Search for Transcriptional and Metabolic Markers of Grape Pre-Ripening and Ripening and Insights into Specific Aroma Development in Three Portuguese Cultivars

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Agudelo Romero, Patricia ^a   Erban, Alexander ^b   Sousa, Lisete ^a   Pais, Maria Salomé ^a   Kopka, Joachim ^b   Fortes, Ana Margarida ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID METABOLISM; AROMA; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; CULTIVAR; CULTIVAR IDENTIFICATION; DEVELOPMENTAL STAGE; DOWN REGULATION; FRUIT RIPENING; GAS CHROMATOGRAPHY; GENE CLUSTER; GENE EXPRESSION; LIPID METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; TIME OF FLIGHT MASS SPECTROMETRY; UPREGULATION; VARIETAS; VITIS;

FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; ODORS; VITIS;

VITACEAE; VITIS;

EID: 84875670721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060422     Document Type: Article

References (93)

1. Yadav M, Jain S, Bhardwaj A, Nagpal R, Puniya M, et al. (2009) Biological and medicinal properties of grapes and their bioactive constituents: an update. J Med Food 12: 473-484.
2. Ali K, Maltese F, Choi YH, Verpoorte R, (2010) Metabolic constituents of grapevine and grape-derived products. Phytochem Rev 9: 357-378.
3. Coombe B, McCarthy M, (2000) Dynamics of grape berry growth and physiology of ripening. Australian Journal of Grape and Wine Research 6: 131-135.
4. Coombe B, (1995) Growth Stages of the Grapevine: Adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1: 104-110.
5. Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, et al. (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222: 832-847.
6. Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, et al. (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8: 429.
7. Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, et al. (2007) Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison. BMC Genomics 8: 428.
8. Negri AS, Prinsi B, Rossoni M, Failla O, Scienza A, et al. (2008) Proteome changes in the skin of the grape cultivar Barbera among different stages of ripening. BMC Genomics 9: 378.
9. Zamboni A, Di Carli M, Guzzo F, Stocchero M, Zenoni S, et al. (2010) Identification of Putative Stage-Specific Grapevine Berry Biomarkers and Omics Data Integration into Networks. Plant Physiology: 1439-1459.
10. Martínez-Esteso MJ, Sellés-Marchart S, Lijavetzky D, Pedreño MA, Bru-Martínez R, (2011) A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism. J Exp Bot 62: 2521-2569.
11. Fortes AM, Agudelo-Romero P, Silva MS, Ali K, Sousa L, et al. (2011) Transcript and metabolite analysis in Trincadeira cultivar reveals novel information regarding the dynamics of grape ripening. BMC Plant Biol 11: 149.
12. Ali MB, Howard S, Chen S, Wang Y, Yu O, et al. (2011) Berry skin development in Norton grape: distinct patterns of transcriptional regulation and flavonoid biosynthesis. BMC Plant Biol 11: 7.
13. Ali K, Maltese F, Fortes A, Pais M, Choi Y, et al. (2011) Monitoring biochemical changes during grape berry development in Portuguese cultivars by NMR spectroscopy. Food Chemistry: 1760-1769.
14. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289-300.
15. Vignault C, Vachaud M, Cakir B, Glissant D, Dédaldéchamp F, et al. (2005) VvHT1 encodes a monosaccharide transporter expressed in the conducting complex of the grape berry phloem. J Exp Bot 56: 1409-1418.
16. Zhang XY, Wang XL, Wang XF, Xia GH, Pan QH, et al. (2006) A shift of Phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142: 220-232.
17. Dai ZW, Léon C, Feil R, Lunn JE, Delrot S, et al. (2013) Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit. J Exp Bot.
18. Davies C, Wolf T, Robinson S (1999) Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Science: 93-100.
19. Takashima Y, Senoura T, Yoshizaki T, Hamada S, Ito H, et al. (2007) Differential chain-length specificities of two isoamylase-type starch-debranching enzymes from developing seeds of kidney bean. Biosci Biotechnol Biochem 71: 2308-2312.
20. Janssen B, Thodey K, Schaffer R, Alba R, Balakrishnan L, et al. (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. Bmc Plant Biology:-.
21. Conde C, Delrot S, Geros H, (2008) Physiological, biochemical and molecular changes occurring during olive development and ripening. Journal of Plant Physiology pp. 1545-1562.
22. Grant T, Dami I, Ji T, Scurlock D, Streeter J, (2009) Variation in leaf and bud soluble sugar concentration among Vitis genotypes grown under two temperature regimes. Canadian Journal of Plant Science 89: 961-968.
23. Sweetman C, Deluc LG, Cramer GR, Ford CM, Soole KL, (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70: 1329-1344.
24. Livio T, Tadiello A, Casadoro G (2007) Variations of the peach fruit transcriptome during ripening and in response to hormone treatments. Caryologia: 156-159.
25. Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, et al. (2002) The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J 30: 329-336.
26. Wills R, Wimalasiri P, Greenfield H, (1984) Dehydroascorbic acid levels in fresh fruit and vegetables in relation to total vitamin-C activity. Journal of Agricultural and Food Chemistry pp. 836-838.
27. Okuda T, Yokotsuka K, (1999) Levels of glutathione and activities of related enzymes during ripening of koshu and Cabernet Sauvignon grapes and during winemaking. American Journal of Enology and Viticulture pp. 264-270.
28. Helsper J, Loewus F (1982) Metabolism of L-threonic acid in Rumex-x-acutus L and Pelargonium crispum (L) Lher. Plant Physiology: 1365-1368.
29. Millán C, Vargas A, Rubio A, Moreno J, Ortega J, (1992) Fatty acid content of unripe and ripe 'Pedro Ximénez' Vitis vinifera grapes. Journal of Wine Research3.
30. Grncarevic M, Radler F, (1971) A Review of the Surface Lipids of Grapes and Their Importance in the Drying Process. Am J Enol Vitic 22: 80-86.
31. Commenil P, Brunet L, Audran J, (1997) The development of the grape berry cuticle in relation to susceptibility to bunch rot disease. Journal of Experimental Botany pp. 1599-1607.
32. Zhang J, Wang X, Yu O, Tang J, Gu X, et al. (2011) Metabolic profiling of strawberry (Fragariaxananassa Duch.) during fruit development and maturation. Journal of Experimental Botany pp. 1103-1118.
33. Byfield G, Upchurch R (2007) Effect of temperature on delta-9 stearoyl-ACP and microsomal omega-6 desaturase gene expression and fatty acid content in developing soybean seeds. Crop Science: 1698-1704.
34. Liu Z, Yang X, Fu Y, (2009) SAD, a Stearoyl-Acyl Carrier Protein Desaturase Highly Expressed in High-Oil Maize Inbred Lines. Russian Journal of Plant Physiology pp. 709-715.
35. Whitaker B, Gapper N, (2008) Ripening-specific stigmasterol increase in tomato fruit is associated with increased sterol C-22 desaturase (CYP710A11) gene expression. Journal of Agricultural and Food Chemistry pp. 3828-3835.
36. Chow E, Jen J, (1978) Phytosterol biosynthesis in ripening tomatoes. Journal of Food Science pp. 1424-1426.
37. Symons G, Davies C, Shavrukov Y, Dry I, Reid J, et al. (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiology: 150-158.
38. Karlova R, Rosin F, Busscher-Lange J, Parapunova V, Do P, et al. (2011) Transcriptome and Metabolite Profiling Show That APETALA2a Is a Major Regulator of Tomato Fruit Ripening. Plant Cell: 923-941.
39. Lung SC, Weselake RJ, (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41: 1073-1088.
40. Bianchi G, Murelli C, Vlahov G (1992) Surface waxes from olive fruits. Phytochemistry: 3503-3506.
41. Saber M, Kashmiri M, Mohy-Ud-Din A, Ahmad M, Khanum R, (2010) Epicuticular Wax of Tamarix aphylla L. Journal of the Chemical Society of Pakistan pp. 662-667.
42. Arisz S, Testerink C, Munnik T (2009) Plant PA signaling via diacylglycerol kinase. Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids: 869-875.
43. Camara B, Brangeon J (1981) Carotenoid metabolism during chloroplast to chromoplast transformation in Capsicum annuum fruit. Planta: 359-364.
44. Jackson RS (2000) Wine science: principles and applications: Elsevier.
45. van Damme M, Zeilmaker T, Elberse J, Andel A, de Sain-van der Velden M, et al. (2009) Downy Mildew Resistance in Arabidopsis by Mutation of HOMOSERINE KINASE. Plant Cell: 2179-2189.
46. Agudelo-Romero P, Bortolloti C, Pais MS, Tiburcio A, Fortes AM (2013) Study of Polyamines during Grape Ripening Indicate an Important Role of Polyamine Catabolism. Plant Physiology and Biochemistry accepted.
47. Downey M, Harvey J, Robinson S, (2003) Synthesis of flavonols and expression of flavonol synthase genes in the developing grape berries of Shiraz and Chardonnay (Vitis vinifera L.). Australian Journal of Grape and Wine Research 9: 110-121.
48. Zheng HQ, Liu DY, (2003) [Anti-invasive and anti-metastatic effect of ampelopsin on melanoma]. Ai Zheng 22: 363-367.
49. Harbertson J, Kennedy J, Adams D, (2002) Tannin in skins and seeds of Cabernet Sauvignon, Syrah, and Pinot noir berries during ripening. American Journal of Enology and Viticulture pp. 54-59.
50. Katiyar SK, Afaq F, Perez A, Mukhtar H, (2001) Green tea polyphenol (-)-epigallocatechin-3-gallate treatment of human skin inhibits ultraviolet radiation-induced oxidative stress. Carcinogenesis 22: 287-294.
51. Toffali K, Zamboni A, Anesi A, Stocchero M, Pezzotti M, et al. (2011) Novel aspects of grape berry ripening and post-harvest withering revealed by untargeted LC-ESI-MS metabolomics analysis. pp.424-436.
52. Pereira D, Valentao P, Pereira J, Andrade P (2009) Phenolics: From Chemistry to Biology. Molecules: 2202-2211.
53. Ali K, Iqbal M, Korthout H, Maltese F, Fortes A, et al. (2012) NMR spectroscopy and chemometrics as a tool for anti-TNFα activity screening in crude extracts of grapes and other berries. Metabolomics.
54. Bogs J, Ebadi A, McDavid D, Robinson S (2006) Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiology: 279-291.
55. Croft K, (1998) The chemistry and biological effects of flavonoids and phenolic acids: towards prolongation of the healthy life span. Annals of the New York Academy of Sciences 854: 435-442.
56. Pichersky E, Noel J, Dudareva N, (2006) Biosynthesis of plant volatiles: Nature's diversity and ingenuity. Science pp. 808-811.
57. Oliveira C, Silva Ferreira AC, Mendes Pinto M, Hogg T, Alves F, et al. (2003) Carotenoid compounds in grapes and their relationship to plant water status. J Agric Food Chem 51: 5967-5971.
58. Vogel J, Tan B, McCarty D, Klee H, (2008) The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. Journal of Biological Chemistry pp. 11364-11373.
59. Gao H, Zhu H, Shao Y, Chen A, Lu C, et al. (2008) Lycopene accumulation affects the biosynthesis of some carotenoid-related volatiles independent of ethylene in tomato. J Integr Plant Biol 50: 991-996.
60. Lucker J, Bowen P, Bohlman J, (2004) 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 65: 2649-2659.
61. De Pinho PG, Falqué E, Castro M, Oliveira E, Silva H, Machado B, et al. (2007) Further insights into the floral character of Touriga Nacional wines. J Food Sci 72: S396-401.
62. Martin D, Aubourg S, Schouwey M, Daviet L, Schalk M, et al. (2010) Functional Annotation, Genome Organization and Phylogeny of the Grapevine (Vitis vinifera) Terpene Synthase Gene Family Based on Genome Assembly, FLcDNA Cloning, and Enzyme Assays. Bmc Plant Biology 10.
63. Kita M, Hirata Y, Moriguchi T, Endo-Inagaki T, Matsumoto R, et al. (2000) Molecular cloning and characterization of a novel gene encoding limonoid UDP-glucosyltransferase in Citrus. Febs Letters: 173-178.
64. Zamboni A, Minoia L, Ferrarini A, Tornielli G, Zago E, et al. (2008) Molecular analysis of post-harvest withering in grape by AFLP transcriptional profiling. Journal of Experimental Botany pp. 4145-4159.
65. Pripis-Nicolau L, de Revel G, Bertrand A, Maujean A, (2000) Formation of flavor components by the reaction of amino acid and carbonyl compounds in mild conditions. Journal of Agricultural and Food Chemistry pp. 3761-3766.
66. Kotseridis Y, Baumes R, (2000) Identification of impact odorants in Bordeaux red grape juice, in the commercial yeast used for its fermentation, and in the produced wine. Journal of Agricultural and Food Chemistry pp. 400-406.
67. D'Auria J, Chen F, Pichersky E (2002) Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiology: 466-476.
68. Vetter J, (2000) Plant cyanogenic glycosides. Toxicon 38: 11-36.
69. Aharoni A, O′Connell A, (2002) Microarray Gene Expression Analysis During Strawberry Achenes and Receptacle Maturation. Journal of Experimental Botany 53: 2073-2087.
70. Franks TK, Hayasaka Y, Choimes S, van Heeswijck R, (2005) Cyanogenic glucosides in grapevine: polymorphism, identification and developmental patterns. Phytochemistry 66: 165-173.
71. Creelman R, Mullet J (1997) Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology: 355-381.
72. Kalua C, Boss P, (2009) Evolution of Volatile Compounds during the Development of Cabernet Sauvignon Grapes (Vitis vinifera L.). Journal of Agricultural and Food Chemistry pp. 3818-3830.
73. Longhurst T, Tung H, Brady C, (1990) Developmental regulation of the expression of alcohol dehydrogenase in ripening tomato fruit. J Food Biochem 14: 421-433.
74. Franco M, Peinado R, Medina M, Moreno J, (2004) Off-vine grape drying effect on volatile compounds and aromatic series in must from Pedro Ximenez grape variety. Journal of Agricultural and Food Chemistry pp. 3905-3910.
75. Flamini R, (2005) Some advances in the knowledge of grape, wine and distillates chemistry as achieved by mass spectrometry. J Mass Spectrom 40: 705-713.
76. Ong P, Acree T, Lavin E, (1998) Characterization of volatiles in rambutan fruit (Nephelium lappaceum L.). Journal of Agricultural and Food Chemistry pp. 611-615.
77. Wang J, De Luca V, (2005) The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including 'foxy' methylanthranilate. Plant J 44: 606-619.
78. Effmert U, Saschenbrecker S, Ross J, Negre F, Fraser C, et al. (2005) Floral benzenoid carboxyl methyltransferases: From in vitro to in planta function. Phytochemistry: 1211-1230.
79. Havkin-Frenkel D, Podstolski A, Witkowska E, Molecki P, Mlkolajczyk M (1999) Vanillin biosynthetic pathways: an overview. In: T.J Fu, Singh G, Curtis WR, editors. Plant Cell and Tissue Culture for the Production of Food Ingredients. New York: Kluwer Academic Press/Plenum Publishers. pp. 35-43.
80. Jones M, Hughes J, Tregova A, Milne J, Tomsett A, et al. (2004) Biosynthesis of the flavour precursors of onion and garlic. Journal of Experimental Botany pp. 1903-1918.
81. Kobayashi H, Takase H, Suzuki Y, Tanzawa F, Takata R, et al. (2011) Environmental stress enhances biosynthesis of flavor precursors, S-3-(hexan-1-ol)-glutathione and S-3-(hexan-1-ol)-L-cysteine, in grapevine through glutathione S-transferase activation. J Exp Bot 62: 1325-1336.
82. Dubourdieu D, Torninaga T, Masneuf I, Des Gachons C, Murat M, (2006) The role of yeasts in grape flavor development during fermentation: The example of Sauvignon blanc. American Journal of Enology and Viticulture pp. 81-88.
83. Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics: 249-264.
84. Grimplet J, Cramer GR, Dickerson JA, Mathiason K, Van Hemert J, et al. (2009) VitisNet: "Omics" integration through grapevine molecular networks. PLoS One 4: e8365.
85. Wagner C, Sefkow M, Kopka J (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry: 887-900.
86. Erban A, Schauer N, Fernie AR, Kopka J, (2007) Nonsupervised construction and application of mass spectral and retention time index libraries from time-of-flight gas chromatography-mass spectrometry metabolite profiles. Methods Mol Biol 358: 19-38.
87. Strehmel N, Hummel J, Erban A, Strassburg K, Kopka J, (2008) Retention index thresholds for compound matching in GC-MS metabolite profiling. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences pp. 182-190.
88. Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography- mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics: 732-737.
89. Allwood J, Erban A, de Koning S, Dunn W, Luedemann A, et al. (2009) Inter-laboratory reproducibility of fast gas chromatography-electron impact-time of flight mass spectrometry (GC-EI-TOF/MS) based plant metabolomics. Metabolomics: 479-496.
90. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, et al. (2005) GMD@CSB.DB:the Golm Metabolome Database. Bioinformatics: 1635-1638.
91. Hummel J, Strehmel N, Selbig J, Walther D, Kopka J (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics: 322-333.
92. Lommen A, (2009) MetAlign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Anal Chem 81: 3079-3086.
93. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.