C Bae C%2C Kim SB%2C Lee HY%2C Kim SY%2C Kim MS%2C Kang BC%2C Jo YD%2C Yang HB%2C Jeong HJ%2C Kang WH%2C Kwon JK%2C Shin C%2C Lim JY%2C Park JH%2C Huh JH%2C Kim JS%2C Kim BD%2C Cohen O%2C Paran I%2C Suh MC%2C Lee SB%2C Kim YK%2C Shin Y%2C Noh SJ%2C Park J%2C Seo YS%2C Kwon SY%2C Kim HA%2C Park JM%2C Kim HJ%2C Choi SB%2C Bosland PW%2C Reeves G%2C Jo SH%2C Lee BW%2C Cho HT%2C Choi HS%2C Lee MS%2C Yu Y%2C Do Choi Y%2C Park BS%2C van Deynze A%2C Ashrafi H%2C Hill T%2C Kim WT%2C Pai HS%2C Ahn HK%2C Yeam I%2C Giovannoni JJ%2C Rose JKC%2C Sorensen I%2C Lee SJ%2C Kim RW%2C Choi IY%2C Choi BS%2C Lim JS%2C Lee YH%2C Choi D %282014%29 Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species%2E Nature Genetics 46%3A 270%2D278&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim SB, Lee HY, Kim SY, Kim MS, Kang BC, Jo YD, Yang HB, Jeong HJ, Kang WH, Kwon JK, Shin C, Lim JY, Park JH, Huh JH, Kim JS, Kim BD, Cohen O, Paran I, Suh MC, Lee SB, Kim YK, Shin Y, Noh SJ, Park J, Seo YS, Kwon SY, Kim HA, Park JM, Kim HJ, Choi SB, Bosland PW, Reeves G, Jo SH, Lee BW, Cho HT, Choi HS, Lee MS, Yu Y, Do Choi Y, Park BS, van Deynze A, Ashrafi H, Hill T, Kim WT, Pai HS, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sorensen I, Lee SJ, Kim RW, Choi IY, Choi BS, Lim JS, Lee YH, Choi D (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46: 270-278


http://scholar.google.com/scholar?as_q=Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species&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=Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=King RR%2C Calhoun LA%2C Singh RP %281988%29 3%2C4%2DDi%2DO%2Dacylated and 2%2C3%2C4%2Dtri%2DO%2Dacylated glucose esters from the glandular trichomes of nontuberous Solanum species%2E Phytochemistry 27%3A 3765%2D3768&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=King RR, Calhoun LA, Singh RP (1988) 3,4-Di-O-acylated and 2,3,4-tri-O-acylated glucose esters from the glandular trichomes of nontuberous Solanum species. Phytochemistry 27: 3765-3768

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

http://scholar.google.com/scholar?as_q=3,4-Di-O-acylated and 2,3,4-tri-O-acylated glucose esters from the glandular trichomes of nontuberous Solanum species&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=3,4-Di-O-acylated and 2,3,4-tri-O-acylated glucose esters from the glandular trichomes of nontuberous Solanum species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=King&as_ylo=1988&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=King RR%2C Pelletier Y%2C Singh RP%2C Calhoun LA %281986%29 3%2C4%2Ddi%2Do%2Disobutyryl%2D6%2Do%2Dcaprylsucrose %2D the major component of a novel sucrose ester complex from type B glandular trichomes of Solanum berthaultii Hawkes %28PI 473340%29%2E Journal of the Chemical Society%2DChemical Communications%3A 1078%2D1079&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=King RR, Pelletier Y, Singh RP, Calhoun LA (1986) 3,4-di-o-isobutyryl-6-o-caprylsucrose - the major component of a novel sucrose ester complex from type B glandular trichomes of Solanum berthaultii Hawkes (PI 473340). Journal of the Chemical Society-Chemical Communications: 1078-1079

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

http://scholar.google.com/scholar?as_q=(1986) 3,4-di-o-isobutyryl-6-o-caprylsucrose - the major component of a novel sucrose ester complex from type B glandular trichomes of Solanum berthaultii Hawkes (PI 473340)&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=(1986) 3,4-di-o-isobutyryl-6-o-caprylsucrose - the major component of a novel sucrose ester complex from type B glandular trichomes of Solanum berthaultii Hawkes (PI 473340)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=King&as_ylo=1079&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klahre U%2C Gurba A%2C Hermann K%2C Saxenhofer M%2C Bossolini E%2C Guerin PM%2C Kuhlemeier C %282011%29 Pollinator choice in Petunia depends on two major genetic loci for floral scent production%2E Current Biology 21%3A 730%2D739&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E, Guerin PM, Kuhlemeier C (2011) Pollinator choice in Petunia depends on two major genetic loci for floral scent production. Current Biology 21: 730-739

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

http://scholar.google.com/scholar?as_q=Pollinator choice in Petunia depends on two major genetic loci for floral scent production&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=Pollinator choice in Petunia depends on two major genetic loci for floral scent production&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klahre&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lange BM%2C Turner GW %282013%29 Terpenoid biosynthesis in trichomes%2Dcurrent status and future opportunities%2E Plant Biotechnology Journal 11%3A 2%2D22&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lange BM, Turner GW (2013) Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant Biotechnology Journal 11: 2-22

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

http://scholar.google.com/scholar?as_q=Terpenoid biosynthesis in trichomes-current status and future opportunities&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=Terpenoid biosynthesis in trichomes-current status and future opportunities&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lange&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu X%2C Enright M%2C Barry CS%2C Jones AD %282017%29 Profiling%2C isolation and structure elucidation of specialized metabolites accumulating in trichomes of Petunia species%2E Metabolomics 13%3A 85&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu X, Enright M, Barry CS, Jones AD (2017) Profiling, isolation and structure elucidation of specialized metabolites accumulating in trichomes of Petunia species. Metabolomics 13: 85

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

http://scholar.google.com/scholar?as_q=Profiling, isolation and structure elucidation of specialized metabolites accumulating in trichomes of Petunia species.&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=Profiling, isolation and structure elucidation of specialized metabolites accumulating in trichomes of Petunia species.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Luckwill L %281943%29 The genus Lycopersicon%3A A historical%2C biological%2C and taxonomic survey of the wild and cultivated tomatoes%2E Aberdeen University Press%2C Aberdeen%2C Scotland&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Luckwill L (1943) The genus Lycopersicon: A historical, biological, and taxonomic survey of the wild and cultivated tomatoes. Aberdeen University Press, Aberdeen, Scotland

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

http://scholar.google.com/scholar?as_q=The genus Lycopersicon: A historical, biological, and taxonomic survey of the wild and cultivated tomatoes.&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 genus Lycopersicon: A historical, biological, and taxonomic survey of the wild and cultivated tomatoes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Luckwill&as_ylo=1943&as_allsubj=all&hl=en&c2coff=1


Luu VT, Weinhold A, Ullah C, Dressel S, Schoettner M, Gase K, Gaquerel E, Xu S, Baldwin IT (2017) O-acyl sugars protect a wildtobacco from both native fungal pathogens and a specialist herbivore. Plant Physiology 174: 370-386


Mallona I, Lischewski S, Weiss J, Hause B, Egea-Cortines M (2010) Validation of reference genes for quantitative real-time PCRduring leaf and flower development in Petunia hybrida. Bmc Plant Biology 10


Matsuba Y, Nguyen TTH, Wiegert K, Falara V, Gonzales-Vigil E, Leong B, Schafer P, Kudrna D, Wing RA, Bolger AM, Usadel B,Tissier A, Fernie AR, Barry CS, Pichersky E (2013) Evolution of a complex locus for terpene biosynthesis in Solanum. Plant Cell 25:2022 - 2036


Milo R, Last RL (2012) Achieving diversity in the face of constraints: Lessons from metabolism. Science 336: 1663-1667Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mithofer A, Boland W (2012) Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology 63: 431-450Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mugford ST, Qi XQ, Bakht S, Hill L, Wegel E, Hughes RK, Papadopoulou K, Melton R, Philo M, Sainsbury F, Lomonossoff GP, RoyAD, Goss RJM, Osbourn A (2009) A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobialcompounds and disease resistance in oats. Plant Cell 21: 2473-2484


Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemicalspecialization. Plant Cell 20: 524-542


Ning J, Moghe GD, Leong B, Kim J, Ofner I, Wang ZZ, Adams C, Jones AD, Zamir D, Last RL (2015) A feedback-insensitiveisopropylmalate synthase affects acylsugar composition in cultivated and wild tomato. Plant Physiology 169: 1821-1835


Nishizaki Y, Yasunaga M, Okamoto E, Okamoto M, Hirose Y, Yamaguchi M, Ozeki Y, Sasaki N (2013) p-Hydroxybenzoyl-glucose is azwitter donor for the biosynthesis of 7-polyacylated anthocyanin in Delphinium. Plant Cell 25: 4150-4165


Pichersky E, Lewinsohn E (2011) Convergent evolution in plant specialized metabolism. Annual Review of Plant Biology 62: 549-566


Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Rambla JL, Tikunov YM, Monforte AJ, Bovy AG, Granell A (2014) The expanded tomato fruit volatile landscape. Journal ofExperimental Botany 65: 4613-4623


Sarkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades(Solanaceae): a dated 1000-tip tree. Bmc Evolutionary Biology 13: 214


Schilmiller A, Shi F, Kim J, Charbonneau AL, Holmes D, Jones AD, Last RL (2010) Mass spectrometry screening revealswidespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant Journal 62: 391-403

Pubmed: Author and Title www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Luu VT%2C Weinhold A%2C Ullah C%2C Dressel S%2C Schoettner M%2C Gase K%2C Gaquerel E%2C Xu S%2C Baldwin IT %282017%29 O%2Dacyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore%2E Plant Physiology 174%3A 370%2D386&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Luu VT, Weinhold A, Ullah C, Dressel S, Schoettner M, Gase K, Gaquerel E, Xu S, Baldwin IT (2017) O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore. Plant Physiology 174: 370-386

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

http://scholar.google.com/scholar?as_q=O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore&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=O-acyl sugars protect a wild tobacco from both native fungal pathogens and a specialist herbivore&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Luu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mallona I%2C Lischewski S%2C Weiss J%2C Hause B%2C Egea%2DCortines M %282010%29 Validation of reference genes for quantitative real%2Dtime PCR during leaf and flower development in Petunia hybrida%2E Bmc Plant Biology 10&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mallona I, Lischewski S, Weiss J, Hause B, Egea-Cortines M (2010) Validation of reference genes for quantitative real-time PCR during leaf and flower development in Petunia hybrida. Bmc Plant Biology 10

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

http://scholar.google.com/scholar?as_q=Validation of reference genes for quantitative real-time PCR during leaf and flower development in Petunia hybrida.&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=Validation of reference genes for quantitative real-time PCR during leaf and flower development in Petunia hybrida.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mallona&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Matsuba Y%2C Nguyen TTH%2C Wiegert K%2C Falara V%2C Gonzales%2DVigil E%2C Leong B%2C Schafer P%2C Kudrna D%2C Wing RA%2C Bolger AM%2C Usadel B%2C Tissier A%2C Fernie AR%2C Barry CS%2C Pichersky E %282013%29 Evolution of a complex locus for terpene biosynthesis in Solanum%2E Plant Cell 25%3A 2022 %2D 2036&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Matsuba Y, Nguyen TTH, Wiegert K, Falara V, Gonzales-Vigil E, Leong B, Schafer P, Kudrna D, Wing RA, Bolger AM, Usadel B, Tissier A, Fernie AR, Barry CS, Pichersky E (2013) Evolution of a complex locus for terpene biosynthesis in Solanum. Plant Cell 25: 2022 - 2036

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

http://scholar.google.com/scholar?as_q=Evolution of a complex locus for terpene biosynthesis in Solanum&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=Evolution of a complex locus for terpene biosynthesis in Solanum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matsuba&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Milo R%2C Last RL %282012%29 Achieving diversity in the face of constraints%3A Lessons from metabolism%2E Science 336%3A 1663%2D1667&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Milo R, Last RL (2012) Achieving diversity in the face of constraints: Lessons from metabolism. Science 336: 1663-1667

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

http://scholar.google.com/scholar?as_q=Achieving diversity in the face of constraints: Lessons from metabolism&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=Achieving diversity in the face of constraints: Lessons from metabolism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Milo&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mithofer A%2C Boland W %282012%29 Plant defense against herbivores%3A Chemical aspects%2E Annual Review of Plant Biology 63%3A 431%2D450&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mithofer A, Boland W (2012) Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology 63: 431-450

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

http://scholar.google.com/scholar?as_q=Plant defense against herbivores: Chemical aspects&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=Plant defense against herbivores: Chemical aspects&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mithofer&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mugford ST%2C Qi XQ%2C Bakht S%2C Hill L%2C Wegel E%2C Hughes RK%2C Papadopoulou K%2C Melton R%2C Philo M%2C Sainsbury F%2C Lomonossoff GP%2C Roy AD%2C Goss RJM%2C Osbourn A %282009%29 A serine carboxypeptidase%2Dlike acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats%2E Plant Cell 21%3A 2473%2D2484&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mugford ST, Qi XQ, Bakht S, Hill L, Wegel E, Hughes RK, Papadopoulou K, Melton R, Philo M, Sainsbury F, Lomonossoff GP, Roy AD, Goss RJM, Osbourn A (2009) A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats. Plant Cell 21: 2473-2484

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

http://scholar.google.com/scholar?as_q=A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats&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 serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mugford&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Murata J%2C Roepke J%2C Gordon H%2C De Luca V %282008%29 The leaf epidermome of Catharanthus roseus reveals its biochemical specialization%2E Plant Cell 20%3A 524%2D542&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20: 524-542

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

http://scholar.google.com/scholar?as_q=The leaf epidermome of Catharanthus roseus reveals its biochemical specialization&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 leaf epidermome of Catharanthus roseus reveals its biochemical specialization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Murata&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ning J%2C Moghe GD%2C Leong B%2C Kim J%2C Ofner I%2C Wang ZZ%2C Adams C%2C Jones AD%2C Zamir D%2C Last RL %282015%29 A feedback%2Dinsensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato%2E Plant Physiology 169%3A 1821%2D1835&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ning J, Moghe GD, Leong B, Kim J, Ofner I, Wang ZZ, Adams C, Jones AD, Zamir D, Last RL (2015) A feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato. Plant Physiology 169: 1821-1835

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

http://scholar.google.com/scholar?as_q=A feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato&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 feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ning&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nishizaki Y%2C Yasunaga M%2C Okamoto E%2C Okamoto M%2C Hirose Y%2C Yamaguchi M%2C Ozeki Y%2C Sasaki N %282013%29 p%2DHydroxybenzoyl%2Dglucose is a zwitter donor for the biosynthesis of 7%2Dpolyacylated anthocyanin in Delphinium%2E Plant Cell 25%3A 4150%2D4165&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nishizaki Y, Yasunaga M, Okamoto E, Okamoto M, Hirose Y, Yamaguchi M, Ozeki Y, Sasaki N (2013) p-Hydroxybenzoyl-glucose is a zwitter donor for the biosynthesis of 7-polyacylated anthocyanin in Delphinium. Plant Cell 25: 4150-4165

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

http://scholar.google.com/scholar?as_q=p-Hydroxybenzoyl-glucose is a zwitter donor for the biosynthesis of 7-polyacylated anthocyanin in Delphinium&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=p-Hydroxybenzoyl-glucose is a zwitter donor for the biosynthesis of 7-polyacylated anthocyanin in Delphinium&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nishizaki&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pichersky E%2C Lewinsohn E %282011%29 Convergent evolution in plant specialized metabolism%2E Annual Review of Plant Biology 62%3A 549%2D566&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pichersky E, Lewinsohn E (2011) Convergent evolution in plant specialized metabolism. Annual Review of Plant Biology 62: 549-566

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

http://scholar.google.com/scholar?as_q=Convergent evolution in plant specialized metabolism&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=Convergent evolution in plant specialized metabolism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pichersky&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Potato Genome Sequencing Consortium %282011%29 Genome sequence and analysis of the tuber crop potato%2E Nature 475%3A 189%2D195&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195

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

http://scholar.google.com/scholar?as_q=Genome sequence and analysis of the tuber crop potato&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=Genome sequence and analysis of the tuber crop potato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Potato&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rambla JL%2C Tikunov YM%2C Monforte AJ%2C Bovy AG%2C Granell A %282014%29 The expanded tomato fruit volatile landscape%2E Journal of Experimental Botany 65%3A 4613%2D4623&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rambla JL, Tikunov YM, Monforte AJ, Bovy AG, Granell A (2014) The expanded tomato fruit volatile landscape. Journal of Experimental Botany 65: 4613-4623

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

http://scholar.google.com/scholar?as_q=The expanded tomato fruit volatile landscape&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 expanded tomato fruit volatile landscape&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rambla&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sarkinen T%2C Bohs L%2C Olmstead RG%2C Knapp S %282013%29 A phylogenetic framework for evolutionary study of the nightshades %28Solanaceae%29%3A a dated 1000%2Dtip tree%2E Bmc Evolutionary Biology 13%3A 214&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sarkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. Bmc Evolutionary Biology 13: 214

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

http://scholar.google.com/scholar?as_q=A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree.&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 phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sarkinen&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schilmiller A%2C Shi F%2C Kim J%2C Charbonneau AL%2C Holmes D%2C Jones AD%2C Last RL %282010%29 Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines%2E Plant Journal 62%3A 391%2D403&dopt=abstract


CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Schilmiller AL, Charbonneau AL, Last RL (2012) Identification of a BAHD acetyltransferase that produces protective acyl sugars intomato trichomes. Proceedings of the National Academy of Sciences of the United States of America 109: 16377-16382


Schilmiller AL, Last RL, Pichersky E (2008) Harnessing plant trichome biochemistry for the production of useful compounds. PlantJournal 54: 702-711


Schilmiller AL, Miner DP, Larson M, McDowell E, Gang DR, Wilkerson C, Last RL (2010) Studies of a biochemical factory: Tomatotrichome deep expressed sequence tag sequencing and proteomics. Plant Physiology. 153: 1212-1223


Schilmiller AL, Moghe GD, Fan P, Ghosh B, Ning J, Jones AD, Last RL (2015) Functionally divergent alleles and duplicated lociencoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes. Plant Cell 27: 1002-1017


Severson RF, Arrendale RF, Chortyk OT, Green CR, Thome FA, Stewart JL, Johnson AW (1985) Isolation and characterization ofthe sucrose esters of the cuticular waxes of green tobacco leaf. Journal of Agricultural and Food Chemistry 33: 870-875


Shapiro JA, Steffens JC, Mutschler MA (1994) Acylsugars of the wild tomato Lycopersicon pennellii in relation to geographicdistribution of the species. Biochemical Systematics and Ecology 22: 545-561


Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J, Dixon RA,Broun P (2008) Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanumpennellii and Nicotiana benthamiana. Plant Physiology. 148: 1830-1846


Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis usingmaximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739


Tewksbury JJ, Nabhan GP (2001) Seed dispersal - Directed deterrence by capsaicin in chillies. Nature 412: 403-404Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant Journal 70: 51-68Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641


Velasquez AC, Chakravarthy S, Martin GB (2009) Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato.Journal of Visualized Experiments 28: e1292


Walters DS, Steffens JC (1990) Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucoseesters. Plant Physiology 93: 1544-1551


Weinhold A, Baldwin IT (2011) Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. www.plantphysiol.orgon June 8, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://search.crossref.org/?page=1&rows=2&q=Schilmiller A, Shi F, Kim J, Charbonneau AL, Holmes D, Jones AD, Last RL (2010) Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant Journal 62: 391-403

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

http://scholar.google.com/scholar?as_q=Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines&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=Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schilmiller&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schilmiller AL%2C Charbonneau AL%2C Last RL %282012%29 Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes%2E Proceedings of the National Academy of Sciences of the United States of America 109%3A 16377%2D16382&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schilmiller AL, Charbonneau AL, Last RL (2012) Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes. Proceedings of the National Academy of Sciences of the United States of America 109: 16377-16382


http://scholar.google.com/scholar?as_q=Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes&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=Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schilmiller&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schilmiller AL%2C Last RL%2C Pichersky E %282008%29 Harnessing plant trichome biochemistry for the production of useful compounds%2E Plant Journal 54%3A 702%2D711&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schilmiller AL, Last RL, Pichersky E (2008) Harnessing plant trichome biochemistry for the production of useful compounds. Plant Journal 54: 702-711


http://scholar.google.com/scholar?as_q=Harnessing plant trichome biochemistry for the production of useful compounds&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=Harnessing plant trichome biochemistry for the production of useful compounds&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schilmiller&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schilmiller AL%2C Miner DP%2C Larson M%2C McDowell E%2C Gang DR%2C Wilkerson C%2C Last RL %282010%29 Studies of a biochemical factory%3A Tomato trichome deep expressed sequence tag sequencing and proteomics%2E Plant Physiology%2E 153%3A 1212%2D1223&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schilmiller AL, Miner DP, Larson M, McDowell E, Gang DR, Wilkerson C, Last RL (2010) Studies of a biochemical factory: Tomato trichome deep expressed sequence tag sequencing and proteomics. Plant Physiology. 153: 1212-1223


http://scholar.google.com/scholar?as_q=Studies of a biochemical factory: Tomato trichome deep expressed sequence tag sequencing and proteomics&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=Studies of a biochemical factory: Tomato trichome deep expressed sequence tag sequencing and proteomics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schilmiller&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schilmiller AL%2C Moghe GD%2C Fan P%2C Ghosh B%2C Ning J%2C Jones AD%2C Last RL %282015%29 Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes%2E Plant Cell 27%3A 1002%2D1017&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schilmiller AL, Moghe GD, Fan P, Ghosh B, Ning J, Jones AD, Last RL (2015) Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes. Plant Cell 27: 1002-1017


http://scholar.google.com/scholar?as_q=Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes&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=Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schilmiller&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Severson RF%2C Arrendale RF%2C Chortyk OT%2C Green CR%2C Thome FA%2C Stewart JL%2C Johnson AW %281985%29 Isolation and characterization of the sucrose esters of the cuticular waxes of green tobacco leaf%2E Journal of Agricultural and Food Chemistry 33%3A 870%2D875&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Severson RF, Arrendale RF, Chortyk OT, Green CR, Thome FA, Stewart JL, Johnson AW (1985) Isolation and characterization of the sucrose esters of the cuticular waxes of green tobacco leaf. Journal of Agricultural and Food Chemistry 33: 870-875

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

http://scholar.google.com/scholar?as_q=Isolation and characterization of the sucrose esters of the cuticular waxes of green tobacco leaf&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=Isolation and characterization of the sucrose esters of the cuticular waxes of green tobacco leaf&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Severson&as_ylo=1985&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shapiro JA%2C Steffens JC%2C Mutschler MA %281994%29 Acylsugars of the wild tomato Lycopersicon pennellii in relation to geographic distribution of the species%2E Biochemical Systematics and Ecology 22%3A 545%2D561&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shapiro JA, Steffens JC, Mutschler MA (1994) Acylsugars of the wild tomato Lycopersicon pennellii in relation to geographic distribution of the species. Biochemical Systematics and Ecology 22: 545-561

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

http://scholar.google.com/scholar?as_q=Acylsugars of the wild tomato Lycopersicon pennellii in relation to geographic distribution of the species&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=Acylsugars of the wild tomato Lycopersicon pennellii in relation to geographic distribution of the species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shapiro&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Slocombe SP%2C Schauvinhold I%2C McQuinn RP%2C Besser K%2C Welsby NA%2C Harper A%2C Aziz N%2C Li Y%2C Larson TR%2C Giovannoni J%2C Dixon RA%2C Broun P %282008%29 Transcriptomic and reverse genetic analyses of branched%2Dchain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana%2E Plant Physiology%2E 148%3A 1830%2D1846&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J, Dixon RA, Broun P (2008) Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiology. 148: 1830-1846

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

http://scholar.google.com/scholar?as_q=Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana&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=Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Slocombe&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tamura K%2C Peterson D%2C Peterson N%2C Stecher G%2C Nei M%2C Kumar S %282011%29 MEGA5%3A Molecular evolutionary genetics analysis using maximum likelihood%2C evolutionary distance%2C and maximum parsimony methods%2E Molecular Biology and Evolution 28%3A 2731%2D2739&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739

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

http://scholar.google.com/scholar?as_q=&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=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tamura&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tewksbury JJ%2C Nabhan GP %282001%29 Seed dispersal %2D Directed deterrence by capsaicin in chillies%2E Nature 412%3A 403%2D404&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tewksbury JJ, Nabhan GP (2001) Seed dispersal - Directed deterrence by capsaicin in chillies. Nature 412: 403-404

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

http://scholar.google.com/scholar?as_q=Seed dispersal - Directed deterrence by capsaicin in chillies&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=Seed dispersal - Directed deterrence by capsaicin in chillies&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tewksbury&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tissier A %282012%29 Glandular trichomes%3A what comes after expressed sequence tags%3F Plant Journal 70%3A 51%2D68&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant Journal 70: 51-68

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

http://scholar.google.com/scholar?as_q=Glandular trichomes: what comes after expressed sequence tags&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=Glandular trichomes: what comes after expressed sequence tags&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tissier&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tomato Genome Consortium %282012%29 The tomato genome sequence provides insights into fleshy fruit evolution%2E Nature 485%3A 635%2D641&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641

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

http://scholar.google.com/scholar?as_q=The tomato genome sequence provides insights into fleshy fruit 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=The tomato genome sequence provides insights into fleshy fruit evolution&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tomato&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Velasquez AC%2C Chakravarthy S%2C Martin GB %282009%29 Virus%2Dinduced gene silencing %28VIGS%29 in Nicotiana benthamiana and tomato%2E Journal of Visualized Experiments 28%3A e1292&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Velasquez AC, Chakravarthy S, Martin GB (2009) Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. Journal of Visualized Experiments 28: e1292

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

http://scholar.google.com/scholar?as_q=Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato.&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=Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Velasquez&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Walters DS%2C Steffens JC %281990%29 Branched%2Dchain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters%2E Plant Physiology 93%3A 1544%2D1551&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walters DS, Steffens JC (1990) Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiology 93: 1544-1551

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

http://scholar.google.com/scholar?as_q=Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters&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=Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walters&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1


Proceedings of the National Academy of Sciences of the United States of America 108: 7855-7859Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Winzer T, Gazda V, He Z, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE, Walker C, Bowser TA, Graham IA(2012) A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336: 1704-1708



http://www.ncbi.nlm.nih.gov/pubmed?term=Weinhold A%2C Baldwin IT %282011%29 Trichome%2Dderived O%2Dacyl sugars are a first meal for caterpillars that tags them for predation%2E Proceedings of the National Academy of Sciences of the United States of America 108%3A 7855%2D7859&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Weinhold A, Baldwin IT (2011) Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proceedings of the National Academy of Sciences of the United States of America 108: 7855-7859

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

http://scholar.google.com/scholar?as_q=Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation&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=Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Weinhold&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Winzer T%2C Gazda V%2C He Z%2C Kaminski F%2C Kern M%2C Larson TR%2C Li Y%2C Meade F%2C Teodor R%2C Vaistij FE%2C Walker C%2C Bowser TA%2C Graham IA %282012%29 A Papaver somniferum 10%2Dgene cluster for synthesis of the anticancer alkaloid noscapine%2E Science 336%3A 1704%2D1708&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Winzer T, Gazda V, He Z, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE, Walker C, Bowser TA, Graham IA (2012) A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336: 1704-1708

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

http://scholar.google.com/scholar?as_q=A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine&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 Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Winzer&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


1 biochemistry and metabolism 2 - plant physiology · 54 biochemical analyses coupled with...

Documents