Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development

Springer Science and Business Media LLC - Tập 8 Số 1 - 2007
Laurent Deluc1, Jérôme Grimplet1, Matthew D. Wheatley1, Richard Tillett1, David R. Quilici1, Craig Osborne2, David A. Schooley1, Karen Schlauch3, John C. Cushman1, Grant R. Cramer1
1Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA
2Department of Animal Biotechnology, University of Nevada, Reno, USA
3Boston University School of Medicine, Department of Genetics and Genomics, Boston University, E632, Boston, USA

Tóm tắt

AbstractBackgroundGrape berry development is a dynamic process that involves a complex series of molecular genetic and biochemical changes divided into three major phases. During initial berry growth (Phase I), berry size increases along a sigmoidal growth curve due to cell division and subsequent cell expansion, and organic acids (mainly malate and tartrate), tannins, and hydroxycinnamates accumulate to peak levels. The second major phase (Phase II) is defined as a lag phase in which cell expansion ceases and sugars begin to accumulate. Véraison (the onset of ripening) marks the beginning of the third major phase (Phase III) in which berries undergo a second period of sigmoidal growth due to additional mesocarp cell expansion, accumulation of anthocyanin pigments for berry color, accumulation of volatile compounds for aroma, softening, peak accumulation of sugars (mainly glucose and fructose), and a decline in organic acid accumulation. In order to understand the transcriptional network responsible for controlling berry development, mRNA expression profiling was conducted on berries ofV. viniferaCabernet Sauvignon using the Affymetrix GeneChip®Vitisoligonucleotide microarray ver. 1.0 spanning seven stages of berry development from small pea size berries (E-L stages 31 to 33 as defined by the modified E-L system), through véraison (E-L stages 34 and 35), to mature berries (E-L stages 36 and 38). Selected metabolites were profiled in parallel with mRNA expression profiling to understand the effect of transcriptional regulatory processes on specific metabolite production that ultimately influence the organoleptic properties of wine.ResultsOver the course of berry development whole fruit tissues were found to express an average of 74.5% of probes represented on theVitismicroarray, which has 14,470 Unigenes. Approximately 60% of the expressed transcripts were differentially expressed between at least two out of the seven stages of berry development (28% of transcripts, 4,151 Unigenes, had pronounced (≥2 fold) differences in mRNA expression) illustrating the dynamic nature of the developmental process. The subset of 4,151 Unigenes was split into twenty well-correlated expression profiles. Expression profile patterns included those with declining or increasing mRNA expression over the course of berry development as well as transient peak or trough patterns across various developmental stages as defined by the modified E-L system. These detailed surveys revealed the expression patterns for genes that play key functional roles in phytohormone biosynthesis and response, calcium sequestration, transport and signaling, cell wall metabolism mediating expansion, ripening, and softening, flavonoid metabolism and transport, organic and amino acid metabolism, hexose sugar and triose phosphate metabolism and transport, starch metabolism, photosynthesis, circadian cycles and pathogen resistance. In particular, mRNA expression patterns of transcription factors, abscisic acid (ABA) biosynthesis, and calcium signaling genes identified candidate factors likely to participate in the progression of key developmental events such as véraison and potential candidate genes associated with such processes as auxin partitioning within berry cells, aroma compound production, and pathway regulation and sequestration of flavonoid compounds. Finally, analysis of sugar metabolism gene expression patterns indicated the existence of an alternative pathway for glucose and triose phosphate production that is invoked from véraison to mature berries.ConclusionThese results reveal the first high-resolution picture of the transcriptome dynamics that occur during seven stages of grape berry development. This work also establishes an extensive catalog of gene expression patterns for future investigations aimed at the dissection of the transcriptional regulatory hierarchies that govern berry development in a widely grown cultivar of wine grape. More importantly, this analysis identified a set of previously unknown genes potentially involved in critical steps associated with fruit development that can now be subjected to functional testing.

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Tài liệu tham khảo

FAOSTAT database (http://faostat.fao.org). 2007, Food and Agriculture Organization of the United Nations

Wine Institute. [http://www.wineinstitute.org/]

[http://www.wineinstitute.org/industry/statistics/2006/ca_wine_economic_impact.php]

German JB, Walzem RL: The health benefits of wine. Annu Rev Nutr. 2000, 20: 561-593. 10.1146/annurev.nutr.20.1.561.

Wollin SD, Jones PJ: Alcohol, red wine and cardiovascular disease. J Nutr. 2001, 131: 1401-1404.

Bradamante S, Barenghi L, Villa A: Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev. 2004, 22: 169-188.

Bruno R, Ghisolfi L, Priulla M, Nicolin A, Bertelli A: Wine and tumors: study of resveratrol. Drugs Exp Clin Res. 2003, 29: 257-261.

Baur JA, Sinclair DA: Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006, 5: 493-506. 10.1038/nrd2060.

Dore S: Unique properties of polyphenol stilbenes in the brain: more than direct antioxidant actions; gene/protein regulatory activity. Neurosignals. 2005, 14: 61-70.

Jones SB, DePrimo SE, Whitfield ML, Brooks JD: Resveratrol-induced gene expression profiles in human prostate cancer cells. Cancer Epidemiol Biomarkers Prev. 2005, 14: 596-604. 10.1158/1055-9965.EPI-04-0398.

Giovannoni JJ: Genetic regulation of fruit development and ripening. Plant Cell. 2004, 16 Suppl: S170-80. 10.1105/tpc.019158.

Given NK, Venis MA, Gierson D: Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta. 1988, 174: 402-406. 10.1007/BF00959527.

Coombe BG: Research on development and ripening of the grape berry. Am J Enol Vitic. 1992, 43: 101-110.

Coombe BG: Adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res. 1995, 1: 100-110.

Noordeloos S, Nagel CW: Effect of sugar on acid perception in wine. Am J Enol Vitic. 1972, 23: 139-143.

Davies C, Robinson SP: Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Physiol. 2000, 122: 803-812. 10.1104/pp.122.3.803.

Waters DL, Holton TA, Ablett EM, Lee LS, Henry RJ: cDNA microarray analysis of developing grape (Vitis vinifera cv. Shiraz) berry skin. Funct Integr Genomics. 2005, 5: 40-58. 10.1007/s10142-004-0124-z.

Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Leon C, Renaudin JP, Dedaldechamp F, Romieu C, Delrot S, Hamdi S: Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta. 2005, 222: 832-847. 10.1007/s00425-005-0017-y.

Fernandez L, Torregrosa L, Terrier N, Sreekantan L, Grimplet J, Davies C, Thomas MR, Romieu C, Ageorges A: Identification of genes associated with flesh morphogenesis during grapevine fruit development. Plant Mol Biol. 2007, 63: 307-323. 10.1007/s11103-006-9090-2.

Waters DLE, Holton TA, Ablett EM, Slade Lee L, Henry RJ: The ripening wine grape berry skin transcriptome. Plant Sci. 2006, 171: 132-138. 10.1016/j.plantsci.2006.03.002.

Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003, 4: 249-264. 10.1093/biostatistics/4.2.249.

Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Stat Method). 1995, 57: 289-300.

DFCI Grape Gene Index. [http://biocomp.dfci.harvard.edu/tgi/cgi-bin/tgi/gimain.pl?gudb=grape]

Pavlidis P, Noble WS: Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol. 2001, 2: research0042.1–research0042.15-10.1186/gb-2001-2-10-research0042.

Schoof H, Ernst R, Nazarov V, Pfeifer L, Mewes HW, Mayer KF: MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource for plant genomics. Nucleic Acids Res. 2004, 32 (Database issue): D373-6. 10.1093/nar/gkh068.

Altman A, Kaur-Sawhney R, Galston AW: Stabilization of oat leaf protoplasts through polyamine-mediated inhibition of senescence. Plant Physiol. 1977, 60: 570-574.

Egea-Cortines M, Mizrahi Y: Polyamines in cell division, fruit set and development and seed germination. Biochemistry and physiology of polyamines in plants. Edited by: Slocum RD, Flores HE. 1991, Boca Raton , CRC Press, 143-159.

Geny L, Broquedis M, Martin TJ, Bouard J: Free, conjugated, and wall-bound polyamines in various organs of fruiting cuttings of Vitis vinifera L. cv. Cabernet Sauvignon. Am J Enol Vitic. 1997, 48: 80-84.

Burtin D, Martin-Tanguy J, Paynot M, Rossin N: Effects of the suicide inhibitors of arginine and ornithine decarboxylase activities on organogenesis, growth, free polyamine and hydroxycinnamoyl putrescine levels in leaf explants of Nicotiana xanthi n.c. cultivated in vitro in a medium producing callus formation. Plant Physiol. 1989, 89: 104-110.

Sieciechowicz KA, Joy KW, Ireland RJ: The metabolism of asparagine in plants. Phytochemistry. 1988, 27: 663-671. 10.1016/0031-9422(88)84071-8.

Miflin BJ, Habash DZ: The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot. 2002, 53: 979-987. 10.1093/jexbot/53.370.979.

Nunan KJ, Sims IM, Bacic A, Robinson SP, Fincher GB: Changes in cell wall composition during ripening of grape berries. Plant Physiol. 1998, 118: 783-792. 10.1104/pp.118.3.783.

Thomas TR, Matthews MA, Shackel KA: Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant Cell Environ. 2006, 29: 993-1001. 10.1111/j.1365-3040.2006.01496.x.

Brummell DA, Harpster MH: Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol. 2001, 47: 311-340. 10.1023/A:1010656104304.

Saladie M, Rose JK, Cosgrove DJ, Catala C: Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J. 2006, 47: 282-295. 10.1111/j.1365-313X.2006.02784.x.

Sampedro J, Cosgrove DJ: The expansin superfamily. Genome Biol. 2005, 6: 242-10.1186/gb-2005-6-12-242.

Dotto MC, Martinez GA, Civello PM: Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Physiol Biochem. 2006, 44: 301-307. 10.1016/j.plaphy.2006.06.008.

Lund ST, Bohlmann J: The molecular basis for wine grape quality--a volatile subject. Science. 2006, 311: 804-805. 10.1126/science.1118962.

Lucker J, Bowen P, Bohlman J: Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+)-valencene synthase and (-)-germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Phytochemistry. 2004, 65: 2649-2659. 10.1016/j.phytochem.2004.08.017.

Martin DM, Bohlman J: Identification of Vitis vinifera (-)-alpha-terpineol synthase by in silico screening of full-length cDNA ESTs and functional characterization of recombinant terpene synthase. Phytochemistry. 2004, 65: 1223-1229. 10.1016/j.phytochem.2004.03.018.

Mahmoud SS, Croteau RB: Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci. 2002, 7: 366-373. 10.1016/S1360-1385(02)02303-8.

Jackson RS: Wine Science: Principles, Practice, Perception. Food Science and Technology International Series. Edited by: Taylor SL. 2000, San Diego , Academic Press, 2nd

Farina L, Boido E, Carrau F, Versini G, Dellacassa E: Terpene compounds as possible precursors of 1,8-cineole in red grapes and wines. J Agric Food Chem. 2005, 53: 1633-1636. 10.1021/jf040332d.

Ringer KL, Davis EM, Croteau R: Monoterpene metabolism. Cloning, expression, and characterization of (-)-isopiperitenol/(-)-carveol dehydrogenase of peppermint and spearmint. Plant Physiol. 2005, 137: 863-872. 10.1104/pp.104.053298.

Davies C, Boss PK, Robinson SP: Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol. 1997, 115: 1155-1161.

Chervin C, Tira-Umphon A, Roustan JP, Lamon J, El-Kereamy A, Kanellis A: Ethylene is required for the ripening of grape. Acta Hort. 2005, 689: 251-256.

El-Kereamy A, Chervin C, Roustan JP, Cheynier V, Souquet JM, Moutounet M, Raynal J, Ford C, Latche A, Pech JC, Bouzayen M: Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiol Plant. 2003, 119: 175-182. 10.1034/j.1399-3054.2003.00165.x.

Tesniere C, Pradal M, El-Kereamy A, Torregrosa L, Chatelet P, Roustan JP, Chervin C: Involvement of ethylene signalling in a non-climacteric fruit: new elements regarding the regulation of ADH expression in grapevine. J Exp Bot. 2004, 55: 2235-2240. 10.1093/jxb/erh244.

Hale CR, Coombe BG, Hawker JS: Effects of ethylene and 2-chloroethylphosphonic acid on the ripening of grapes. Plant Physiol. 1970, 45: 620-623.

Chen YF, Etheridge N, Schaller GE: Ethylene signal transduction. Ann Bot (Lond). 2005, 95: 901-915. 10.1093/aob/mci100.

Klee H, Tieman D: The tomato ethylene receptor gene family: Form and function. Physiol Plant. 2002, 115: 336-341. 10.1034/j.1399-3054.2002.1150302.x.

Trainotti L, Pavanello A, Casadoro G: Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits?. J Exp Bot. 2005, 56: 2037-2046. 10.1093/jxb/eri202.

Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR: Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol. 2006, 140: 150-158. 10.1104/pp.105.070706.

Belkhadir Y, Chory J: Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science. 2006, 314: 1410-1411. 10.1126/science.1134040.

Cawthon D, Morris J: Relationship of seed number and maturity to berry development, fruit maturation, hormonal changes and uneven ripening of "Concord" (Vitis labrusca L.) grapes. J Am Soc Hort Sci. 1982, 107: 1097-1104.

Perez FJ, Viani C, Retamales J: Bioactive gibberellins in seeded and seedless grapes: Identification and changes in content during berry development. Am J Enol Vitic. 2000, 51: 315-318.

Costantini E, Landi L, Silvestroni O, Pandolfini T, Spena A, Mezzetti B: Auxin synthesis-encoding transgene enhances grape fecundity. Plant Physiol. 2007, 143: 1689-1694. 10.1104/pp.106.095232.

Bartel B, Fink GR: ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science. 1995, 268: 1745-1748. 10.1126/science.7792599.

Hampel D, Mosandl A, Wust M: Induction of de novo volatile terpene biosynthesis via cytosolic and plastidial pathways by methyl jasmonate in foliage of Vitis vinifera L. J Agric Food Chem. 2005, 53: 2652-2657. 10.1021/jf040421q.

Tassoni A, Fornale S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N: Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol. 2005, 166: 895-905. 10.1111/j.1469-8137.2005.01383.x.

Schaller F, Biesgen C, Mussig C, Altmann T, Weiler EW: 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta. 2000, 210: 979-984. 10.1007/s004250050706.

Werner T, Kollmer I, Bartrina I, Holst K, Schmulling T: New insights into the biology of cytokinin degradation. Plant Biol (Stuttg). 2006, 8: 371-381. 10.1055/s-2006-923928.

Hepler PK: Calcium: a central regulator of plant growth and development. Plant Cell. 2005, 17: 2142-2155. 10.1105/tpc.105.032508.

Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP: Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol. 2006, 140: 558-579. 10.1104/pp.105.074971.

Cerana M, Bonza MC, Harris R, Sanders D, De Michelis MI: Abscisic acid stimulates the expression of two isoforms of plasma membrane Ca2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol (Stuttg). 2006, 8: 572-578. 10.1055/s-2006-924111.

Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD: Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol. 2005, 138: 2048-2060. 10.1104/pp.105.061218.

Coombe BG, Hale CR: The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiol. 1973, 51: 629-634.

McCormack E, Tsai YC, Braam J: Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci. 2005, 10: 383-389. 10.1016/j.tplants.2005.07.001.

Anandalakshmi R, Marathe R, Ge X, Herr JM, Mau C, Mallory A, Pruss G, Bowman L, Vance VB: A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science. 2000, 290: 142-144. 10.1126/science.290.5489.142.

Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H: AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci U S A. 2000, 97: 11650-11654. 10.1073/pnas.200217597.

Grimplet J, Deluc LG, Tillett RL, Wheatley MD, Schlauch KA, Cramer GR, Cushman JC: Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics. 2007, 8: 187-10.1186/1471-2164-8-187.

Kitamura S, Shikazono N, Tanaka A: TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J. 2004, 37: 104-114. 10.1046/j.1365-313X.2003.01943.x.

Goodman CD, Casati P, Walbot V: A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell. 2004, 16: 1812-1826. 10.1105/tpc.022574.

Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V: Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell. 1998, 10: 1135-1149. 10.1105/tpc.10.7.1135.

Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M: The transparent testa12 gene of arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell. 2001, 13: 853-872. 10.1105/tpc.13.4.853.

Walker AR, Lee E, Bogs J, McDavid DA, Thomas MR, Robinson SP: White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J. 2007, 49: 772-785. 10.1111/j.1365-313X.2006.02997.x.

Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP: The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol. 2007, 143 (3): 1347-1361. 10.1104/pp.106.093203.

Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Merillon JM, Hamdi S: Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol. 2006, 140: 499-511. 10.1104/pp.105.067231.

Kobayashi S, Ishimaru M, Hiraoka K, Honda C: Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta. 2002, 215: 924-933. 10.1007/s00425-002-0830-5.

Kobayashi S, Goto-Yamamoto N, Hirochika H: Retrotransposon-induced mutations in grape skin color. Science. 2004, 304 (5673): 982-10.1126/science.1095011.

Goodrich J, Carpenter R, Coen ES: A common gene regulates pigmentation pattern in diverse plant species. Cell. 1992, 68: 955-964. 10.1016/0092-8674(92)90038-E.

Luan F, Wüst M: Differential incorporation of 1-deoxy-D-xylulose into (3S)-linalool and geraniol in grape berry exocarp and mesocarp. Phytochemistry. 2002, 60: 451-459. 10.1016/S0031-9422(02)00147-4.

Wu S, Watanabe N, Mita S, Dohra H, Ueda Y, Shibuya M, Ebizuka Y: The key role of phloroglucinol O-methyltransferase in the biosynthesis of Rosa chinensis volatile 1,3,5-trimethoxybenzene. Plant Physiol. 2004, 135: 95-102. 10.1104/pp.103.037051.

Ross JR, Nam KH, D'Auria JC, Pichersky E: S-Adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys. 1999, 367: 9-16. 10.1006/abbi.1999.1255.

Pichersky E, Noel JP, Dudareva N: Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science. 2006, 311: 808-811. 10.1126/science.1118510.

DeBolt S, Cook DR, Ford CM: L-tartaric acid synthesis from vitamin C in higher plants. Proc Natl Acad Sci U S A. 2006, 103: 5608-5613. 10.1073/pnas.0510864103.

Possner DRE, Kliewer WM: The localization of acids, sugars, potassium and calcium in developing grape berries. Vitis. 1985, 24: 229-240.

Stines AP, Naylor DJ, Hoj PB, Van Heeswijck R: Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of Delta1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiol. 1999, 120: 923-931. 10.1104/pp.120.3.923.

Stines AP, Grubb J, Gockowiak H, Henschke PA, Hoj PB, Heeswijck RV: Proline and arginine accumulation in developing berries of V. vinifera in Australian vineyards: Influence of vine cultivar, berry maturity and tissue type. Aust J Grape Wine Res. 2000, 6: 150-158.

Conde C, Silva P, Fontes N, Dias A, Tavares R, Sousa M, Agasse A, Delrot S, Geros H: Biochemical changes throughout grape berry development and fruit and wine quality. Food. 2007, 1: 1-22.

Swanson CA, El-Shishiny ED: Translocation of sugars in the Concord grape. Plant Physiol. 1958, 33: 33-37.

Conde C, Agasse A, Glissant D, Tavares R, Geros H, Delrot S: Pathways of glucose regulation of monosaccharide transport in grape cells. Plant Physiol. 2006, 141: 1563-1577. 10.1104/pp.106.080804.

Komatsu A, Moriguchi T, Koyama K, Omura M, Akihama T: Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J Exp Bot. 2002, 53: 61-71. 10.1093/jexbot/53.366.61.

Davies C, Robinson SP: Sugar accumulation in grape berries: cloning for two putative vacuolar invertase cDNAs and their expression in grapevine tissue. Plant Physiol. 1996, 111: 275-283. 10.1104/pp.111.1.275.

Zhang XY, Wang XL, Wang XF, Xia GH, Pan QH, Fan RC, Wu FQ, Yu XC, Zhang DP: A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol. 2006, 142: 220-232. 10.1104/pp.106.081430.

Geigenberger P, Stitt M: Sucrose synthase catalyses a readily reversible reaction in vivo developing potato tubers and other plant tissues. Planta. 1993, 189: 329-393. 10.1007/BF00194429.

Koch KE: Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol. 1996, 47: 509-540. 10.1146/annurev.arplant.47.1.509.

Ruan Y: Rapid cell expansion and cellulose synthesis regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre. Funct Plant Biol. 2007, 34: 1-10. 10.1071/FP06234.

Vignault C, Vachaud M, Cakir B, Glissant D, Dedaldechamp F, Buttner M, Atanassova R, Fleurat-Lessard P, Lemoine R, Delrot S: VvHT1 encodes a monosaccharide transporter expressed in the conducting complex of the grape berry phloem. J Exp Bot. 2005, 56: 1409-1418. 10.1093/jxb/eri142.

Davies C, Wolf T, Robinson SP: Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Sci. 1999, 147: 93-100. 10.1016/S0168-9452(99)00059-X.

Klepek YS, Geiger D, Stadler R, Klebl F, Landouar-Arsivaud L, Lemoine R, Hedrich R, Sauer N: Arabidopsis POLYOL TRANSPORTER5, a new member of the monosaccharide transporter-like superfamily, mediates H+-symport of numerous substrates, including myo-inositol, glycerol, and ribose. Plant Cell. 2005, 17: 204-218. 10.1105/tpc.104.026641.

Kore-eda S, Noake C, Ohishi M, Ohnishi J, Cushman JC: Transcriptional profiles of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum. Funct Plant Biol. 2005, 32: 451-466. 10.1071/FP04188.

Gao Z, Maurousset L, Lemoine R, Yoo SD, van Nocker S, Loescher W: Cloning, expression, and characterization of sorbitol transporters from developing sour cherry fruit and leaf sink tissues. Plant Physiol. 2003, 131: 1566-1575. 10.1104/pp.102.016725.

Roubelakis-Angelakis KA, Kliewer WM: The composition of bleeding sap from Thompson Seedless grapevines as affected by nitrogen fertilization. Am J Enol Vitic. 1979, 30: 14-18.

Delvalle D, Dumez S, Wattebled F, Roldan I, Planchot V, Berbezy P, Colonna P, Vyas D, Chatterjee M, Ball S, Merida A, D'Hulst C: Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J. 2005, 43: 398-412. 10.1111/j.1365-313X.2005.02462.x.

Li CY, Weiss D, Goldschmidt EE: Effects of carbohydrate starvation on gene expression in citrus root. Planta. 2003, 217: 11-20.

Diakou P, Carde JP: In situ fixation of grape berries. Protoplasma. 2001, 218: 225-235. 10.1007/BF01306611.

Hotta CT, Gardner MJ, Hubbard KE, Baek SJ, Dalchau N, Suhita D, Dodd AN, Webb AA: Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ. 2007, 30 (3): 333-349. 10.1111/j.1365-3040.2006.01627.x.

Lu Y, Gehan JP, Sharkey TD: Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol. 2005, 138 (4): 2280-2291. 10.1104/pp.105.061903.

Pocock KF, Sefton MA, Williams PJ: Taste thresholds of phenolic extracts of French and American oakwood: the influence of oak phenols on wine flavor. Am J Enol Vitic. 1994, 45 (4): 429-434.

Robinson SP, Jacobs AK, Dry IB: A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol. 1997, 114 (3): 771-778. 10.1104/pp.114.3.771.

Jach G, Gornhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C: Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J. 1995, 8 (1): 97-109. 10.1046/j.1365-313X.1995.08010097.x.

Tattersall DB, Van Heeswijck R, Hoj PB: Identification and characterization of a fruit-specific, thaumatin-like protein that accumulates at very high levels in conjunction with the onset of sugar accumulation and berry softening in grapes. Plant Physiol. 1997, 114 (3): 759-769. 10.1104/pp.114.3.759.

Busam G, Junghanns KT, Kneusel RE, Kassemeyer HH, Matern U: Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L. Plant Physiol. 1997, 115 (3): 1039-1048. 10.1104/pp.115.3.1039.

McCutchan J, Shackel KA: Stem-water potential as a sensitive indicator of water stress in prune trees (Prunus domestica L. cv. French). J Amer Soc Hort Sci. 1992, 117: 607-611.

Tattersall EAR, Ergul A, AlKayal F, DeLuc L, Cushman JC, Cramer GR: Comparison of methods for isolating high-quality RNA from leaves of grapevine. Am J Enol Vitic. 2005, 56: 400-406.

Gautier L, Cope L, Bolstad BM, Irizarry RA: affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004, 20: 307-315. 10.1093/bioinformatics/btg405.

Didier G, Brezellec P, Remy E, Henaut A: GeneANOVA--gene expression analysis of variance. Bioinformatics. 2002, 18: 490-491. 10.1093/bioinformatics/18.3.490.

Shen L, Gong J, Caldo RA, Nettleton D, Cook D, Wise RP, Dickerson JA: BarleyBase--an expression profiling database for plant genomics. Nucleic Acids Res. 2005, 33 (Database Issue): D614-D618. 10.1093/nar/gki123.

Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J: TM4: a free, open-source system for microarray data management and analysis. BioTechniques. 2003, 34: 374-378.

Chernoff H, Lehman EL: The use of maximum likelihood estimates in chi2 tests for goodness-of-fit. Ann Math Stat. 1954, 25: 579-586. 10.1214/aoms/1177728726.

Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.

Luu-The V, Paquet N, Calvo E, Cumps J: Improved real-time RT-PCR method for high-throughput measurements using second derivative calculation and double correction. BioTechniques. 2005, 38: 287-293.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3: RESEARCH0034-10.1186/gb-2002-3-7-research0034.

Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW: Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot. 2005, 56: 323-336. 10.1093/jxb/eri058.

NIST Standard Reference Database. National Institute of Standards and Technology, [http://www.nist.gov/srd/]

Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D: [email protected]: the Golm Metabolome Database. Bioinformatics. 2005, 21: 1635-1638. 10.1093/bioinformatics/bti236.

Dubois M, Gilles K, Hamilton J, Rebers P, Smith F: Colorimetric method for the determination of sugars and related substances. Anal Chem. 1956, 28: 350-356. 10.1021/ac60111a017.

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