Regulation of flavonol content and composition in (Syrah×Pinot Noir) mature grapes: Integration of transcriptional profiling and metabolic quantitative trait locus analyses

Journal of Experimental Botany

Volumn 66, Issue 15, 2015, Pages 4441-4453

  Malacarne, Giulia ^a   Costantini, Laura ^a   Coller, Emanuela ^a   Battilana, Juri ^a   Velasco, Riccardo ^a   Vrhovsek, Urska ^a   Grando, Maria Stella ^a   Moser, Claudio ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

Berry; candidate gene; flavonols; metabolic profiling; microarray; quantitative trait loci; segregating population; Vitis vinifera

Indexed keywords

VITACEAE; VITIS VINIFERA;

FLAVONOL DERIVATIVE; PLANT PROTEIN;

DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PIGMENTATION; QUANTITATIVE TRAIT LOCUS; VITIS;

FLAVONOLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PIGMENTATION; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, DNA; VITIS;

EID: 84940116877     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv243     Document Type: Article

References (71)

1. Ali MB, Howard S, Chen S, Wang Y, Yu O, Kovacs LG, Qiu W. 2011. Berry skin development in Norton grape: distinct patterns of transcriptional regulation and flavonoid biosynthesis. BMC Plant Biology 11, 7.
2. Ashburner M, Ball CA, Blake JA, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25, 25-29.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B: Methodological 57, 289-300.
4. Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R. 2010. Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant, Cell and Environment 33, 1-10.
5. Boulton R. 2001. The copigmentation of anthocyanins and its role in the color of red wine: a critical review. American Journal of Enology and Viticulture 52, 67-87.
6. Buer CS, Muday GK. 2004. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. The Plant Cell 16, 1191-1205.
7. Buer CS, Sukumar P, Muday GK. 2006. Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiology 140, 1384-1396.
8. Carbonell-Bejerano P, Diago MP, Martinez-Abaigar J, Martinez-Zapater JM, Tardaguila J, Nunez-Olivera E. 2014. Solar ultraviolet radiation is necessary to enhance grapevine fruit ripening transcriptional and phenolic responses. BMC Plant Biology 14, 183.
9. Castillo-Munoz N, Gomez-Alonso S, Garcia-Romero E, Hermosin-Gutierrez I. 2007. Flavonol profiles of Vitis vinifera red grapes and their single-cultivar wines. Journal of Agricultural and Food Chemistry 55, 992-1002.
10. Castillo-Munoz N, Gomez-Alonso S, Garcia-Romero E, Hermosin-Gutierrez I. 2010. Flavonol profiles of Vitis vinifera white grape cultivars. Journal of Food Composition and Analysis 23, 699-705.
11. Chen XW, Hedley PE, Morris J, Liu H, Niks RE, Waugh R. 2011. Combining genetical genomics and bulked segregant analysis-based differential expression: an approach to gene localization. Theoretical and Applied Genetics 122, 1375-1383.
12. Chen XW, Niks RE, Hedley PE, Morris J, Druka A, Marcel TC, Vels A, Waugh R. 2010. Differential gene expression in nearly isogenic lines with QTL for partial resistance to Puccinia hordei in barley. BMC Genomics 11, 629.
13. Costantini L, Malacarne G, Lorenzi S, Troggio M, Mattivi F, Moser C, Grando MS. 2015. New candidate genes for the fine regulation of the colour of grapes. Journal of Experimental Botany 66, 4427-4440.
14. Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J. 2009. The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiology 151, 1513-1530.
15. Dal Santo S, Tornielli GB, Zenoni S, Fasoli M, Farina L, Anesi A, Guzzo F, Delledonne M, Pezzotti M. 2013. The plasticity of the grapevine berry transcriptome. Genome Biology 14, r54.
16. Dietrich K, Weltmeier F, Ehlert A, Weiste C, Stahl M, Harter K, Droge-Laser W. 2011. Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. The Plant Cell 23, 381-395.
17. Dixon DP, Skipsey M, Edwards R. 2010. Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71, 338-350.
18. Downey MO, Harvey JS, Robinson SP. 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.
19. Engelen K, Fu Q, Meysman P, Sanchez-Rodriguez A, De Smet R, Lemmens K, Fierro AC, Marchal K. 2011. COLOMBOS: access port for cross-platform bacterial expression compendia. PLoS One 6, e20938.
20. Fasoli M, Dal Santo S, Zenoni S, et al. 2012. The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. The Plant Cell 24, 3489-3505.
21. Fernandez-Del-Carmen A, Celis-Gamboa C, Visser RG, Bachem CW. 2007. Targeted transcript mapping for agronomic traits in potato. Journal of Experimental Botany 58, 2761-2774.
22. Flamini R, Mattivi F, De Rosso M, Arapitsas P, Bavaresco L. 2013. Advanced knowledge of three important classes of grape phenolics: anthocyanins, stilbenes and flavonols. International Journal of Molecular Sciences 14, 19651-19669.
23. Fontes N, Geros H, Delrot S. 2011. Grape berry vacuole: a complex and heterogeneous membrane system specialized in the accumulation of solutes. American Journal of Enology and Viticulture 62, 270-278.
24. Fournier-Level A, Hugueney P, Verries C, This P, Ageorges A. 2011. Genetic mechanisms underlying the methylation level of anthocyanins in grape (Vitis vinifera L.). BMC Plant Biology 11, 179.
25. Fujita A, Goto-Yamamoto N, Aramaki I, Hashizume K. 2006. Organspecific transcription of putative flavonol synthase genes of grapevine and effects of plant hormones and shading on flavonol biosynthesis in grape berry skins. Bioscience, Biotechnology, and Biochemistry 70, 632-638.
26. Giacomelli L, Nanni V, Lenzi L, Zhuang J, Dalla Serra M, Banfield MJ, Town CD, Silverstein KA, Baraldi E, Moser C. 2012. Identification and characterization of the defensin-like gene family of grapevine. Molecular Plant-Microbe Interactions 25, 1118-1131.
27. Gouthu S, O'Neil ST, Di Y, Ansarolia M, Megraw M, Deluc LG. 2014. A comparative study of ripening among berries of the grape cluster reveals an altered transcriptional programme and enhanced ripening rate in delayed berries. Journal of Experimental Botany 65, 5889-902.
28. Grimplet J, Van Hemert J, Carbonell-Bejerano P, Diaz-Riquelme J, Dickerson J, Fennell A, Pezzotti M, Martinez-Zapater JM. 2012. Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences. BMC Research Notes 5, 213.
29. Guo J, Jiang RH, Kamphuis LG, Govers F. 2006. A cDNA-AFLP based strategy to identify transcripts associated with avirulence in Phytophthora infestans. Fungal Genetics and Biology 43, 111-123.
30. Hanana M, Deluc L, Fouquet R, Daldoul S, Leon C, Barrieu F, Ghorbel A, Mliki A, Hamdi S. 2008. [Identification and characterization of 'rd22' dehydration responsive gene in grapevine (Vitis vinifera L.)]. Comptes Rendus Biologies 331, 569-578.
31. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B. 2005. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control lightresponsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Molecular Biology 57, 155-171.
32. Heddad M, Noren H, Reiser V, Dunaeva M, Andersson B, Adamska I. 2006. Differential expression and localization of early light-induced proteins in Arabidopsis. Plant Physiology 142, 75-87.
33. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.
34. Hmamouchi M, EsSafi N, Lahrichi M, Fruchier A, Essassi EM. 1996. Flavones and flavonols in leaves of some Moroccan Vitis vinifera cultivars. American Journal of Enology and Viticulture 47, 186-192.
35. Hugueney P, Provenzano S, Verries C, Ferrandino A, Meudec E, Batelli G, Merdinoglu D, Cheynier V, Schubert A, Ageorges A. 2009. A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine. Plant Physiology 150, 2057-2070.
36. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
37. Jeong ST, Goto-Yamamoto N, Hashizume K, Esaka M. 2006. Expression of the flavonoid 3?-hydroxylase and flavonoid 3?,5?-hydroxylase genes and flavonoid composition in grape (Vitis vinifera). Plant Science 170, 61-69.
38. Kloosterman B, Oortwijn M, uitdeWilligen J, America T, de Vos R, Visser RG, Bachem CW. 2010. From QTL to candidate gene: genetical genomics of simple and complex traits in potato using a pooling strategy. BMC Genomics 11, 158.
39. Kobayashi S, Ishimaru M, Hiraoka K, Honda C. 2002. Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215, 924-933.
40. Lewis DR, Ramirez MV, Miller ND, Vallabhaneni P, Ray WK, Helm RF, Winkel BS, Muday GK. 2011. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiology 156, 144-164.
41. Li X, Chen L, Hong M, et al. 2012. A large insertion in bHLH transcription factor BrTT8 resulting in yellow seed coat in Brassica rapa. PLoS One 7, e44145.
42. Liang Z, Owens CL, Zhong G-Y, Cheng L. 2011. Polyphenolic profiles detected in the ripe berries of Vitis vinifera germplasm. Food Chemistry 129, 940-950.
43. Liang Z, Yang Y, Cheng L, Zhong G-Y. 2012. Polyphenolic composition and content in the ripe berries of wild Vitis species. Food Chemistry 132, 730-738.
44. Lijavetzky D, Carbonell-Bejerano P, Grimplet J, Bravo G, Flores P, Fenoll J, Hellin P, Oliveros JC, Martinez-Zapater JM. 2012. Berry flesh and skin ripening features in Vitis vinifera as assessed by transcriptional profiling. PLoS One 7, e39547.
45. Liu J, Chen N, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng ZM. 2014. Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15, 281.
46. Martinez-Luscher J, Sanchez-Diaz M, Delrot S, Aguirreolea J, Pascual I, Gomes E. 2014. Ultraviolet-B radiation and water deficit interact to alter flavonol and anthocyanin profiles in grapevine berries through transcriptomic regulation. Plant and Cell Physiology 55, 1925-1936.
47. Mattivi F, Guzzon R, Vrhovsek U, Stefanini M, Velasco R. 2006. Metabolite profiling of grape: flavonols and anthocyanins. Journal of Agricultural and Food Chemistry 54, 7692-7702.
48. McDonald MS, Hughes M, Burns J, Lean ME, Matthews D, Crozier A. 1998. Survey of the free and conjugated myricetin and quercetin content of red wines of different geographical origins. Journal of Agricultural and Food Chemistry 46, 368-375.
49. Meysman P, Sonego P, Bianco L, et al. 2014. COLOMBOS v2. 0: an ever expanding collection of bacterial expression compendia. Nucleic Acids Research 42, D649-D653.
50. Nakayama M, Aihara M, Chen YN, Araie M, Tomita-Yokotani K, Iwashina T. 2011. Neuroprotective effects of flavonoids on hypoxia-, glutamate-, and oxidative stress-induced retinal ganglion cell death. Molecular Vision 17, 1784-1793.
51. Nassiri-Asl M, Hosseinzadeh H. 2009. Review of the pharmacological effects of Vitis vinifera (Grape) and its bioactive compounds. Phytotherapy Research 23, 1197-1204.
52. Ono E, Homma Y, Horikawa M, Kunikane-Doi S, Imai H, Takahashi S, Kawai Y, Ishiguro M, Fukui Y, Nakayama T. 2010. Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera). The Plant Cell 22, 2856-2871.
53. Oren-Shamir M. 2009. Does anthocyanin degradation play a significant role in determining pigment concentration in plants? Plant Science 177, 310-316.
54. Pons C, Marti C, Forment J, Crisosto CH, Dandekar AM, Granell A. 2014. A bulk segregant gene expression analysis of a peach population reveals components of the underlying mechanism of the fruit cold response. PLoS One 9, e90706.
55. Pontin MA, Piccoli PN, Francisco R, Bottini R, Martinez-Zapater JM, Lijavetzky D. 2010. Transcriptome changes in grapevine (Vitis vinifera L.) cv. Malbec leaves induced by ultraviolet-B radiation. BMC Plant Biology 10, 224.
56. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I. 2005. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. The Plant Cell 17, 2966-2980.
57. Reid KE, Olsson N, Schlosser J, Peng F, Lund ST. 2006. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biology 6, 27.
58. Ruepp A, Zollner A, Maier D, et al. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Research 32, 5539-5545.
59. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF. 2009. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45.
60. Sternad Lemut M, Sivilotti P, Franceschi P, Wehrens R, Vrhovsek U. 2013. Use of metabolic profiling to study grape skin polyphenol behavior as a result of canopy microclimate manipulation in a 'Pinot noir' vineyard. Journal of Agricultural and Food Chemistry 61, 8976-8986.
61. Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R. 2010. The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell and Environment 33, 88-103.
62. Teixeira A, Eiras-Dias J, Castellarin SD, Geros H. 2013. Berry phenolics of grapevine under challenging environments. International Journal of Molecular Science 14, 18711-18739.
63. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, RESEARCH0034.
64. Van Ooijen JW. 2009. MapQTL 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. Wageningen, The Netherlands: Plant Research International B. V. and Kyazma B. V.
65. Wils CR, Brandt W, Manke K, Vogt T. 2013. A single amino acid determines position specificity of an Arabidopsis thaliana CCoAOMT-like O-methyltransferase. FEBS Letters 587, 683-689.
66. Winkel-Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218-223.
67. Wong DC, Sweetman C, Drew DP, Ford CM. 2013. VTCdb: a gene co-expression database for the crop species Vitis vinifera (grapevine). BMC Genomics 14, 882.
68. Yamaguchi-Shinozaki K, Shinozaki K. 1993. The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Molecular and General Genetics 238, 17-25.
69. Yang J, Martinson TE, Liu RH. 2009. Phytochemical profiles and antioxidant activities of wine grapes. Food Chemistry 116, 332-339.
70. Zhao J, Dixon RA. 2010. The 'ins' and 'outs' of flavonoid transport. Trends in Plant Science 15, 72-80.
71. Zipor G, Duarte P, Carqueijeiro I, et al. 2014. In planta anthocyanin degradation by a vacuolar class III peroxidase in Brunfelsia calycina flowers. New Phytologist 205, 653-665.