a tomato vacuolar invertase inhibitor mediates sucrose ......2016/09/30 · a tomato vacuolar...

1

A Tomato Vacuolar Invertase Inhibitor Mediates Sucrose Metabolism and Influences 1 Fruit Ripening 2 3

4

Guozheng Qin2, Zhu Zhu2, Weihao Wang, Jianghua Cai, Yong Chen, Li Li, Shiping 5

Tian* 6

7

Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, No.20 8

Nanxincun, Xiangshan, Haidian District, Beijing 100093, China (G.Q., Z.Z., W.W., J.C., Y.C., 9

S.T.); University of Chinese Academy of Sciences, Yuquanlu, Beijing 100049, China (W.W., 10

J.C., Y.C., S.T.); and Robert W. Holley Center for Agriculture and Health, Agricultural 11

Research Service, US Department of Agriculture, 14850 (L.L.). 12

13

1 This work was supported by the National Natural Science Foundation of China (NSFC; 14

grant number 31530057 to S.T.), the National Basic Research Program of China (973 15

Program; grant number 2011CB100604 to S.T.), and the Youth Innovation Promotion 16

Association CAS (to G.Q.). 17

2 These authors contributed equally to the article. 18

* Address correspondence to [email protected]. 19

The author responsible for distribution of materials integral to the findings presented in this 20

article in accordance with the policy described in the Instructions for Authors 21

(www.plantphysiol.org) is: Shiping Tian ([email protected]). 22

S.T. and G.Q. designed research. G.Q. and W.W. carried out quantitative RT-PCR analysis, 23

ChIP assay, EMSA, and iTRAQ analysis. Z.Z. participated in overexpression and RNAi 24

vector construction, plant transformation, phenotype observation, lycopene and ethylene 25

measurements, enzyme assay, and Y2H. J.C. performed Western blot and protein localization 26

analysis. Y.C. participated in detection of sugar content. G.Q., Z.Z., W.W., L.L., and S.T. 27

analyzed data. G.Q., S.T., Z.Z., W.W. and L.L. wrote the paper. 28

29

Short title: Regulation of fruit ripening by tomato SlVIF 30

ABSTRACT 31

Plant Physiology Preview. Published on September 30, 2016, as DOI:10.1104/pp.16.01269

Copyright 2016 by the American Society of Plant Biologists

https://plantphysiol.orgDownloaded on May 3, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://plantphysiol.org

2

Fruit ripening is a complex process that involves a series of physiological and biochemical 32

changes that ultimately influence fruit quality traits, such as color and flavor. Sugar 33

metabolism is an important factor in ripening and there is evidence that it influences various 34

aspects of ripening, although the associated mechanism is not well understood. In this study, 35

we identified and analyzed the expression of 36 genes involved in sucrose metabolism in 36

ripening tomato (Solanum lycopersicum) fruit. Chromatin immunoprecipitation and gel 37

mobility shift assays indicated that SlVIF, which encodes a vacuolar invertase inhibitor, and 38

SlVI, encoding a vacuolar invertase, are directly regulated by the global fruit ripening 39

regulator RIN (RIPENING INHIBITOR). Moreover, we showed that SlVIF physically 40

interacts with SlVI to control sucrose metabolism. Repression of SlVIF by RNA interference 41

(RNAi) delayed tomato fruit ripening, while overexpression of SlVIF accelerated ripening, 42

with concomitant changes in lycopene production and ethylene biosynthesis. An iTRAQ 43

(isobaric tags for relative and absolute quantification)-based quantitative proteomic analysis 44

further indicated that the abundance of a set of proteins involved in fruit ripening was altered 45

by suppressing SlVIF expression, including proteins associated with lycopene generation and 46

ethylene synthesis. These findings provide evidence for the role of sucrose in promoting fruit 47

ripening and establish that SlVIF contributes to fruit quality and the RIN-mediated ripening 48

regulatory mechanisms, which are of significant agricultural value. 49

50



3

INTRODUCTION 51

Fleshy fruit ripening is a complex process involving a series of physiological and 52

biochemical changes that influence fruit characteristics such as color, flavor, aroma and 53

texture (Giovannoni, 2004). Considerable progress has been made in elucidating the 54

biochemical and molecular basis of fruit ripening, including the discovery and 55

characterization of associated transcription factor networks and phytohormone signaling 56

pathways (Alba et al., 2005; Giovannoni, 2007; Klee and Giovannoni, 2011). As an example, 57

the MADS box transcription factor, RIPENING INHIBITOR (RIN) has been defined as a 58

global regulator of ripening, and has been shown to play a key role in modulating ethylene 59

biosynthesis, carbohydrate metabolism and aroma compound production (Vrebalov et al., 60

2002; Ito et al., 2008; Qin et al., 2012). Much current research into ripening focuses on the 61

identification of new candidate genes that affect fruit quality traits (Fujisawa et al., 2013; 62

Zhong et al., 2013), an important examples of which is flavor. 63

In general, fruit ripening is characterized by a substantial accumulation of 64

carbohydrates (Fraser et al., 1994) that provide energy for fruit development and contribute to 65

its flavor (Rolland et al., 2002; Zhu et al., 2013), thereby promoting consumption and seed 66

dispersal. Indeed, the content and composition of sugars largely determine fruit sweetness 67

and nutritional quality (Borsanie et al., 2009). Although the regulatory effects of sugars on 68

photosynthetic activity and plant metabolism have long been recognized (Godt and Roitsch, 69

1997; Koch, 2004; Kocal et al., 2008), the role of sugars as signaling molecules in fruit is less 70

understood. In many plant species, the major form of carbohydrate transported from the 71

leaves to the fruit is sucrose, which acts as an important form of energy storage/translocation 72

and plays a central role in the growth and development. There is also increasing evidence that 73

sucrose may play a non-nutritive role as a regulator of cellular metabolism, possibly by 74

altering gene expression (Huber and Huber, 1996; Rolland et al., 2002; Vaughn et al., 2002; 75

Ruan et al., 2010; Eveland and Jackson, 2012). Sucrose imported into fruits is degraded into 76

hexoses (glucose and fructose) for various metabolic and biosynthetic processes and 77

re-synthesized in the cytosol, vacuole and apoplast (Koch, 2004). Sucrose turnover in vivo is 78

catalyzed by sucrose synthase (SS) and invertase (Ruan et al., 2010). SS converts sucrose into 79



4

UDP-glucose and fructose in the presence of UDP, whereas invertase hydrolyzes sucrose into 80

glucose and fructose in an irreversible reaction (Klann et al., 1996; Ruan et al., 2010). 81

Invertases play a major role in plant development and in responses to biotic and abiotic 82

stresses, and have been suggested to have important regulatory functions in carbon 83

metabolism and development in fruit (Jin et al., 2009). According to their subcellular 84

locations, invertases are classified as cell wall invertase (CWI), vacuolar invertase (VI), and 85

cytoplasmic invertase (CI) or neutral invertase (NI) forms (Sturm, 1999). In tomato fruit, 86

CWI activity is tightly linked with fruit sugar levels (Fridman et al., 2004), and is thought to 87

hydrolyze extracellular sucrose when the apoplastic pathway is active (Jin et al., 2009). Since 88

the vacuole is a storage organelle for sugars, VI is believed to modulate the sucrose/hexose 89

ratio in fruits. Antisense suppression of TIV1, a VI gene, in tomato was reported to result in 90

reduced hexose accumulation during fruit ripening (Klann et al., 1996). Similar findings were 91

reported in other fruits, such as grape (Vitis vinifera) berry (Davies and Robinson, 1996) and 92

muskmelon (Cucumis melo) (Yu et al., 2008), suggesting that VI controls the sugar 93

composition in broad range of fleshy fruit. Given the critical role of VI in fruit development 94

and ripening, its activity is likely to be tightly regulated in vivo. Studies have shown that the 95

invertase is regulated by a range of signals at the transcriptional level (Long et al., 2002; 96

Proels and Roitsch, 2009), and that invertase activity is controlled post-translationally by 97

inhibitor proteins (Hothorn et al., 2004). 98

Invertase inhibitors bind to invertases to form inactive complexes. Vacuolar invertase 99

inhibitors (VIF) have been isolated from tobacco (Nicotiana tabacum), Arabidopsis thaliana, 100

and potato (S. tuberosum) (Greiner et al., 1998; Link et al., 2004; Brummell et al., 2011). 101

Moreover, ectopic expression of Nt-inhh, a tobacco VIF, in potato tubers strongly reduced VI 102

activity and blocked hexose accumulation (Greiner et al., 1999), while heterologous 103

expression of recombinant potato VIF (INH2) suppressed potato VI activity in vitro 104

(Brummell et al., 2011). However, to our knowledge nothing has been reported regarding the 105

action or significance of fruit VIFs, which, if present, may be important for regulating VI 106

activity and hence the sugar composition of fruits. 107

Previous studies suggested a link between sugars and pigment metabolism in fleshy 108

fruit: in vitro sucrose supplementation promotes color changes in citrus (Citrus unshiu) fruit 109



5

epicarp (Iglesias et al., 2001) and in tomato (Solanum lycopersicum) fruit pericarp discs 110

(Télef et al., 2006). However, evidence that the internal quality trait (sugar levels) and 111

external quality trait (color) of fruits are linked in vivo is lacking. Moreover, much remains to 112

be learnt about how sugars affect fruit quality traits and regulate ripening remains. In this 113

current study, we identified a set of genes involved in sucrose synthesis and degradation, 114

including VI and VIF, in tomato as direct targets of the ripening regulator, RIN. Our findings 115

indicate a role for sucrose in promoting pigment biosynthesis and fruit ripening in vivo, and 116

establish VIF as a novel genetic tool for regulating fruit ripening. 117

118

119



6

RESULTS 120

Expression Analysis of Genes Involved in Sucrose Metabolism during Tomato Fruit 121

Ripening 122

The sucrose metabolic pathway is well-established; however, the expression profiles of 123

genes involved in this process during fruit ripening have not been well characterized. Sucrose 124

metabolism includes the degradation and re-synthesis of sucrose in the cytosol, vacuole and 125

apoplast. Several gene families are involved in these processes, including those encoding 126

invertase, invertase inhibitor, sucrose synthase, hexokinase, fructokinase, and sucrose 127

phosphate synthase (Carrari and Fernie, 2006) (Figure 1A). We identified the orthologs of 128

these genes in tomato in the SGN (SOL Genomics Network, http://solgenomics.net/) 129

databases using the reported gene sequence of each gene family from tomato, or another 130

Solanaceous species, as a query. A total of 36 genes were identified (Supplemental Table S1), 131

of which, 20 have previously been reported (Klann et al., 1992; Elliott et al., 1993; Wang et 132

al., 1993; Kanayama et al., 1997; Menu et al., 2001; Fridman and Zamir, 2003; Lunn and 133

MacRae, 2003; German et al., 2004; Kandel-Kfir et al., 2006; Jin et al., 2009; Goren et al., 134

2011; Li et al., 2012). The 16 unreported genes were named numerically, or on the basis of 135

the results of phylogenetic analysis. The expression of these 36 genes during ripening in 136

wild-type tomato, or in fruits at an equivalent stage, based on the number of days after 137

anthesis, in the rin mutant during fruit ripening was analyzed by quantitative RT-PCR, using 138

gene specific primers (Supplemental Table S2). To understand the temporal expression of 139

these sucrose metabolism related genes in the overall context of fruit ripening, the expression 140

of ripening marker genes (RIN, NOR, LePG, EXP1, ACS2, ACO1, PSY1, PDS) (Supplemental 141

Table S3) was also determined. 142

Eleven invertase genes were identified in the tomato genome, of which five are 143

predicted to encode CWI proteins (LIN5-9), one encodes a VI (VI), and five encode CI 144

(NI1-5). The expression of these genes had different patterns from each other in the rin 145

mutant during ripening (Figure 1B). Notably, LIN8, LIN9, NI2, and NI4 showed higher 146

expression levels in rin, whereas VI expression was significantly lower in the mutant 147

throughout ripening. 148



7

The activity of invertase has been shown to be controlled post-translationally by 149

binding to inhibitor proteins (Hothorn et al., 2004), forming an inactive complex. Although 150

no inhibitor proteins were identified in the tomato genome for CI, one gene encoding an 151



8

inhibitory protein, VIF, was found for VI and two inhibitors, CIF1 and CIF2, were identified 152

for CWI. The expression of VIF was higher in the fruit of rin mutant than in wild type, while 153

the opposite expression patterns were found for CIF1 and CIF2 (Figure 1B). These results 154

indicated that RIN promotes the expression of the VI gene and suppresses the expression of 155

its inhibitor. Conversely, RIN suppresses the expression of the CWI gene and promotes the 156

expression of its inhibitor. 157

Six sucrose synthase genes (SS1-7) were identified in the tomato genome, which 158

showed different patterns of gene expression from each other in the rin mutant at equivalent 159

days after anthesis, and the expression of SS6 was notably lower in the mutant throughout 160

ripening (Figure 1B). In addition, six hexokinase genes (HK1-6) and six fructokinase genes 161

(FK1-FKL2) were identified in the tomato genome. Their expression also showed different 162

patterns from each other in the rin mutant during ripening (Figure 1B), with the exception of 163

the fructokinase gene, FK4, whose expression has been specifically linked to stamen 164

development (German et al., 2002) and was not detected in this study. Lastly, four sucrose 165

phosphate synthase genes (SPSA1-SPSC) were identified, and their expression was shown to 166

be generally lower in rin mutant compared with wild type (Figure 1B). 167

168

ChIP-qPCR Analysis Reveals that RIN Directly Binds to the Promoters of Genes 169

Involved in Sucrose Metabolism 170

RIN regulates the expression of ripening-related genes, either directly or indirectly 171

(Fujisawa et al., 2013). To examine whether genes involved in sucrose metabolism are also 172

directly regulated by RIN, a chromatin immunoprecipitation (ChIP) assay was carried out. An 173

analysis of the promoter regions of the genes analyzed in this study identified varying 174

numbers of CArG-box binding motifs (Supplemental Table S1), which are elements that are 175

commonly found in MADS-box transcription factor binding sites (Ito et al., 2008). The 176

cross-linked DNA-protein complexes were immunoprecipitated with anti-RIN polyclonal 177

antibody that was prepared using a bacterial expressed recombinant RIN protein. To amplify 178

the promoter sequences surrounding the CArG-box binding sites from the 179

immunoprecipitated DNA, specific primers were designed (Supplemental Table S4), and the 180

binding of RIN to the promoter of ACC synthase 2 (ACS2), a known RIN-target gene (Ito et 181



9

al., 2008), served as a positive control (Supplemental Figure S1). 182

ChIP screening using affinity-purified RIN antibodies, in combination with quantitative 183

PCR (ChIP-qPCR), resulted in an enrichment in the promoter regions of 16 genes compared 184

with when non-specific antibodies (pre-immune rabbit IgG) were used (Figure 2; 185

Supplemental Figure S2). Notably, RIN directly bound to the promoter of VI and VIF (Figure 186

2). Taken together with the gene expression analysis showing that VI expression was lower in 187

the rin mutant than in the wild type, while VIF expression was higher (Figure 1B), these data 188

suggest that RIN modulates sucrose degradation in the vacuole during fruit ripening. A 189

similar result was found for genes encoding CWIs, specifically LIN7 and LIN8, and the gene 190

encoding the inhibitory protein of CWI, CIF1 (Figure 2). However, while the expression of 191

LIN7 and LIN8 was up-regulated, the expression of CIF1 was down-regulated in the rin 192

mutant during fruit ripening (Figure 1B). This indicates that sucrose degradation associated 193

with CWI is inhibited by the RIN protein during fruit ripening. The ChIP-qPCR analysis also 194

showed that RIN directly bound to the promoter of NI2 and NI4 (Figure 2), which encodes CI. 195

Lastly, RIN was shown to bind directly to the promoter of several other genes involved in 196

sucrose metabolism, e.g. SS3, HK3, and SPSA1 (Supplemental Figure S2). 197

198

Gel Mobility Shift Assay Confirms that RIN Binds to the Promoters of Sucrose 199

Metabolic Genes 200

In order to confirm the binding ability of RIN to the promoter regions of genes 201

identified in the ChIP assay, an electrophoretic mobility shift assay (EMSA) was performed 202

with purified recombinant RIN protein. Specifically we examined the ability of RIN to bind 203

to double-stranded and biotin-labeled probes (Supplemental Table S5) for the genes shown in 204

Figure 2 (VI, VIF, LIN7, LIN8, CIF1, NI2, and NI4), which contained CArG-box motifs. For 205

each gene, a band shift was observed when the purified RIN protein was mixed with the 206

biotin-labeled probe (Figure 3). Formation of the DNA-protein complexes could be prevented 207

by addition of an excessive amount of the corresponding unlabeled probe, indicating specific 208

binding of RIN to the biotin-labeled probe. Based on the different extent of competition by 209

the unlabeled DNA fragment that was observed among these genes, we concluded that RIN 210

had different binding affinities for the promoters of the analyzed genes. 211



10

212

Identification of SlVIF and Assessment of its Physical Interaction with VI 213

Having demonstrated that VI and VIF were directly regulated by RIN, the putative VI 214



11

inhibitor gene, VIF, was chosen for further functional analysis. VIF genes have been cloned 215

from A. thaliana, tobacco (Nicotiana tabacum), and potato (S. tuberosum), and reported to 216

modulate sucrose metabolism (Link et al., 2004); however, little is known about the 217



12

expression of VIF genes in tomato fruit or their roles in ripening. Tomato VIF (GenBank 218

accession no. KC007445; hereafter referred to as SlVIF) was cloned based on sequence 219

similarity to the N. tabacum VIF (AY145781). SlVIF showed 81% and 71% amino acid 220



13

identity with NtVIF (Y12806) and StVIF (FJ810206), respectively (Supplemental Figure S3). 221

All deduced proteins contained the four conserved cysteine residues that are a hallmark of all 222

known plant invertase inhibitors (Rausch and Greiner, 2004). We observed that SlVIF was 223

expressed in both vegetative and reproductive organs, but at different levels (Figure 4A). 224

Notably, SlVIF mRNA levels were high in fruit, and SlVIF protein levels peaked at 38 days 225

post-anthesis (dpa) before dropping (Figure 4B), consistent with SlVIF transcript abundance. 226

To confirm that SlVIF indeed localizes in the vacuole, we transformed tomato with a 227

construct encoding SlVIF fused to a green fluorescent protein marker, (GFP):SlVIF, as well 228

as with a GFP only construct. When we imaged transgenic tomato root cells, we observed 229

that the GFP:SlVIF fusion protein produced a strong signal in the vacuole (Figure 4C), while, 230

the GFP only control displayed fluorescence throughout the cell (Figure 4C). 231

Recombinant SlVIF protein was purified and tested for its inhibitory activity against VI 232

extracted from 44 dpa tomato fruit, to confirm whether SlVIF indeed acts as a SlVI inhibitor. 233

As shown in Figure 5A, a decrease in the VI activity was observed upon increasing the SlVIF 234

concentration, while SlVIF had no inhibitory effects on CWI activity. To investigate whether 235

SlVIF physically interacted with SlVI, a yeast-2-hybrid (Y2H) assay was performed. The 236

cDNA fragments of SlVIF and SlVI were cloned into pGBKT7 (BD) and pGADT7 (AD) 237

vectors, respectively. The resulted plasmids, BD-SlVIF and AD-SlVI, were co-transformed 238

into yeast strains. Yeasts co-transformed with BD and AD (BD/AD), BD-SlVIF and AD 239

(BD-SlVIF/AD), and AD-SlVI and BD (AD-SlVI/BD) were used as controls. As shown in 240

Figure 5B, yeast co-transformed with BD-SlVIF and AD-SlVI displayed normal growth and 241

blue color on the selective SD/-Leu/-Trp/-His/-Ade (SD-LTHA) medium containing X-α-Gal, 242

whereas the controls showed no growth. Taken together, these results indicate that SlVIF 243

interacts with SlVI to suppress SlVI activity. 244

245

SlVIF Influences Sucrose Metabolism and Fruit Ripening 246

To examine the effects of SlVIF on sugar metabolism and fruit ripening, a 35S:SlVIF 247

overexpression construct and a SlVIF RNAi construct were separately introduced into tomato. 248

Three independent transgenic lines corresponding to each construct and containing 249

single-copy transgenes were identified by quantitative real-time PCR analyses (Mason et al., 250



14

2002). The OE2 (SlVIF overexpression line 2) and S4 (SlVIF silenced line 4) lines with the 251

highest and lowest transcript level of SlVIF, respectively, were selected for further study. 252

Enzyme activity assays revealed that the VI activity was suppressed in fruit of the OE2 253

line, but elevated in fruit of the S4 line compared, with wild-type fruit at different ripening 254

stages (Figure 6A). CWI and NI activities were not affected by presence of the transgenes 255

(Figure 6B and 6C), confirming that SlVIF specifically inhibited VI activity. To investigate 256



15

whether alteration of the SlVIF activity affected fruit sugar metabolism, levels of sucrose, 257

glucose, and fructose were measured. Overexpression of SlVIF resulted in 10-fold increase in 258

sucrose levels and a 40% decrease in hexose levels in 38 dpa OE2 fruits. In contrast, 259

silencing SlVIF led to lower sucrose levels and higher hexose levels than in the wild-type 260

control fruit (Figure 6D to 6F). These results demonstrated that SlVIF influenced sugar 261

metabolism and that altering its expression caused a substantial change in sucrose levels in 262



16

fruits. 263

We noted that alteration of sucrose levels in the transgenic lines was accompanied by 264

changes in the onset of fruit ripening (Figure 6G). Fruit color changed from 35 dpa to 44 dpa 265

in wild-type fruit, but the color transition from green to red was faster in the OE2 line and 266

slower in the S4 line (Figure 6G). Moreover, we determined that while the red colored 267

carotenoid pigment, lycopene, was detectable from 38 dpa in the wild-type fruit, it started to 268

accumulate in the OE2 line at 35 dpa, and continued to increase over time, whereas no 269

significant changes in lycopene levels were observed from 35 dpa to 38 dpa in fruit of the S4 270

line (Figure 6H). We concluded that altering sugar content affected carotenoid pigment 271

biosynthesis, which in turn affected the timing of the onset of ripening. We also observed that 272

overexpression of SlVIF led to a 60% increase of ethylene production at 35 dpa compared 273

with the control, and repression of SlVIF expression resulted in significant reduction in 274

ethylene production throughout the ripening process (Figure 6I), suggesting that the altered 275

sugar levels also affected phytohormone production to coordinately regulate fruit ripening. 276

To better understand the mechanism of action of SlVIF in ripening fruit, the transcript 277

levels of a set of ripening related marker genes (RIN, NOR, LePG, EXP1, ACS2, ACO1, PSY1 278

and PDS) were evaluated in SlVIF overexpressing and silenced tomato fruits by quantitative 279

RT-PCR (Figure 7). The results indicated that the expression levels of these ripening marker 280

genes were significantly influenced by SlVIF. Notably, the ripening regulators RIN and NOR 281

were repressed in the SlVIF RNAi fruits at 38 dpa and 41 dpa, but exhibited higher transcript 282

levels at 44 dpa compared with the wild type. This suggests that gene expression of RIN and 283

NOR was delayed in the SlVIF RNAi tomatoes during fruit ripening. 284

285

SlVIF Modulates the Expression of Ripening-Related Proteins 286

To further elucidate how SlVIF coordinately regulated fruit ripening, we performed an 287

isobaric tags for relative and absolute quantification (iTRAQ)-based quantitative proteomic 288

analysis of wild-type and SlVIF RNAi fruit. Proteins were extracted from the frozen pericarp 289

tissue of wild-type and SlVIF RNAi fruits at 38 dpa and 41 dpa and labeled with 4-plex 290

iTRAQ reagents (Figure 8A). We analyzed three independent biological replicates, with a 291

replicate corresponding to tissue pooled from fruits from five different plants for each stage 292



17

and each genotype. Using a S. lycopersicum protein database 293

(ftp://ftp.solgenomics.net/genomes/Solanum_lycopersicum/annotation/ITAG2.4_release/), a 294

total of 4,240, 4,225, and 4,381 proteins were identified in both wild type and transgenic line 295



18

in biological replicate 1, 2, and 3, respectively, with a global false discovery rate (FDR) < 1% 296

in each. A two-fold cut-off led to the identification of 185 and 203 proteins with significantly 297

altered levels in the SlVIF silenced fruits at 38 dpa and 41 dpa, respectively (Supplemental 298

Table S6). 299

The differentially expressed proteins identified at 38 dpa and 41 dpa were categorized 300

using Blast2go (https://www.blast2go.com/) into fourteen functional categories (Figure 8B). 301

Overall 139 of them were more abundant and 212 were less abundant, respectively, in the 302

transgenic fruit than in wide type (Figure 8C). We concluded that a set of ripening related 303

proteins were significantly affected by SlVIF expression (Figure 9). These included proteins 304



19

involved in carotenoid biosynthesis, such as phytoene desaturase (PDS), in ethylene synthesis, 305

such as ACC oxidase 1 (ACO1) and peptide methionine sulfoxide reductase msrA (E4), and 306

in cell wall degradation, such as polygalacturonase A (LePG) and pectinesterase (PME). To 307



20

determine whether the protein expression patterns correlated with transcript levels, 308

quantitative RT-PCR was carried out for the corresponding genes using gene specific primers 309

(Supplemental Table S7). Of the 15 genes analyzed, the expression of 12, including PDS, 310

CRTISO, ACO1, E4, and LePG, were consistent with the protein abundance variations 311

(Figure 9). These results further indicated that SlVIF affected the expression of 312

ripening-related genes. 313

314

315



21

DISCUSSION 316

RIN Regulates Expression of Genes Involved in Sucrose Metabolism 317

Given the importance of the ripening process in determining the quality, taste and 318

aroma of fruit, considerable effort had been focused on understanding its control (Klee and 319

Giovannoni, 2011; Ecker, 2013). The MADS-box transcription factor, RIN, has been shown 320

to be a global regulator of fruit ripening (Vrebalov et al., 2002; Martel et al., 2011) and to be 321

critical for the production of characteristic tomato aromas derived from the LOX pathway 322

(Qin et al., 2012). However, the particular genes related to sugar metabolism and their 323

specific modulation by RIN have not been well defined. The VI, VIF, SS, HK, FK and SPS 324

gene families have been shown to be involved in sucrose metabolism by regulating the 325

degradation and re-synthesis of sucrose (Carrari and Fernie, 2006). Here, we identified a total 326

of 36 genes involved in sucrose metabolism in tomato (Supplemental Table S1) and analyzed 327

their expression in the wild type and the rin mutant by quantitative RT-PCR using gene 328

specific primers (Figure 1). Many of these genes were differentially expressed in the rin 329

mutant compared with the wild type at equivalent days after anthesis, including 11 invertase 330

genes (LIN5-9, VI, NI1-5), a VI inhibitor gene (VIF), 6 sucrose synthase genes (SS1-7), 4 331

sucrose phosphate synthase genes (SPSA1-SPSC) and 6 hexokinase genes (HK1-6). The data 332

suggest that RIN regulates sucrose metabolism during ripening by modulating the expression 333

of a specific set of genes that play crucial roles in sucrose degradation and re-synthesis. 334

Sugars have important hormone-like functions as primary messengers in signal 335

transduction, in addition to their essential roles as substrates in the carbon and energy 336

metabolism, and in polymer biosynthesis (Rolland et al., 2002). Following sucrose 337

degradation by SS and VI, the resulting hexoses undergo phosphorylation by FK and HK for 338

further metabolism (Claeyssen and Rivoal, 2007), suggesting that FK and HK are important 339

in hexose metabolism, hexose sensing and signaling (Eveland and Jackson, 2012). In this 340

study, we showed that RIN governs sugar metabolism via the regulation of a number of genes, 341

including SlVI and SlVIF, in the sucrose synthesis and degradation pathway (Figure 1B). SlVI 342

expression was lower in the rin mutant while that of SlVIF was higher, suggesting that RIN 343

can modulate sucrose degradation during fruit ripening via promoting SlVI expression and 344

suppressing its inhibitor SlVIF. Interestingly, the expression of RIN changed substantially in 345



22

the SlVIF RNAi tomatoes during fruit ripening (Figure 7), suggesting that SlVIF affects RIN 346

expression via a positive feed-back loop. 347

348

SlVIF Functions on Sucrose Metabolism and Lycopene Synthesis 349

The deduced SlVIF sequence was shown to share a high homology with vacuolar 350

invertase inhibitors from tobacco and potato (Supplemental Figure S3). Four conserved 351

cysteine (Cys) residues were identified that, in a potato vacuolar invertase inhibitor, have 352

been shown to form disulfide bridges to stabilize the protein (Brummell et al., 2011). Gene 353

expression analysis showed that SlVIF was expressed in both vegetative and reproductive 354

organs (Figure 4A), and that its expression increased in fruit from 35 dpa to 44 dpa (Figure 355

4B), indicating that it is involved in fruit ripening. Greiner et al., (1999) suggested that the 356

homologous protein from tobacco, NtVIF, is vacuolar, because overexpression of NtVIF in 357

potato strongly inhibited VI but not CWI. This is consistent with our observation that 358

recombinant GFP-SlVIF fusion protein accumulated in the vacuole of tomato root cells 359

(Figure 4C). Overexpression of SlVIF in tomato reduced the activity of VI, whereas silencing 360

its expression resulted in increased VI activity (Figure 6A), indicating that invertase activity 361

is regulated by its endogenous inhibitor. Importantly, altered SlVIF expression did not affect 362

the activities of CWI or NI (Figure 6B and 6C), demonstrating the specificity of SlVIF for 363

SlVI. These results were further confirmed by Y2H analysis (Figure 5B). Previous reports 364

indicated a role for invertases and invertase inhibitors in mediating sugar levels in plants 365

(Greiner et al., 1999). Induction of the VIF expression in potato tubers contributes to 366

cold-induced sweetening resistance due to its inhibition of VI and resulting decrease in the 367

accumulation of reducing sugars (Brummell et al., 2011). Consistent with its predicted role, 368

overexpression of SlVIF in tomato fruits significantly inhibited sucrose hydrolysis, leading to 369

an increase in sucrose content and a reduction in hexose levels, while suppression of SlVIF 370

promoted sucrose hydrolysis and enhanced hexose levels (Figure 6D to 6F). 371

Post-translational regulation of enzymes involved in the sugar metabolic pathway 372

represents an important mechanism for regulating sugar levels and composition in plants 373

(Koch, 2004). Moreover, post-translational elevation of CWI activity by silencing of its 374

inhibitor has been shown to result in increased hexose accumulation in tomato fruits (Jin et al., 375



23

2009), and a number of studies have shown that VI activity is correlated with hexose levels in 376

hexose-accumulating species of tomato (Miron and Schaffer 1991; Klann et al., 1996). 377

External sucrose supplementation was previously reported to promote a color break in citrus 378

(Citrus unshiu) and tomato fruit (Iglesias et al., 2001; Télef N, et al., 2006), indicating a link 379

between sugars and pigments. Color transition in tomato fruits is due to the degradation of 380

chlorophylls and the simultaneous accumulation of carotenoids, mainly lycopene, which is 381

affected by several factors (Giovannoni, 2004). However, evidence supporting a role for 382

sugars in pigment synthesis, and consequently fruit ripening, in vivo is still lacking. In this 383

study, overexpression of SlVIF in tomato decreased hexose content during ripening, in 384

contrast to fruits from wild-type and SlVIF RNAi plants (Figure 6E and 6F), suggesting a 385

connection between VI activity and hexose accumulation. Interestingly, altering sucrose 386

levels by modification of SlVIF expression resulted in a clear change in the timing of the 387

onset of fruit ripening. Specifically, the red transition was faster in fruit of the SlVIF 388

overexpressing line, but slower in the SlVIF RNAi line compared with the wild-type fruit 389

(Figure 6G), indicating that SlVIF plays a role in the regulation of sucrose metabolism and 390

pigment biosynthesis. 391

392

SlVIF Modulates Ethylene Production and the Expression of Ripening-Related Genes 393

Ethylene is thought to be required for the sucrose-induced modulation of carotenoid 394

accumulation in both climacteric and non-climacteric fruit (Iglesias et al., 2001; Télef et al., 395

2006), and ethylene production is concomitant with color change and lycopene biosynthesis, 396

which is an indicator of ripening in many climacteric fruit (Giovannoni, 2007). Suppression 397

of acid invertase expression can stimulate ethylene production in tomato and muskmelon fruit 398

(Klann et al., 1996; Yu et al., 2008), and we saw that overexpression of SlVIF in tomato 399

increased ethylene production (Figure 6I) and led to a precocious color shift, due to elevated 400

lycopene accumulation (Figure 6H). In contrast, ethylene production was decreased and fruit 401

coloring was delayed by silencing SlVIF in tomato (Figure 6G). This suggests that SlVIF is 402

involved in the regulation of ethylene production and fruit ripening. Using iTRAQ-based 403

quantitative proteomic analysis, we identified 185 and 203 proteins whose abundance was 404

significantly different in SlVIF silenced fruit compared with wild-type fruit at 38 dpa and 41 405



24

dpa, respectively (Figure 8). Of these, 139 were more abundant in the transgenic fruit and 212 406

were less abundant (Figure 8C). Suppression of SlVIF expression affected the abundance of 407

many ripening-related proteins (Figure 9), including PDS, ACO1, E4, and LePG. Quantitative 408

RT-PCR analysis indicated that the expression levels of several ripening-related genes (PDS, 409

ACO1, E4, and LePG) were consistent with the corresponding protein abundance variations 410

(Figure 9). Altering sugar content and/or SlVIF expression also affected the abundance of 411

other ripening-related genes, suggesting a potential role for SlVIF in the regulation of fruit 412

ripening. Finally, ChIP-qPCR and EMSA assays showed that RIN directly bound to the 413

promoters of SlVI and SlVIF, along with those of 14 other genes involved in sucrose 414

metabolism (Figure 2 and 3; Supplemental Figure S2). These results indicate that RIN 415

controls sugar metabolism by modulating the expression of genes involved in sucrose 416

synthesis and degradation. 417

In conclusion, our study highlights an important role for SlVIF in fruit ripening and 418

establishes a link between sucrose metabolism, lycopene synthesis and ripening in tomato 419

fruit. Our results further suggest that SlVIF has potential value as a genetic tool to regulate 420

tomato fruit ripening through manipulating the interaction of VI and its inhibitor. 421

422

MATERIALS AND METHODS 423

Plant Materials and Growth Conditions 424

Tomato (Solanum lycopersicum cv. Ailsa Craig) plants were grown at 25°C with a 16-h 425

photoperiod. The flowers were tagged at anthesis to determine ripening-stages. For plants 426

grown in vitro, seeds were germinated on MS medium (Murashige and Skoog, 1962) with 16 427

h of light at 25°C and 8 h of darkness at 22°C. Seeds of the tomato mutant rin in the ‘Ailsa 428

Craig’ background were kindly provided by Dr. James J. Giovannoni (Boyce Thompson 429

Institute for Plant Research, Cornell University, Ithaca, NY). Fruit ripening stages used in 430

this study were 35, 38, 41 and 44 days post-anthesis (dpa). Fruits of rin or transgenic lines 431

were collected at the equivalent ripening stages determined by the number of dpa. 432

433

Identification of Tomato Genes Involved in Sucrose Metabolism 434

In order to identify tomato orthologs of genes involved in sucrose metabolism (i.e. 435



25

genes encoding invertases, invertase inhibitors, sucrose synthases, sucrose phosphate 436

synthases, fructokinases and hexokinases), BLAST searches were carried out against the 437

NCBI (National Center for Biotechnology Information, http://www.ncbi.nlm.nih.gov/) and 438

SGN (SOL Genomics Network, http://solgenomics.net/) databases using the reported gene 439

sequence as a query. The uniqueness of the identified genes was manually verified to remove 440

redundant sequences. GENSCAN (http://genscanw.biosino.org/) was used to predict the 441

putative open reading frames (ORFs) and proteins sequences. 442

443

Quantitative Real-Time PCR 444

Total RNA (2 μg) was extracted from pericarp tissues as described by Moore et al. 445

(2005). The extracted RNA was treated with DNase (Promega) and reverse-transcribed using 446

an oligo (dT)18 primer with Moloney murine leukemia virus (M-MLV) reverse transcriptase 447

(Promega) to synthesize cDNA. Quantitative real-time PCR (qRT-PCR) was performed with 448

Takara SYBR Green Master Mix and gene specific primers in a volume of 20 μL using an 449

Mx3000P system (Stratagene). The following condition was applied for PCR amplification: 450

95°C for 10 min, followed by 40 cycles of 95°C for 15 s and 60°C for 30 s. ACTIN 451

(BT012695) was used as an internal control, and the relative expression was calculated using 452

the comparative 2(−ΔCt) method (Schmittgen and Livak, 2008). Each experiment had three 453

biological repeats, each with three technical replicates. 454

455

Chromatin Immunoprecipitation (ChIP) Assay 456

ChIP assays were performed as previously described (Qin et al., 2012). Pericarp tissue 457

from 41 dpa fruit was collected and submerged in 1% formaldehyde under a vacuum to 458

cross-link genomic DNA and protein. Nuclei were enriched and then sonicated in nuclei 459

lysing buffer containing 50 mM Tris–HCl, pH 8.0, 10 mM EDTA, 1% SDS, 0.1 mM PMSF, 460

and proteinase inhibitors. The conditions for sonication were optimized to shear DNA to an 461

average size of 500~1,000 bp. A small aliquot of sonicated chromatin was reversely 462

cross-linked and served as the input DNA control. The remaining chromatin sample was 463

centrifuged at 16,000g for 5 min at 4°C, and the supernatant was diluted 10-fold in ChIP 464

dilution buffer (1.1% Triton X-100, 1.2 mM EDTA, 16.7 mM Tris–HCl, pH 8.0, 167 mM 465



26

NaCl, 0.1 mM PMSF, and proteinase inhibitors). Protein A-agarose/salmon sperm DNA 466

beads (Millipore) were used to preclear the chromatin solution for 1 h at 4°C. 467

Immunoprecipitation was carried out with affinity purified RIN polyclonal antibody (see 468

below), and the tube containing the samples were incubated on a rotator with gentle agitation 469

(25 rpm) for 12 h at 4°C. Reactions with preimmune serum IgG and without antibody were 470

used as negative and mock controls, respectively. Protein-chromatin immunocomplexes were 471

captured on Protein A-agarose beads by incubating at 4°C for 1 h. The beads were collected 472

by centrifugation at 16,000g for 2 min at 4°C, and the bead-bound immunocomplexes were 473

eluted with elution buffer (1% SDS, 0.1 M NaHCO3) by gently rotating for 15 min at 65°C. 474

The beads were collected and the supernatant (eluate) was transferred to a fresh tube. The 475

cross-linking of immunoprecipitated DNA was then reversed by incubation of the eluate in 476

0.2 M NaCl at 65°C overnight. The immunoprecipitated DNA was purified after Proteinase K 477

(Invitrogen, Carlsbad, CA, U.S.A.) treatment, and eluted in TE buffer (10 mM Tris-HCl, pH 478

8.0, 1 mM EDTA) before being used for PCR using the same conditions as for quantitative 479

RT-PCR analysis. The RIN binding sites (CArG-box) in the promoters of selected genes were 480

analyzed using PLACE Web Signal Scan (http://www.dna.affrc.go.jp/PLACE/signalup.html). 481

Primers used for PCR amplification are listed in Supplemental Table S4. 482

483

Electrophoretic Mobility Shift Assay (EMSA) 484

Recombinant His-tagged RIN protein was expressed in E. coli and purified as 485

previously described (Qin et al., 2012). The binding activity of RIN to specific DNA 486

sequences was assayed using a Lightshift Chemiluminescent EMSA kit (Thermo Scientific). 487

Briefly, purified RIN protein (1 μg) in a binding buffer containing 10 mM Tris-HCl (pH 7.2), 488

50 mM KCl, 1 mM DTT, 2.5% glycerol, 0.05% NP-40, and 50 ng μL-1 polydeoxy 489

(inosinate-cytidylate), was incubated for 20 min at room temperature in the presence or 490

absence of unlabeled (double-stranded) competitor probes. The 3' biotin end-labeled 491

double-stranded DNA probes, which were constructed by annealing complementary 492

oligonucleotides, were then added, and the incubation continued for 20 min. The sequences 493

of the biotin-labeled probes are listed in Supplemental Table S5. Protein-DNA complexes 494

were separated on 6% native polyacrylamide gels, and the biotin-labeled probes were 495



27

detected according to the instructions provided with the EMSA kit. 496

497

Recombinant Protein Expression and Antibody Preparation 498

Recombinant RIN protein was prepared as previously described (Qin et al., 2012). For 499

recombinant SlVIF protein preparation, a SlVIF gene fragment without the predicted putative 500

vacuolar sorting sequence (SignalP 4.0) was amplified from tomato cDNA using primers 501

SlVIF-F (5’-GGTACCAACAACAACAACAACATCAT-3’) and SlVIF-R (5’-GAGCT 502

CTCATAATAACATTCTAATTA-3’). The fragments were digested using KpnI and SacI 503

and inserted into the pET30a vector (Merck KGaA, Darmstadt, Germany). The resulting 504

plasmid was transformed into Escherichia coli BL21 (Lys) cells, and expression of the 505

recombinant protein was induced by 1 mM of isopropyl-β-D-thiogalacto- pyranoside (IPTG). 506

Recombinant His-tagged proteins were purified using Ni-NTA His-Bind resin (Merck). 507

Antibodies were raised against the recombinant RIN and SlVIF proteins in New 508

Zealand White rabbits by AbMax Biotechnology Co.Ltd (Beijing, China). Polyclonal 509

antibodies were affinity-purified from antisera using AminoLink Plus coupling resin, 510

according to the manufacturer’s instructions (Thermo Scientific, 511

http://www.thermoscientific.com/). 512

513

Western Blot Analysis 514

Proteins were extracted from tomato fruit harvested at different ripening stages as in 515

Bate et al. (2004), fractionated on a 12% SDS-PAGE gel and electrotransferred to an 516

Immobilon-P PVDF membrane (Millipore). The membranes were blocked at 20°C for 2 h 517

with 5% BSA in PBS-Tween buffer (137 mM NaCl, 2.7 mM KCl, 8.1 mM NaH2PO4, 1.5 mM 518

KH2PO4 and 0.1% Tween-20, pH 7.4). Immunoblots were performed at 4°C overnight with 519

affinity-purified rabbit polyclonal anti-SlVIF as described by Wang et al. (2014). The 520

membranes were washed with PBS-Tween (3 × 10 min) and treated with the corresponding 521

secondary antibodies (Abmart) (1:5,000 dilutions) conjugated to horseradish peroxidase. 522

Immunoreactive bands were visualized using a chemiluminescence detection kit 523

(SuperSignal®, Pierce Biotechnology). As a protein control, an anti-GAPDH 524

(glyceraldehyde-3-phosphate dehydrogenase) (Abmart) immunoblot was used. Additionally, 525



28

Coomassie brilliant blue staining was used as a loading control. 526

527

Plasmid Construction and Plant Transformation 528

To construct the 35S:GFP:SlVIF vector, the full-length SlVIF cDNA was inserted into a 529

GFP expression vector pCAMBIA2300. The SlVIF overexpression construct was made by 530

cloning the full-length SlVIF cDNA into the pBI121 vector (kindly provided by Dr. Jing Bo 531

Jin from Institute of Botany, the Chinese Academy of Sciences, Beijing, China) downstream 532

of the 35S promoter. 533

To construct the SlVIF RNAi plasmid, a 285 bp SlVIF fragment was amplified from 534

tomato cDNA (prepared from fruit pericarp at 35 dpa as described above) by the primer pair: 535

5’-TATAACACCGTCCTACGAGCCG-3’ and 5’-TCTTTATATCTGGTTC 536

ACGTAACG-3’. The resulting product was cloned into the PCR8/GW/TOPO Gateway entry 537

vector (Invitrogen). The cloned fragment was subsequently transferred into the destination 538

vector pK7GWIWG2 (Karimi et al., 2002) using the LR Clonase II enzyme (Invitrogen) 539

according to the manufacturer’s instructions. 540

The above constructs were individually transformed into Agrobacterium tumefaciens 541

strain GV3101 by electroporation. Tomato transformation was performed according to Fillatti 542

et al. (1987). The presence of transgenes in kanamycin resistant plants was confirmed by 543

PCR using a forward primer corresponding to the 35S promoter and a reverse primer specific 544

for SlVIF: 5’-CGGAAACCTCCTCGGATTCCATT-3’ and 5’-GGCTACCG 545

TTACATCGGCTCGTA-3’. 546

547

Invertase Activity and Inhibition Assays 548

The activities of VI, CWI and NI were assayed according to Miron and Schaffer (1991) 549

and Klann et al. (1993). Approximately 2 g of pericarp was homogenized in 10 mL of 550

extraction buffer containing 50 mM HEPES-NaOH (pH 7.5), 5 mM MgC12, 1 mM EDTA, 551

2.5 mM DTT, 10 mM ascorbic acid and 5 % polyvinyl-polypyrrolidone (PVPP). After 552

centrifugation at 20,000g for 30 min at 4°C, the supernatants were dialyzed for 16 h against 553

25 mM HEPES-NaOH (pH 7.5) and 0.5 mM EDTA and used as a crude enzyme extract for 554

VI and NI activity assays. The insoluble pellet was washed three times with extraction buffer 555



29

and extracted for 1 hour with 10 mL of extraction buffer containing 1 M NaCl. After 556

centrifugation at 20,000g for 30 min at 4°C, the supernatants were dialyzed overnight and 557

used as crude enzyme extract for CWI assays. For VI and CWI activity assays, 0.2 mL of 558

enzyme extract was incubated for 30 min at 37°C with 0.6 mL of 100 mM sodium acetate 559

(pH 4.8) and 0.2 mL of 100 mM sucrose. Reactions were stopped by placing the reaction 560

tubes in boiling water for 5 min and reducing sugars were measured using dinitrosalicylic 561

acid (Sumner, 1921). NI activity was assayed in 50 mM HEPES-NaOH (pH 7.5) instead of 562

sodium acetate (pH 4.8). 563

For inhibition studies, VI or CWI enzyme preparations were mixed with recombinant 564

SlVIF protein, and incubated in the assay buffer for 30 min at 37°C prior to addition of 565

sucrose and measurement of enzyme activity. 566

567

Y-2-H Assay 568

To generate the vector system for the Y-2-H analysis, the SlVIF cDNA fragment 569

encoding the mature protein and the full-length cDNA of SlVI (Genbank accession no. 570

M81081) were cloned into the pGBKT7 (BD) and pGADT7 (AD) vectors (Clontech), using 571

specific primers (SlVIF: 5’-CGGAATTCAACAACAACAACAACATCAT-3’ and 572

5’-AACTGCAGTCATAATAACATTCTAATTATG-3’; SlVI: 573

5’-CGGAATTCATGGCCACTCAGTGTTATGA-3’ and 574

5’-CCGCTCGAGTTACAAGTCTTGCAAAGGGA-3’), resulting in the BD-SlVIF and 575

AD-SlVI plasmids. The two plasmids were co-transformed into the yeast strain 576

Saccharomyces cerevisiae AH109 according to the manufacturer’s instructions (Clontech), 577

and dripped on synthetic dropout nutrient medium SD-LT (SD/-Leu/-Trp) and SD-LTHA 578

(SD/-Leu/-Trp/-His/-Ade) containing X-α-Gal. As a control, BD and AD, BD-SlVIF and AD, 579

BD and AD-SlVI were also co-transformed and analyzed, respectively. 580

581

Sugar, Lycopene and Ethylene Measurements 582

Sugars were extracted and determined according to Zhu et al. (2013). 583

Pericarp lycopene content was measured as described by Choi and Huber (2008). 584

Tomato pericarp tissue samples (5 g) were homogenized for 1 min in 50 mL of hexane–585



30

acetone–ethanol (2:1:1, v/v) wrapped in aluminum foil to exclude light, then 15 mL of water 586

was added and the samples were vortexed for 10 s. After allowing phase separation on ice, 587

the lycopene concentration was determined by measuring the absorbance of the organic phase 588

(hexane) at 503 nm. The lycopene content was calculated using the molar extinction 589

coefficient of 17.2 L mol−1 m−1 and expressed as μg g−1 fresh weight. Three independent 590

samples derived from five fruits at each ripening stage were used for lycopene measurements. 591

Ethylene production was determined according to Zhu et al. (2010). Fruit were 592

harvested at different ripening stages, weighed and transferred to 1 L gas-tight jars. The jars 593

were sealed and incubated at 25°C for 2 h, then 1 mL of gas sample was withdrawn from the 594

headspace with a syringe and injected into a gas chromatograph (SQ-206, Beijing, China), 595

equipped with an activated alumina column and a flame ionization detector. Three 596

independent samples derived from five fruits at each ripening stage were used for the 597

ethylene measurements. 598

599

Protein Isolation, iTRAQ Labeling, and NanoLC–MS/MS Analysis 600

Fruits were harvested at 38 dpa and 41 dpa and total cellular protein was extracted from 601

fruit pericarp tissue as described by Saravanan and Rose (2004). Proteins were solubilized in 602

a protein buffer consisting of 500 mM triethylammonium bicarbonate (TEAB) and 0.6% SDS 603

(w/v), pH 8.5, and the protein concentrations were determined using the Bradford method 604

(Bradford, 1976) with bovine serum albumin as a standard. Proteins from each sample were 605

reduced with 10 mM tris-(2-carboxyethyl) phosphine (TCEP), alkylated with 50 mM methyl 606

methanethiosulfonate (MMTS), and digested with 10 ng μL-1 trypsin using the filter-aided 607

sample preparation (FASP) method (Wiśniewski et al., 2009). The tryptic peptides were 608

labeled using the iTRAQ Reagents 4-plex Kit (Applied Biosystems, 609

http://www.appliedbiosystems.com/) according to the manufacturer’s protocol. Samples 610

taken from wild-type and SlVIF silenced tomatoes at 38 dpa were labeled with iTRAQ tags 611

116 and 114, respectively, while samples from wild-type and SlVIF silenced tomatoes at 41 612

dpa were labeled with iTRAQ tags 117 and 115, respectively. Three independent biological 613

replicates were analyzed. The iTRAQ-labeled samples were combined and then fractionated 614

with high-pH reversed-phase chromatography using the Agilent Technologies 1290 UPLC 615



31

system. Briefly, the pooled iTRAQ-labeled peptides were reconstituted using buffer A (20 616

mM ammonium formate, pH 10, in water) and loaded onto a 4.6 × 250 mm, 150 Å size 617

Durashell C18 (L) column containing 5 μm particles (Agela Technologies). The peptides was 618

eluted at a flow rate of 0.8 ml min-1 with a gradient of 2% buffer B (20 mM ammonium 619

formate in 80% acetonitrile, pH 10) for 5 min, 2-30% buffer B for 25 min, and 30-90% buffer 620

B for 10 min. The system was maintained in 90% buffer B for 10 min and then equilibrated 621

with 2% buffer B for 10 min. The elution was monitored by measuring UV absorbance at 210 622

nm, and fractions were collected every 1 min. A total of 48 fractions were collected and 623

pooled into a total of 6 fractions. After reconstitution in formic acid, the labeled peptides 624

were desalted and submitted for NanoLC–MS/MS analysis. 625

The MS analysis was carried out using a NanoLC system (NanoLC–2D Ultra Plus, 626

Eksigent, http://www.eksigent.com/) equipped with a Triple TOF 5600 Plus mass 627

spectrometer (AB SCIEX, http://www.absciex.com/). The iTRAQ-labeled peptide mixtures 628

were desalted on a 100 μm× 20 mm trap column and eluted on an analytical 75 μm× 150 mm 629

column. Both the trap column and the analytical column were filled with the Magic C18-AQ 630

5 μm 200 Å phase (Michrom BIORESOURCES, Inc). Peptides were separated by a gradient 631

formed by 0.1% formic acid (mobile phase A) and 100% acetonitrile, 0.1% formic acid 632

(mobile phase B), from 5 to 30% of mobile phase B over 75 min at a flow rate of 300 nL/min. 633

The precursor ions were selected across the mass range of 350–1500 m/z. High resolution 634

mode (>30000) was applied using 250 ms accumulation time per spectrum. A maximum of 635

25 precursors per cycle from each MS spectrum were chosen for fragmentation with 100 ms 636

minimum accumulation time for each precursor and dynamic exclusion for 18 s. Tandem 637

mass spectra were recorded in high sensitivity mode (resolution >15000) with rolling 638

collision energy and iTRAQ reagent collision energy adjustment on. 639

Protein identification and quantification were performed using ProteinPilot™ 4.5 640

software (AB SCIEX), and database searches were carried out using the S. lycopersicum 641

protein database ITAG2.4_proteins_full_desc.fasta 642

(ftp://ftp.solgenomics.net/genomes/Solanum_lycopersicum/annotation/ITAG2.4_release/). 643

The following parameters was applied: (i) Sample Type: iTRAQ 4-plex (Peptide Labeled); (ii) 644

Cysteine Alkylation: MMTS; (iii) Digestion: Trypsin; (iv) Instrument: TripleTOF 5600; (v) 645



32

Species: None; (vi) Quantitate: Yes; (vii) Bias Correction: Yes; (viii) Background Correction: 646

Yes; (ix) Search Effort: Thorough; (x) FDR Analysis: Yes. The peptide for quantification was 647

automatically chosen by the Pro GroupTM algorithm (AB SCIEX) to calculate the reporter 648

peak area. The reverse database search method (Elias and Gygi, 2007) was used to estimate 649

the global FDR for peptide identification. Proteins identified below the 1% global FDR were 650

used to calculate the meaningful cut-off value with the experimental replicate method (Gan et 651

al., 2007). 652

653

Supplemental Data 654

The following supplemental materials are available. 655

Supplemental Figure S1. The binding ability of RIN to the promoter of ACS2 as revealed by 656

chromatin immunoprecipitation. 657

Supplemental Figure S2. Chromatin immunoprecipitation reveals the direct binding of RIN 658

to the promoters of genes involved in sucrose metabolism. 659

Supplemental Figure S3. Alignment of amino acid sequences of invertase inhibitors from 660

various plants. 661

Supplemental Table S1. Genes involved in sucrose metabolism. 662

Supplemental Table S2. Primers used in qRT-PCR analysis of sucrose metabolism genes. 663

Supplemental Table S3. Ripening marker genes used for qRT-PCR analysis in this study 664

Supplemental Table S4. Gene-specific primers used in ChIP-qPCR assay. 665

Supplemental Table S5. Primers used for probes of EMSA. 666

Supplemental Table S6. Identification of the differentially expressed proteins in the SlVIF 667

silenced tomato fruit (vif) using iTRAQ-based quantitative proteomic analysis. 668

Supplemental Table S7. Primers for qRT-PCR analysis of selected genes identified in 669

iTRAQ. 670

671

ACKNOWLEDGEMENTS 672

We are grateful to Dr. James J. Giovannoni (Boyce Thompson Institute for Plant Research, 673

Cornell University) for providing the tomato seeds of wild type (Ailsa Craig) and mutant rin 674

used in the study. We thank Dr. Jing Bo Jin (Institute of Botany, the Chinese Academy of 675



33

Sciences) for providing pBI121 vector. We also thank Dr. Zhuang Lu for analysis of MS/MS. 676

677



34

FIGURE LEGENDS 678

679

Figure 1. Expression of genes involved in sucrose metabolism during fruit ripening. A, 680

Diagram of sucrose metabolism in tomato (Solanum lycopersicum). LIN, cell wall invertase; 681

VI, vacuolar invertase; NI, cytoplasmic invertase; VIF, vacuolar invertase inhibitor; CIF, cell 682

wall invertase inhibitor; SS, sucrose synthase; HK, hexokinase; FK, fructokinase; SPS, 683

sucrose phosphate synthase. B, Expression analyses of genes involved in sucrose metabolism 684

during fruit ripening in the wild type (WT) and the rin mutant by quantitative RT-PCR. The 685

stages of fruit ripening include 35 days post-anthesis (dpa), 38 dpa, 41 dpa, and 44 dpa. The 686

gene transcript levels are normalized against the ACTIN gene, followed by normalization 687

against the WT at 35 dpa. Values are means ± SD of three independent experiments. The 688

expression of ripening marker genes is shown. RIN, ripening inhibitor; NOR, non-ripening; 689

LePG, polygalacturonase A; EXP1, expansin 1; ACS2, 1-aminocyclopropane-1-carboxylate 690

synthase 2; ACO1, 1-aminocyclopropane-1-carboxylate oxidase; PSY1, phytoene synthase 1; 691

PDS, phytoene desaturase. 692

693

Figure 2. Chromatin immunoprecipitation reveals direct binding of RIN to the promoters of 694

genes involved in sucrose metabolism. The promoter regions of the target genes are indicated. 695

Red boxes represent CArG box elements and numbers above the box indicate the position of 696

these motifs relative to the translational start site. The blue fragments with upper-case letters 697

represent the regions used for ChIP-qPCR. Values are the percentage of DNA fragments that 698

were co-immunoprecipitated with specific anti-RIN antibodies, or non-specific antibodies 699

(preimmune rabbit IgG) relative to the input DNA. Error bars represent the SD of three 700

independent experiments. VI, vacuolar invertase; VIF, vacuolar invertase inhibitor; LIN, cell 701

wall invertase; CIF, cell wall invertase inhibitor; NI, cytoplasmic invertase. 702

703

Figure 3. RIN binding to the regulatory regions of target genes revealed by electrophoretic 704

mobility shift assay. The promoter regions of the target genes are indicated. Red boxes 705

indicate CArG box elements in the promoter region and numbers above represent the position 706

of these motifs relative to the translational start site. The probe sequences used for EMSA for 707



35

each target gene are shown, with red letters representing the CArG box. The protein–DNA 708

complexes were separated on 6% native polyacrylamide gels. Triangles indicate the 709

increasing amounts (10×, 100×, or 1000×) of unlabeled probes used for competition. The 710

specific complexes formed are indicated by arrowheads. VI, vacuolar invertase; VIF, 711

vacuolar invertase inhibitor; LIN, cell wall invertase; CIF, cell wall invertase inhibitor; NI, 712

cytoplasmic invertase. 713

714

Figure 4. Characterization of tomato SlVIF. A, Quantitative RT-PCR analyses of SlVIF in 715

vegetative and reproductive tomato organs. The ACTIN gene was used as an internal control. 716

Values are the means of three biological replicates. Bars represent standard deviations. B, 717

Western blot analysis of SlVIF protein abundance during fruit ripening. Proteins were 718

isolated from fruit at 35 days post-anthesis (dpa), 38 dpa, 41 dpa, and 44 dpa. An 719

anti-GAPDH (glyceraldehyde-3-phosphate dehydrogenase) immunoblot was used as a 720

protein control. In addition, Coomassie brilliant blue staining was used as a loading control. 721

C, Subcellular localization of GFP:SlVIF fusion protein. I, II and III, stable expression of the 722

GFP:SlVIF fusion protein in tomato root cells, showing fluorescent signal in the vacuole. IV, 723

V, and VI, stable expression of GFP alone in tomato root cells, showing fluorescent signals 724

throughout the cell. I and IV show fluorescent images; II and V are the same images viewed 725

using bright-field microscopy. III and VI are overlays of fluorescent and bright field images. 726

Bar =10 μm. 727

728

Figure 5. Interactions between SlVIF and SlVI. A, Inhibitory effects of recombinant SlVIF 729

on tomato vacuolar invertase and cell wall invertase. Residual invertase activity was 730

measured after pre-incubation with 10 to 160 pmol of recombinant SlVIF. Sucrose 731

concentration in the assay was 20 mM. B, Interaction between SlVIF and vacuolar invertase 732

(SlVI) in yeast. BD and AD represent plasmids pGBKT7 and pGADT7, respectively. 733

Transformants were grown on selective medium SD-LT (SD/-Leu/-Trp) and SD-LTHA 734

(SD/-Leu/-Trp/-His/-Ade) containing X-α-Gal for blue color development. 735

736

Figure 6. Function of tomato SlVIF in sucrose metabolism and fruit ripening. Invertase 737



36

activity, sugar content, color change phenotype, lycopene content, and ethylene production in 738

fruit of SlVIF overexpressing line 2 (OE2), SlVIF silenced line 4 (S4) and wild type (WT) 739

were examined during fruit ripening. A, Vacuolar invertase (VI) activity. B, Cell wall 740

invertase (CWI) activity. C, Neutral invertase (NI) activity. D, Sucrose content. E, Glucose 741

content. F, Fructose content. G, Photos of fruit from transgenic lines and wild-type control. H, 742

Lycopene content. I, Ethylene production. Bars represent standard deviations of three 743

biological replicates. 744

745

Figure 7. Expression of ripening marker genes in SlVIF overexpressing and silenced tomato 746

(Solanum lycopersicum) fruits. The gene transcript levels were determined by quantitative 747

RT-PCR. Total RNA was extracted from pericarp tissues of SlVIF overexpressing line 2 748

(OE2), SlVIF silenced line 4 (S4) and wild type (WT) at 35 days post-anthesis (dpa), 38 dpa, 749

41 dpa, and 44 dpa. The gene transcript levels are normalized against the ACTIN gene, 750

followed by normalization against the WT at 35 dpa. Values are means ± SD of three 751

independent experiments. RIN, ripening inhibitor; NOR, non-ripening; LePG, 752

polygalacturonase A; EXP1, expansin 1; ACS2, 1-aminocyclopropane-1-carboxylate synthase 753

2; ACO1, 1-aminocyclopropane-1-carboxylate oxidase; PSY1, phytoene synthase 1; PDS, 754

phytoene desaturase. 755

756

Figure 8. Identification of differentially expressed proteins in SlVIF silenced tomato fruits by 757

iTRAQ-based quantitative proteomic analysis. A, Schematic diagram of the workflow used in 758

this study. Three sets of biological replicate samples from wild-type (WT) and SlVIF silenced 759

fruit (vif) at 38 days post-anthesis (dpa) and 41 dpa were analyzed by iTRAQ, using the 760

nanoLC-MS/MS workflow for examining proteome changes. B, GO categories of 761

differentially expressed proteins at 38 dpa or 41 dpa. C, Venn diagram of differentially 762

expressed proteins identified at 38 dpa and 41 dpa. The numbers of differentially abundant 763

proteins at each ripening stage are shown. 764

765

Figure 9. Quantitative proteomic analysis showing that ripening-related genes are affected by 766

SlVIF expression. The changes in protein abundance in the SlVIF silenced fruits (vif) at 38 767



37

days post-anthesis (dpa) and 41 dpa are shown as the ratio between vif and wild type (WT). 768

The mRNA expression levels were measured by quantitative real-time PCR. Total RNA was 769

extracted from pericarp tissues of SlVIF silenced fruit (vif) and WT at 35 dpa, 38 dpa, 41 dpa, 770

and 44 dpa. The gene transcript levels were normalized against the ACTIN gene, followed by 771

normalization against the WT at 35 dpa. The changes in transcript levels at 38 dpa and 41 dpa 772

are shown. The results for both protein and mRNA expression are means ± SD from three 773

independent experiments. PDS, phytoene desaturase; CRTISO, carotenoid isomerase; ACO1, 774

1-aminocyclopropane-1-carboxylate oxidase; E4, peptide methionine sulfoxide reductase; E8, 775

1-aminocyclopropane-1-carboxylate oxidase-like protein; SAM1, S-adenosylmethionine 776

synthase 1; SAM3, S-adenosylmethionine synthase 3; LoxC, lipoxygenase; PAL, 777

phenylalanine ammonia-lyase; VI, vacuolar invertase; LePG, polygalacturonase A; MAN4, 778

mannan endo-1 4-beta-mannosidase; PME2.1, pectinesterase; EXPA4, expansin. 779



38

REFERENCE 780

Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni 781

JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of 782

ethylene control during tomato fruit development. Plant Cell 17: 2954-2965. 783

Bate NJ, Niu X, Wang Y, Reimann KS, Helentjaris TG (2004) An invertase inhibitor from 784

maize localizes to the embryo surrounding region during early kernel development. Plant 785

physiol 134: 246-254. 786

Borsanie J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo 787

CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: 788

changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60: 789

1823-1837. 790

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram 791

quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 792

248-254. 793

Brummell DA, Chen RK, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ 794

(2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to 795

cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 796

62: 3519-3534. 797

Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J 798

Exp Bot 57: 1883-1897. 799

Choi ST, Huber DJ (2008) Influence of aqueous 1-methylcyclopropene concentration, 800

immersion duration, and solution longevity on the postharvest ripening of breaker-turning 801

tomato (Solanum lycopersicum L.) fruit. Postharvest Biol Tec 49: 147-154. 802

Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and 803

functions. Phytochemistry 68: 709-731. 804

Davies C, Robinson SP (1996) Sugar accumulation in grape berries: cloning of two putative 805

vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 111: 806

275-283. 807

Ecker JR (2013) Epigenetic trigger for tomato ripening. Nat Biotechnol 31: 119-120. 808

Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in 809



39

large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214. 810

Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE 811

(1993) Isolation and characterization of fruit vacuolar invertase genes from two tomato 812

species and temporal differences in mRNA levels during fruit ripening. Plant Mol Biol 21: 813

515-524. 814

Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 815

3367-3377. 816

Fraser PD, Truesdale M, Bird CR, Schuch W, Bramley PM (1994) Carotenoid 817

biosynthesis during tomato fruit development. Plant Physiol 105: 405-413. 818

Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance 819

gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5: 820

726-730. 821

Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative 822

trait for tomato yield using interspecific introgressions. Science 305: 1786-1789. 823

Fridman E, Zamir D (2003) Functional divergence of a syntenic invertase gene family in 824

tomato, potato, and Arabidopsis. Plant Physiol 131: 603-609. 825

Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets 826

of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the 827

regulation of fruit ripening. Plant Cell 25: 371-386. 828

Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological 829

variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 830

6: 821-827. 831

German, MA, Asher I, Petreikov M, Dai N, Schaffer AA, Granot D (2004) Cloning, 832

expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum 833

Mill.) gene encoding fructokinase. Plant Sci 166: 285-291. 834

German MA, Dai N, Chmelnitsky I, Sobolev I, Salts Y, Barg R, Schaffer AA, Granot D 835

(2002) LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically 836

expressed in stamens. Plant Sci 163: 607-613. 837

Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16 838

(suppl.): S170-S180. 839



40

Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin 840

Plant Biol 10: 283-289. 841

Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three 842

extracellular invertase isoenzymes of tomato suggests an important function in 843

establishing and maintaining sink metabolism. Plant Physiol 115: 273-282. 844

Goren S, Huber SC, Granot D (2011) Comparison of a novel tomato sucrose synthase, 845

SlSUS4, with previously described SlSUS isoforms reveals distinct sequence features and 846

differential expression patterns in association with stem maturation. Planta 233: 847

1011-1023. 848

Greiner S, Krausgrill S, Rausch T (1998) Cloning of a tobacco apoplasmic invertase 849

inhibitor - Proof of function of the recombinant protein and expression analysis during 850

plant development. Plant physiol 116: 733-742. 851

Greiner S, Rausch T, Sonnewald U, Herbers K (1999) Ectopic expression of a tobacco 852

invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat 853

Biotechnol 17: 708-711. 854

Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the 855

target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant 856

Cell 16: 3437-3447. 857

Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher 858

plants. Annul Rev. Plant Physiol Plant Mole Biol 47: 431-444. 859

Iglesias DJ, Tadeo FR, Legaz F, Primo-Millo E, Talon M (2001) In vivo sucrose 860

stimulation of colour change in citrus fruit epicarps: Interactions between nutritional 861

andhormonal signals. Physiol Plant 112: 244-250. 862

Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, 863

Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin 864

mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55: 212-223. 865

Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by 866

silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit 867

hexose level. Plant Cell 21: 2072-2089. 868

Kanayama Y, Dai N, Granot D, Petreikov M, Schaffer A, Bennett AB (1997) Divergent 869



41

fructokinase genes are differentially expressed in tomato. Plant Physiol 113: 1379-1384. 870

Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, 871

Petreikov M, Adir N, Granot D (2006) Two newly identified membrane-associated and 872

plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. 873

Planta 224: 1341-1352. 874

Karimi M, Inzé D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated 875

plant transformation. Trends Plant Sci 7: 193-195. 876

Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls 877

sugar composition in tomato (Lycopersicon) fruit. Plant Physiol 103: 863-870. 878

Klann EM, Hall B, Bennett AB (1996) Antisense acid invertase (TIV1) gene alters soluble 879

sugar composition and size in transgenic tomato fruit. Plant physiol 112: 1321-1330. 880

Klann E, Yelle S, Bennett AB (1992) Tomato fruit acid invertase complementary DNA : 881

nucleotide and deduced amino acid sequences. Plant Physiol 99: 351-353. 882

Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality 883

attributes. Annu Rev Genet 45: 41-59. 884

Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose 885

export and is involved in symptom development and inhibition of photosynthesis during 886

compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant 887

Physiol 148: 1523-1536. 888

Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar 889

sensing and plant development. Curr Opin Plant Biol 7: 235-246. 890

Li Z, Palmer WM, Martin AP, Wang R, Rainsford F, Jin Y, Patrick JW, Yang Y, Ruan 891

YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced 892

sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63: 1155-1166. 893

Link M, Rausch T, Greiner S (2004) In Arabidopsis thaliana, the invertase inhibitors 894

AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. FEBS 895

Lett 573: 105-109. 896

Long JC, Shao W, Rashotte AM, Muday GK, Huber SC (2002) Gravity-stimulated 897

changes in auxin and invertase gene expression in maize pulvinal cells. Plant Physiol 128: 898

591-602. 899



42

Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant 900

Biol 6: 208-214. 901

Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box 902

transcription factor RIPENING INHIBITOR interacts with promoters involved in 903

numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. 904

Plant physiol 157: 1568-1579. 905

Mason G, Provero P, Vaira AM, Accotto GP (2002) Estimating the number of integrations 906

in transformed plants by quantitative real-time PCR. BMC Biotechnol 2: 20. 907

Menu T, Rothan C, Dai N, Petreikov M, Etienne C, Destrac-Irvine A, Schaffer A, 908

Granot D, Ricard B (2001) Cloning and characterization of a cDNA encoding 909

hexokinase from tomato. Plant Sci 160: 209-218. 910

Miron D, Schaffer AA (1991) Sucrose phosphate synthase, sucrose synthase, and invertase 911

activities in developing fruit of Lycopersicon esculentum Mill. and the sucrose 912

accumulating Lycopersicon hirsutum Humb. and Bonpl. Plant physiol 95: 623-627. 913

Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato 914

microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56: 915

2885-2895. 916

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with 917

tobacco tissue cultures. Physiol Plant 15: 473-497. 918

Proels R, Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for 919

integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J 920

Exp Bot 60: 1555-1567. 921

Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the 922

MADS box transcription factor RIN in fruit ripening. Plant J 70: 243-255. 923

Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. Biochem Biophys Acta 924

1696: 253-261. 925

Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14 926

(suppl.): S185-S205. 927

Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling 928

mediated by invertase: roles in development, yield potential, and response to drought and 929



43

heat. Mol Plant 3: 942-955. 930

Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for 931

enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4: 2522-2532. 932

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) 933

method. Nat Protoc 3: 1101-1108. 934

Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and 935

sucrose partitioning. Plant physiol 121: 1-8. 936

Sumner JB (1921) Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and 937

diabetic urine. J Biol Chem 47: 5-9. 938

Télef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, 939

Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit 940

pericarp discs. Plant Mol Biol 62: 453-469. 941

Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional 942

regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci USA 99: 943

10876-10880. 944

Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, 945

Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato 946

ripening-inhibitor (Rin) locus. Science 296: 343-346. 947

Wang F, Smith AG, Brenner ML (1993) Isolation and sequencing of tomato fruit sucrose 948

synthase cDNA. Plant Physiol 103: 1463-1464. 949

Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S (2014) Tomato nuclear proteome 950

reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. 951

Genome Biol 15: 548. 952

Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation 953

method for proteome analysis. Nat Methods 6: 359-362. 954

Yu X, Wang X, Zhang W, Qian T, Tang G, Guo Y, Zheng C (2008) Antisense 955

suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit 956

development. J Exp Bot 59: 2969-2977. 957

Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu 958

B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato 959



44

fruit development reveal epigenome modifications associated with ripening. Nat 960

Biotechnol 31: 154-159. 961

Zhu Z, Liu RL, Li BQ, Tian SP (2013) Characterisation of genes encoding key enzymes 962

involved in sugar metabolism of apple fruit in controlled atmosphere storage. Food Chem 963

141: 3323-3328. 964

Zhu Z, Zhang ZQ, Qin GZ, Tian SP (2010) Effects of brassinosteroids on postharvest 965

disease and senescence of jujube fruit in storage. Postharvest Biol Tec 56: 50-55. 966

967



Parsed CitationsAlba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selectedmetabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17: 2954-2965.

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

Bate NJ, Niu X, Wang Y, Reimann KS, Helentjaris TG (2004) An invertase inhibitor from maize localizes to the embryo surroundingregion during early kernel development. Plant physiol 134: 246-254.


Borsanie J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbonmetabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60:1823-1837.


Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle ofprotein-dye binding. Anal Biochem 72: 248-254.


Brummell DA, Chen RK, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitormRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot62: 3519-3534.


Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57: 1883-1897.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Choi ST, Huber DJ (2008) Influence of aqueous 1-methylcyclopropene concentration, immersion duration, and solution longevityon the postharvest ripening of breaker-turning tomato (Solanum lycopersicum L.) fruit. Postharvest Biol Tec 49: 147-154.


Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68: 709-731.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Davies C, Robinson SP (1996) Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and theirexpression in grapevine tissues. Plant Physiol 111: 275-283.


Ecker JR (2013) Epigenetic trigger for tomato ripening. Nat Biotechnol 31: 119-120.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by massspectrometry. Nat Methods 4: 207-214.


Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE (1993) Isolation and characterization of fruitvacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Mol Biol21: 515-524.


Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 3367-3377.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Fraser PD, Truesdale M, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development. Planthttps://plantphysiol.orgDownloaded on May 3, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Alba R%2C Payton P%2C Fei Z%2C McQuinn R%2C Debbie P%2C Martin GB%2C Tanksley SD%2C Giovannoni JJ %282005%29 Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development%2E Plant Cell 17%3A 2954%2D2965%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17: 2954-2965.

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

http://scholar.google.com/scholar?as_q=Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit 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=Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Alba&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bate NJ%2C Niu X%2C Wang Y%2C Reimann KS%2C Helentjaris TG %282004%29 An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development%2E Plant physiol 134%3A 246%2D254%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bate NJ, Niu X, Wang Y, Reimann KS, Helentjaris TG (2004) An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant physiol 134: 246-254.

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

http://scholar.google.com/scholar?as_q=An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel 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=An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bate&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Borsanie J%2C Budde CO%2C Porrini L%2C Lauxmann MA%2C Lombardo VA%2C Murray R%2C Andreo CS%2C Drincovich MF%2C Lara MV %282009%29 Carbon metabolism of peach fruit after harvest%3A changes in enzymes involved in organic acid and sugar level modifications%2E J Exp Bot 60%3A 1823%2D1837%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Borsanie J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60: 1823-1837.

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

http://scholar.google.com/scholar?as_q=Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications&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=Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Borsanie&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bradford MM %281976%29 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein%2Ddye binding%2E Anal Biochem 72%3A 248%2D254%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.

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

http://scholar.google.com/scholar?as_q=A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding&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 rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bradford&as_ylo=1976&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Brummell DA%2C Chen RK%2C Harris JC%2C Zhang H%2C Hamiaux C%2C Kralicek AV%2C McKenzie MJ %282011%29 Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold%2Dinduced sweetening resistance and includes spliced hybrid mRNA variants%2E J Exp Bot 62%3A 3519%2D3534%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Brummell DA, Chen RK, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 62: 3519-3534.

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

http://scholar.google.com/scholar?as_q=Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants&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=Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brummell&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Carrari F%2C Fernie AR %282006%29 Metabolic regulation underlying tomato fruit development%2E J Exp Bot 57%3A 1883%2D1897%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57: 1883-1897.

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

http://scholar.google.com/scholar?as_q=Metabolic regulation underlying tomato fruit 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=Metabolic regulation underlying tomato fruit development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Carrari&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Choi ST%2C Huber DJ %282008%29 Influence of aqueous 1%2Dmethylcyclopropene concentration%2C immersion duration%2C and solution longevity on the postharvest ripening of breaker%2Dturning tomato %28Solanum lycopersicum L%2E%29 fruit%2E Postharvest Biol Tec 49%3A 147%2D154%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Choi ST, Huber DJ (2008) Influence of aqueous 1-methylcyclopropene concentration, immersion duration, and solution longevity on the postharvest ripening of breaker-turning tomato (Solanum lycopersicum L.) fruit. Postharvest Biol Tec 49: 147-154.

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

http://scholar.google.com/scholar?as_q=Influence of aqueous 1-methylcyclopropene concentration, immersion duration, and solution longevity on the postharvest ripening of breaker-turning tomato (Solanum lycopersicum L&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=Influence of aqueous 1-methylcyclopropene concentration, immersion duration, and solution longevity on the postharvest ripening of breaker-turning tomato (Solanum lycopersicum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Choi&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Claeyssen E%2C Rivoal J %282007%29 Isozymes of plant hexokinase%3A occurrence%2C properties and functions%2E Phytochemistry 68%3A 709%2D731%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68: 709-731.

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

http://scholar.google.com/scholar?as_q=Isozymes of plant hexokinase: occurrence, properties and 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=Isozymes of plant hexokinase: occurrence, properties and functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Claeyssen&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Davies C%2C Robinson SP %281996%29 Sugar accumulation in grape berries%3A cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues%2E Plant Physiol 111%3A 275%2D283%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Davies C, Robinson SP (1996) Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 111: 275-283.

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

http://scholar.google.com/scholar?as_q=Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues&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=Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Davies&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ecker JR %282013%29 Epigenetic trigger for tomato ripening%2E Nat Biotechnol 31%3A 119%2D120%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ecker JR (2013) Epigenetic trigger for tomato ripening. Nat Biotechnol 31: 119-120.

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

http://scholar.google.com/scholar?as_q=Epigenetic trigger for tomato ripening&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=Epigenetic trigger for tomato ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ecker&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Elias JE%2C Gygi SP %282007%29 Target%2Ddecoy search strategy for increased confidence in large%2Dscale protein identifications by mass spectrometry%2E Nat Methods 4%3A 207%2D214%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.

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

http://scholar.google.com/scholar?as_q=Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry&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=Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Elias&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Elliott KJ%2C Butler WO%2C Dickinson CD%2C Konno Y%2C Vedvick TS%2C Fitzmaurice L%2C Mirkov TE %281993%29 Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening%2E Plant Mol Biol 21%3A 515%2D524%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE (1993) Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Mol Biol 21: 515-524.

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

http://scholar.google.com/scholar?as_q=Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening&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 fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Elliott&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Eveland AL%2C Jackson DP %282012%29 Sugars%2C signalling%2C and plant development%2E J Exp Bot 63%3A 3367%2D3377%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 3367-3377.

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

http://scholar.google.com/scholar?as_q=Sugars, signalling, and plant 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=Sugars, signalling, and plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Eveland&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


Physiol 105: 405-413.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binaryAgrobacterium tumefaciens vector. Nat Biotechnol 5: 726-730.


Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecificintrogressions. Science 305: 1786-1789.


Fridman E, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. PlantPhysiol 131: 603-609.


Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcriptionfactor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25: 371-386.


Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological variations in isobaric tags for relative andabsolute quantitation (iTRAQ). J Proteome Res 6: 821-827.


German, MA, Asher I, Petreikov M, Dai N, Schaffer AA, Granot D (2004) Cloning, expression and characterization of LeFRK3, thefourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Sci 166: 285-291.


German MA, Dai N, Chmelnitsky I, Sobolev I, Salts Y, Barg R, Schaffer AA, Granot D (2002) LeFRK4, a novel tomato (Lycopersiconesculentum Mill.) fructokinase specifically expressed in stamens. Plant Sci 163: 607-613.


Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16 (suppl.): S170-S180.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10: 283-289.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes oftomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115: 273-282.


Goren S, Huber SC, Granot D (2011) Comparison of a novel tomato sucrose synthase, SlSUS4, with previously described SlSUSisoforms reveals distinct sequence features and differential expression patterns in association with stem maturation. Planta 233:1011-1023.


Greiner S, Krausgrill S, Rausch T (1998) Cloning of a tobacco apoplasmic invertase inhibitor - Proof of function of the recombinantprotein and expression analysis during plant development. Plant physiol 116: 733-742.


Greiner S, Rausch T, Sonnewald U, Herbers K (1999) Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat Biotechnol 17: 708-711.

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title https://plantphysiol.orgDownloaded on May 3, 2021. - Published by

Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Fraser PD%2C Truesdale M%2C Bird CR%2C Schuch W%2C Bramley PM %281994%29 Carotenoid biosynthesis during tomato fruit development%2E Plant Physiol 105%3A 405%2D413%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fraser PD, Truesdale M, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development. Plant Physiol 105: 405-413.

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

http://scholar.google.com/scholar?as_q=Carotenoid biosynthesis during tomato fruit 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=Carotenoid biosynthesis during tomato fruit development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fraser&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fillatti JJ%2C Kiser J%2C Rose R%2C Comai L %281987%29 Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector%2E Nat Biotechnol 5%3A 726%2D730%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5: 726-730.

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

http://scholar.google.com/scholar?as_q=Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector&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=Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fillatti&as_ylo=1987&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fridman E%2C Carrari F%2C Liu YS%2C Fernie AR%2C Zamir D %282004%29 Zooming in on a quantitative trait for tomato yield using interspecific introgressions%2E Science 305%3A 1786%2D1789%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305: 1786-1789.

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=Zooming in on a quantitative trait for tomato yield using interspecific introgressions&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=Zooming in on a quantitative trait for tomato yield using interspecific introgressions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fridman&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fridman E%2C Zamir D %282003%29 Functional divergence of a syntenic invertase gene family in tomato%2C potato%2C and Arabidopsis%2E Plant Physiol 131%3A 603%2D609%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fridman E, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. Plant Physiol 131: 603-609.

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=Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fridman&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fujisawa M%2C Nakano T%2C Shima Y%2C Ito Y %282013%29 A large%2Dscale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening%2E Plant Cell 25%3A 371%2D386%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25: 371-386.

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

http://scholar.google.com/scholar?as_q=A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening&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 large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fujisawa&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gan CS%2C Chong PK%2C Pham TK%2C Wright PC %282007%29 Technical%2C experimental%2C and biological variations in isobaric tags for relative and absolute quantitation %28iTRAQ%29%2E J Proteome Res 6%3A 821%2D827%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 6: 821-827.

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

http://scholar.google.com/scholar?as_q=Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ)&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=Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gan&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=German%2C MA%2C Asher I%2C Petreikov M%2C Dai N%2C Schaffer AA%2C Granot D %282004%29 Cloning%2C expression and characterization of LeFRK3%2C the fourth tomato %28Lycopersicon esculentum Mill%2E%29 gene encoding fructokinase%2E Plant Sci 166%3A 285%2D291%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=German, MA, Asher I, Petreikov M, Dai N, Schaffer AA, Granot D (2004) Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Sci 166: 285-291.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=German,&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=German,&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=German MA%2C Dai N%2C Chmelnitsky I%2C Sobolev I%2C Salts Y%2C Barg R%2C Schaffer AA%2C Granot D %282002%29 LeFRK4%2C a novel tomato %28Lycopersicon esculentum Mill%2E%29 fructokinase specifically expressed in stamens%2E Plant Sci 163%3A 607%2D613%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=German MA, Dai N, Chmelnitsky I, Sobolev I, Salts Y, Barg R, Schaffer AA, Granot D (2002) LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. Plant Sci 163: 607-613.

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=German&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Giovannoni JJ %282004%29 Genetic regulation of fruit development and ripening%2E Plant Cell 16 %28suppl%2E%29%3A S170%2DS180%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16 (suppl.): S170-S180.

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

http://scholar.google.com/scholar?as_q=Genetic regulation of fruit development and ripening.&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=Genetic regulation of fruit development and ripening.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Giovannoni&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Giovannoni JJ %282007%29 Fruit ripening mutants yield insights into ripening control%2E Curr Opin Plant Biol 10%3A 283%2D289%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10: 283-289.

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

http://scholar.google.com/scholar?as_q=Fruit ripening mutants yield insights into ripening control&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=Fruit ripening mutants yield insights into ripening control&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Giovannoni&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Godt DE%2C Roitsch T %281997%29 Regulation and tissue%2Dspecific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism%2E Plant Physiol 115%3A 273%2D282%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115: 273-282.

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

http://scholar.google.com/scholar?as_q=Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink 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=Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Godt&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Goren S%2C Huber SC%2C Granot D %282011%29 Comparison of a novel tomato sucrose synthase%2C SlSUS4%2C with previously described SlSUS isoforms reveals distinct sequence features and differential expression patterns in association with stem maturation%2E Planta 233%3A 1011%2D1023%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Goren S, Huber SC, Granot D (2011) Comparison of a novel tomato sucrose synthase, SlSUS4, with previously described SlSUS isoforms reveals distinct sequence features and differential expression patterns in association with stem maturation. Planta 233: 1011-1023.

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Goren&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Greiner S%2C Krausgrill S%2C Rausch T %281998%29 Cloning of a tobacco apoplasmic invertase inhibitor %2D Proof of function of the recombinant protein and expression analysis during plant development%2E Plant physiol 116%3A 733%2D742%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Greiner S, Krausgrill S, Rausch T (1998) Cloning of a tobacco apoplasmic invertase inhibitor - Proof of function of the recombinant protein and expression analysis during plant development. Plant physiol 116: 733-742.

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

http://scholar.google.com/scholar?as_q=Cloning of a tobacco apoplasmic invertase inhibitor - Proof of function of the recombinant protein and expression analysis during plant 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=Cloning of a tobacco apoplasmic invertase inhibitor - Proof of function of the recombinant protein and expression analysis during plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Greiner&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Greiner S%2C Rausch T%2C Sonnewald U%2C Herbers K %281999%29 Ectopic expression of a tobacco invertase inhibitor homolog prevents cold%2Dinduced sweetening of potato tubers%2E Nat Biotechnol 17%3A 708%2D711%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Greiner S, Rausch T, Sonnewald U, Herbers K (1999) Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat Biotechnol 17: 708-711.

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

http://scholar.google.com/scholar?as_q=Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers&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=Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Greiner&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1


Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectinmethylesterase inhibitory proteins. Plant Cell 16: 3437-3447.


Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annul Rev. Plant Physiol PlantMole Biol 47: 431-444.


Iglesias DJ, Tadeo FR, Legaz F, Primo-Millo E, Talon M (2001) In vivo sucrose stimulation of colour change in citrus fruit epicarps:Interactions between nutritional andhormonal signals. Physiol Plant 112: 244-250.


Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity,transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55: 212-223.


Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leafsenescence and increases seed weight and fruit hexose level. Plant Cell 21: 2072-2089.


Kanayama Y, Dai N, Granot D, Petreikov M, Schaffer A, Bennett AB (1997) Divergent fructokinase genes are differentiallyexpressed in tomato. Plant Physiol 113: 1379-1384.


Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, Petreikov M, Adir N, Granot D (2006) Two newlyidentified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization.Planta 224: 1341-1352.


Karimi M, Inzé D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193-195.


Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon)fruit. Plant Physiol 103: 863-870.


Klann EM, Hall B, Bennett AB (1996) Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenictomato fruit. Plant physiol 112: 1321-1330.


Klann E, Yelle S, Bennett AB (1992) Tomato fruit acid invertase complementary DNA : nucleotide and deduced amino acidsequences. Plant Physiol 99: 351-353.


Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptomdevelopment and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pvvesicatoria. Plant Physiol 148: 1523-1536.


Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opinhttps://plantphysiol.orgDownloaded on May 3, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Hothorn M%2C Wolf S%2C Aloy P%2C Greiner S%2C Scheffzek K %282004%29 Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins%2E Plant Cell 16%3A 3437%2D3447%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell 16: 3437-3447.

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

http://scholar.google.com/scholar?as_q=Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins&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=Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hothorn&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Huber SC%2C Huber JL %281996%29 Role and regulation of sucrose%2Dphosphate synthase in higher plants%2E Annul Rev%2E Plant Physiol Plant Mole Biol 47%3A 431%2D444%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annul Rev. Plant Physiol Plant Mole Biol 47: 431-444.

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

http://scholar.google.com/scholar?as_q=Role and regulation of sucrose-phosphate synthase in higher 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=Role and regulation of sucrose-phosphate synthase in higher plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Huber&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Iglesias DJ%2C Tadeo FR%2C Legaz F%2C Primo%2DMillo E%2C Talon M %282001%29 In vivo sucrose stimulation of colour change in citrus fruit epicarps%3A Interactions between nutritional andhormonal signals%2E Physiol Plant 112%3A 244%2D250%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Iglesias DJ, Tadeo FR, Legaz F, Primo-Millo E, Talon M (2001) In vivo sucrose stimulation of colour change in citrus fruit epicarps: Interactions between nutritional andhormonal signals. Physiol Plant 112: 244-250.

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

http://scholar.google.com/scholar?as_q=In vivo sucrose stimulation of colour change in citrus fruit epicarps: Interactions between nutritional andhormonal signals&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 vivo sucrose stimulation of colour change in citrus fruit epicarps: Interactions between nutritional andhormonal signals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Iglesias&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ito Y%2C Kitagawa M%2C Ihashi N%2C Yabe K%2C Kimbara J%2C Yasuda J%2C Ito H%2C Inakuma T%2C Hiroi S%2C Kasumi T %282008%29 DNA%2Dbinding specificity%2C transcriptional activation potential%2C and the rin mutation effect for the tomato fruit%2Dripening regulator RIN%2E Plant J 55%3A 212%2D223%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55: 212-223.

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

http://scholar.google.com/scholar?as_q=DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN&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=DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ito&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jin Y%2C Ni DA%2C Ruan YL %282009%29 Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level%2E Plant Cell 21%3A 2072%2D2089%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21: 2072-2089.

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

http://scholar.google.com/scholar?as_q=Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level&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=Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jin&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kanayama Y%2C Dai N%2C Granot D%2C Petreikov M%2C Schaffer A%2C Bennett AB %281997%29 Divergent fructokinase genes are differentially expressed in tomato%2E Plant Physiol 113%3A 1379%2D1384%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kanayama Y, Dai N, Granot D, Petreikov M, Schaffer A, Bennett AB (1997) Divergent fructokinase genes are differentially expressed in tomato. Plant Physiol 113: 1379-1384.

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

http://scholar.google.com/scholar?as_q=Divergent fructokinase genes are differentially expressed in 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=Divergent fructokinase genes are differentially expressed in tomato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kanayama&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kandel%2DKfir M%2C Damari%2DWeissler H%2C German MA%2C Gidoni D%2C Mett A%2C Belausov E%2C Petreikov M%2C Adir N%2C Granot D %282006%29 Two newly identified membrane%2Dassociated and plastidic tomato HXKs%3A characteristics%2C predicted structure and intracellular localization%2E Planta 224%3A 1341%2D1352%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, Petreikov M, Adir N, Granot D (2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta 224: 1341-1352.

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

http://scholar.google.com/scholar?as_q=Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization&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=Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kandel-Kfir&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Karimi M%2C Inz� D%2C Depicker A %282002%29 GATEWAYTM vectors for Agrobacterium%2Dmediated plant transformation%2E Trends Plant Sci 7%3A 193%2D195%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karimi M, Inz� D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195.

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

http://scholar.google.com/scholar?as_q=GATEWAYTM vectors for Agrobacterium-mediated plant transformation&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=GATEWAYTM vectors for Agrobacterium-mediated plant transformation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Karimi&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klann EM%2C Chetelat RT%2C Bennett AB %281993%29 Expression of acid invertase gene controls sugar composition in tomato %28Lycopersicon%29 fruit%2E Plant Physiol 103%3A 863%2D870%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol 103: 863-870.

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

http://scholar.google.com/scholar?as_q=Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit&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=Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klann&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klann EM%2C Hall B%2C Bennett AB %281996%29 Antisense acid invertase %28TIV1%29 gene alters soluble sugar composition and size in transgenic tomato fruit%2E Plant physiol 112%3A 1321%2D1330%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klann EM, Hall B, Bennett AB (1996) Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant physiol 112: 1321-1330.


http://scholar.google.com/scholar?as_q=Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit&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=Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klann&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klann E%2C Yelle S%2C Bennett AB %281992%29 Tomato fruit acid invertase complementary DNA %3A nucleotide and deduced amino acid sequences%2E Plant Physiol 99%3A 351%2D353%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klann E, Yelle S, Bennett AB (1992) Tomato fruit acid invertase complementary DNA : nucleotide and deduced amino acid sequences. Plant Physiol 99: 351-353.


http://scholar.google.com/scholar?as_q=Tomato fruit acid invertase complementary DNA : nucleotide and deduced amino acid sequences&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato fruit acid invertase complementary DNA : nucleotide and deduced amino acid sequences&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klann&as_ylo=1992&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klee HJ%2C Giovannoni JJ %282011%29 Genetics and control of tomato fruit ripening and quality attributes%2E Annu Rev Genet 45%3A 41%2D59%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59.

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

http://scholar.google.com/scholar?as_q=Genetics and control of tomato fruit ripening and quality attributes&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=Genetics and control of tomato fruit ripening and quality attributes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klee&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kocal N%2C Sonnewald U%2C Sonnewald S %282008%29 Cell wall%2Dbound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria%2E Plant Physiol 148%3A 1523%2D1536%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148: 1523-1536.

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

http://scholar.google.com/scholar?as_q=Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria&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=Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kocal&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1


Plant Biol 7: 235-246.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Li Z, Palmer WM, Martin AP, Wang R, Rainsford F, Jin Y, Patrick JW, Yang Y, Ruan YL (2012) High invertase activity in tomatoreproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63: 1155-1166.


Link M, Rausch T, Greiner S (2004) In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzymespecificities and expression profiles. FEBS Lett 573: 105-109.


Long JC, Shao W, Rashotte AM, Muday GK, Huber SC (2002) Gravity-stimulated changes in auxin and invertase gene expressionin maize pulvinal cells. Plant Physiol 128: 591-602.


Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6: 208-214.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITORinteracts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plantphysiol 157: 1568-1579.


Mason G, Provero P, Vaira AM, Accotto GP (2002) Estimating the number of integrations in transformed plants by quantitative real-time PCR. BMC Biotechnol 2: 20.


Menu T, Rothan C, Dai N, Petreikov M, Etienne C, Destrac-Irvine A, Schaffer A, Granot D, Ricard B (2001) Cloning andcharacterization of a cDNA encoding hexokinase from tomato. Plant Sci 160: 209-218.


Miron D, Schaffer AA (1991) Sucrose phosphate synthase, sucrose synthase, and invertase activities in developing fruit ofLycopersicon esculentum Mill. and the sucrose accumulating Lycopersicon hirsutum Humb. and Bonpl. Plant physiol 95: 623-627.


Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expressionanalysis in the Solanaceae. J Exp Bot 56: 2885-2895.


Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497.


Proels R, Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, andstress signals is regulated by a diurnal rhythm. J Exp Bot 60: 1555-1567.


Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruitripening. Plant J 70: 243-255.


Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. Biochem Biophys Acta 1696: 253-261.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title https://plantphysiol.orgDownloaded on May 3, 2021. - Published by


http://www.ncbi.nlm.nih.gov/pubmed?term=Koch K %282004%29 Sucrose metabolism%3A regulatory mechanisms and pivotal roles in sugar sensing and plant development%2E Curr Opin Plant Biol 7%3A 235%2D246%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246.

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

http://scholar.google.com/scholar?as_q=Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant 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=Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Koch&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Li Z%2C Palmer WM%2C Martin AP%2C Wang R%2C Rainsford F%2C Jin Y%2C Patrick JW%2C Yang Y%2C Ruan YL %282012%29 High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into%2C and heat tolerance of%2C young fruit%2E J Exp Bot 63%3A 1155%2D1166%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li Z, Palmer WM, Martin AP, Wang R, Rainsford F, Jin Y, Patrick JW, Yang Y, Ruan YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63: 1155-1166.

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

http://scholar.google.com/scholar?as_q=High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit&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=High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Link M%2C Rausch T%2C Greiner S %282004%29 In Arabidopsis thaliana%2C the invertase inhibitors AtC%2FVIF1 and 2 exhibit distinct target enzyme specificities and expression profiles%2E FEBS Lett 573%3A 105%2D109%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Link M, Rausch T, Greiner S (2004) In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. FEBS Lett 573: 105-109.

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

http://scholar.google.com/scholar?as_q=In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles&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 Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Link&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Long JC%2C Shao W%2C Rashotte AM%2C Muday GK%2C Huber SC %282002%29 Gravity%2Dstimulated changes in auxin and invertase gene expression in maize pulvinal cells%2E Plant Physiol 128%3A 591%2D602%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Long JC, Shao W, Rashotte AM, Muday GK, Huber SC (2002) Gravity-stimulated changes in auxin and invertase gene expression in maize pulvinal cells. Plant Physiol 128: 591-602.

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

http://scholar.google.com/scholar?as_q=Gravity-stimulated changes in auxin and invertase gene expression in maize pulvinal cells&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Gravity-stimulated changes in auxin and invertase gene expression in maize pulvinal cells&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Long&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lunn JE%2C MacRae E %282003%29 New complexities in the synthesis of sucrose%2E Curr Opin Plant Biol 6%3A 208%2D214%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6: 208-214.

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

http://scholar.google.com/scholar?as_q=New complexities in the synthesis of sucrose&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=New complexities in the synthesis of sucrose&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lunn&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Martel C%2C Vrebalov J%2C Tafelmeyer P%2C Giovannoni JJ %282011%29 The tomato MADS%2Dbox transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING%2Ddependent manner%2E Plant physiol 157%3A 1568%2D1579%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant physiol 157: 1568-1579.

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

http://scholar.google.com/scholar?as_q=The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner&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 MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Martel&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mason G%2C Provero P%2C Vaira AM%2C Accotto GP %282002%29 Estimating the number of integrations in transformed plants by quantitative real%2Dtime PCR%2E BMC Biotechnol 2%3A 20%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mason G, Provero P, Vaira AM, Accotto GP (2002) Estimating the number of integrations in transformed plants by quantitative real-time PCR. BMC Biotechnol 2: 20.

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

http://scholar.google.com/scholar?as_q=Estimating the number of integrations in transformed plants by quantitative real-time PCR&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=Estimating the number of integrations in transformed plants by quantitative real-time PCR&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mason&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Menu T%2C Rothan C%2C Dai N%2C Petreikov M%2C Etienne C%2C Destrac%2DIrvine A%2C Schaffer A%2C Granot D%2C Ricard B %282001%29 Cloning and characterization of a cDNA encoding hexokinase from tomato%2E Plant Sci 160%3A 209%2D218%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Menu T, Rothan C, Dai N, Petreikov M, Etienne C, Destrac-Irvine A, Schaffer A, Granot D, Ricard B (2001) Cloning and characterization of a cDNA encoding hexokinase from tomato. Plant Sci 160: 209-218.

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

http://scholar.google.com/scholar?as_q=Cloning and characterization of a cDNA encoding hexokinase from 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=Cloning and characterization of a cDNA encoding hexokinase from tomato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Menu&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Miron D%2C Schaffer AA %281991%29 Sucrose phosphate synthase%2C sucrose synthase%2C and invertase activities in developing fruit of Lycopersicon esculentum Mill%2E and the sucrose accumulating Lycopersicon hirsutum Humb%2E and Bonpl%2E Plant physiol 95%3A 623%2D627%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Miron D, Schaffer AA (1991) Sucrose phosphate synthase, sucrose synthase, and invertase activities in developing fruit of Lycopersicon esculentum Mill. and the sucrose accumulating Lycopersicon hirsutum Humb. and Bonpl. Plant physiol 95: 623-627.

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

http://scholar.google.com/scholar?as_q=Sucrose phosphate synthase, sucrose synthase, and invertase activities in developing fruit of Lycopersicon esculentum Mill&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 phosphate synthase, sucrose synthase, and invertase activities in developing fruit of Lycopersicon esculentum Mill&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Miron&as_ylo=1991&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Moore S%2C Payton P%2C Wright M%2C Tanksley S%2C Giovannoni J %282005%29 Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae%2E J Exp Bot 56%3A 2885%2D2895%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56: 2885-2895.

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

http://scholar.google.com/scholar?as_q=Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae&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=Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moore&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Murashige T%2C Skoog F %281962%29 A revised medium for rapid growth and bio assays with tobacco tissue cultures%2E Physiol Plant 15%3A 473%2D497%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497.

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

http://scholar.google.com/scholar?as_q=A revised medium for rapid growth and bio assays with tobacco tissue cultures&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 revised medium for rapid growth and bio assays with tobacco tissue cultures&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Murashige&as_ylo=1962&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Proels R%2C Roitsch T %282009%29 Extracellular invertase LIN6 of tomato%3A a pivotal enzyme for integration of metabolic%2C hormonal%2C and stress signals is regulated by a diurnal rhythm%2E J Exp Bot 60%3A 1555%2D1567%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Proels R, Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J Exp Bot 60: 1555-1567.

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

http://scholar.google.com/scholar?as_q=Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm&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=Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Proels&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Qin G%2C Wang Y%2C Cao B%2C Wang W%2C Tian S %282012%29 Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening%2E Plant J 70%3A 243%2D255%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J 70: 243-255.

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

http://scholar.google.com/scholar?as_q=Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening&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=Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Qin&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rausch T%2C Greiner S %282004%29 Plant protein inhibitors of invertases%2E Biochem Biophys Acta 1696%3A 253%2D261%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. Biochem Biophys Acta 1696: 253-261.

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

http://scholar.google.com/scholar?as_q=Plant protein inhibitors of invertases&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 protein inhibitors of invertases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rausch&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1


Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14 (suppl.): S185-S205.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles indevelopment, yield potential, and response to drought and heat. Mol Plant 3: 942-955.


Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis ofrecalcitrant plant tissues. Proteomics 4: 2522-2532.


Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant physiol121: 1-8.


Sumner JB (1921) Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine. J Biol Chem 47: 5-9.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Télef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P (2006) Sucrose deficiency delayslycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62: 453-469.


Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in thephloem. Proc Natl Acad Sci USA 99: 10876-10880.


Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box genenecessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296: 343-346.


Wang F, Smith AG, Brenner ML (1993) Isolation and sequencing of tomato fruit sucrose synthase cDNA. Plant Physiol 103: 1463-1464.


Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S (2014) Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biol 15: 548.


Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359-362.


Yu X, Wang X, Zhang W, Qian T, Tang G, Guo Y, Zheng C (2008) Antisense suppression of an acid invertase gene (MAI1) inmuskmelon alters plant growth and fruit development. J Exp Bot 59: 2969-2977.


Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013)Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. NatBiotechnol 31: 154-159.

Pubmed: Author and TitleCrossRef: Author and Title https://plantphysiol.orgDownloaded on May 3, 2021. - Published by


http://www.ncbi.nlm.nih.gov/pubmed?term=Rolland F%2C Moore B%2C Sheen J %282002%29 Sugar sensing and signaling in plants%2E Plant Cell 14 %28suppl%2E%29%3A S185%2DS205%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14 (suppl.): S185-S205.

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

http://scholar.google.com/scholar?as_q=Sugar sensing and signaling 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=Sugar sensing and signaling in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rolland&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ruan YL%2C Jin Y%2C Yang YJ%2C Li GJ%2C Boyer JS %282010%29 Sugar input%2C metabolism%2C and signaling mediated by invertase%3A roles in development%2C yield potential%2C and response to drought and heat%2E Mol Plant 3%3A 942%2D955%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3: 942-955.

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

http://scholar.google.com/scholar?as_q=Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat&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=Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ruan&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Saravanan RS%2C Rose JKC %282004%29 A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues%2E Proteomics 4%3A 2522%2D2532%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4: 2522-2532.

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

http://scholar.google.com/scholar?as_q=A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues&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 critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Saravanan&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schmittgen TD%2C Livak KJ %282008%29 Analyzing real%2Dtime PCR data by the comparative C%28T%29 method%2E Nat Protoc 3%3A 1101%2D1108%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.

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

http://scholar.google.com/scholar?as_q=Analyzing real-time PCR data by the comparative C(T) method&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=Analyzing real-time PCR data by the comparative C(T) method&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmittgen&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sturm A %281999%29 Invertases%2E Primary structures%2C functions%2C and roles in plant development and sucrose partitioning%2E Plant physiol 121%3A 1%2D8%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant physiol 121: 1-8.

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

http://scholar.google.com/scholar?as_q=Invertases&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=Invertases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sturm&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sumner JB %281921%29 Dinitrosalicylic acid%3A a reagent for the estimation of sugar in normal and diabetic urine%2E J Biol Chem 47%3A 5%2D9%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sumner JB (1921) Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine. J Biol Chem 47: 5-9.

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

http://scholar.google.com/scholar?as_q=Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine&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=Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sumner&as_ylo=1921&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=T�lef N%2C Stammitti%2DBert L%2C Mortain%2DBertrand A%2C Maucourt M%2C Carde JP%2C Rolin D%2C Gallusci P %282006%29 Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs%2E Plant Mol Biol 62%3A 453%2D469%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=T�lef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62: 453-469.

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

http://scholar.google.com/scholar?as_q=Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs&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 deficiency delays lycopene accumulation in tomato fruit pericarp discs&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=T�lef&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Vaughn MW%2C Harrington GN%2C Bush DR %282002%29 Sucrose%2Dmediated transcriptional regulation of sucrose symporter activity in the phloem%2E Proc Natl Acad Sci USA 99%3A 10876%2D10880%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci USA 99: 10876-10880.

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

http://scholar.google.com/scholar?as_q=Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem&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-mediated transcriptional regulation of sucrose symporter activity in the phloem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vaughn&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Vrebalov J%2C Ruezinsky D%2C Padmanabhan V%2C White R%2C Medrano D%2C Drake R%2C Schuch W%2C Giovannoni J %282002%29 A MADS%2Dbox gene necessary for fruit ripening at the tomato ripening%2Dinhibitor %28Rin%29 locus%2E Science 296%3A 343%2D346%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296: 343-346.

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

http://scholar.google.com/scholar?as_q=A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus&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 MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Vrebalov&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang F%2C Smith AG%2C Brenner ML %281993%29 Isolation and sequencing of tomato fruit sucrose synthase cDNA%2E Plant Physiol 103%3A 1463%2D1464%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang F, Smith AG, Brenner ML (1993) Isolation and sequencing of tomato fruit sucrose synthase cDNA. Plant Physiol 103: 1463-1464.

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

http://scholar.google.com/scholar?as_q=Isolation and sequencing of tomato fruit sucrose synthase cDNA&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 sequencing of tomato fruit sucrose synthase cDNA&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang Y%2C Wang W%2C Cai J%2C Zhang Y%2C Qin G%2C Tian S %282014%29 Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin%2Dconjugating enzymes in fruit ripening%2E Genome Biol 15%3A 548%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S (2014) Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biol 15: 548.

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

http://scholar.google.com/scholar?as_q=Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wisniewski JR%2C Zougman A%2C Nagaraj N%2C Mann M %282009%29 Universal sample preparation method for proteome analysis%2E Nat Methods 6%3A 359%2D362%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362.

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

http://scholar.google.com/scholar?as_q=Universal sample preparation method for proteome analysis&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=Universal sample preparation method for proteome analysis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wisniewski&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yu X%2C Wang X%2C Zhang W%2C Qian T%2C Tang G%2C Guo Y%2C Zheng C %282008%29 Antisense suppression of an acid invertase gene %28MAI1%29 in muskmelon alters plant growth and fruit development%2E J Exp Bot 59%3A 2969%2D2977%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu X, Wang X, Zhang W, Qian T, Tang G, Guo Y, Zheng C (2008) Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit development. J Exp Bot 59: 2969-2977.

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

http://scholar.google.com/scholar?as_q=Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit 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=Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhong S%2C Fei Z%2C Chen YR%2C Zheng Y%2C Huang M%2C Vrebalov J%2C McQuinn R%2C Gapper N%2C Liu B%2C Xiang J%2C Shao Y%2C Giovannoni JJ %282013%29 Single%2Dbase resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening%2E Nat Biotechnol 31%3A 154%2D159%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31: 154-159.


Google Scholar: Author Only Title Only Author and Title

Zhu Z, Liu RL, Li BQ, Tian SP (2013) Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruitin controlled atmosphere storage. Food Chem 141: 3323-3328.


Zhu Z, Zhang ZQ, Qin GZ, Tian SP (2010) Effects of brassinosteroids on postharvest disease and senescence of jujube fruit instorage. Postharvest Biol Tec 56: 50-55.



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

http://scholar.google.com/scholar?as_q=Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening&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=Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhong&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu Z%2C Liu RL%2C Li BQ%2C Tian SP %282013%29 Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage%2E Food Chem 141%3A 3323%2D3328%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu Z, Liu RL, Li BQ, Tian SP (2013) Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage. Food Chem 141: 3323-3328.

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

http://scholar.google.com/scholar?as_q=Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage&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=Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu Z%2C Zhang ZQ%2C Qin GZ%2C Tian SP %282010%29 Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage%2E Postharvest Biol Tec 56%3A 50%2D55%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu Z, Zhang ZQ, Qin GZ, Tian SP (2010) Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage. Postharvest Biol Tec 56: 50-55.

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

http://scholar.google.com/scholar?as_q=Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage&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=Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1


a tomato vacuolar invertase inhibitor mediates sucrose ......2016/09/30 · a tomato vacuolar...

Documents