Plant flavonoids-biosynthesis, transport and involvement in stress responses

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14950-14973

  Petrussa, Elisa ^a   Braidot, Enrico ^a   Zancani, Marco ^a   Peresson, Carlo ^a   Bertolini, Alberto ^a   Patui, Sonia ^a   Vianello, Angelo ^a  

^a UNIVERSITY OF UDINE   (Italy)

Author keywords

ABC transporters; Bilitranslocase; Biotic and abiotic stress; Flavonoid transport; Secondary metabolites

Indexed keywords

ABC TRANSPORTER; BILITRANSLOCASE; FLAVONOID; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MULTIDRUG AND TOXIC COMPOUND EXTRUSION; MULTIDRUG RESISTANCE PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ABIOTIC STRESS; ARABIDOPSIS; BIOSYNTHESIS; BIOTIC STRESS; CELL COMPARTMENTALIZATION; CELL VACUOLE; CELLULAR DISTRIBUTION; FRUIT RIPENING; GENE EXPRESSION REGULATION; GLUTATHIONE S TRANSFERASE GENE; GRAPE; NONHUMAN; PLANT GENOME; PLANT RESPONSE; PLANT STRESS; PROTEIN EXPRESSION; REVIEW; STRUCTURE ANALYSIS; TEMPERATURE MEASUREMENT; TONOPLAST; TRANSPORT KINETICS; UPREGULATION; VASCULAR BUNDLE (PLANT); WATER DEFICIT;

EID: 84880750196     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714950     Document Type: Review

References (129)

1. Debeaujon, I.; Peeters, A.J.M.; Leon-Kloosterziel, K.M.; 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, 853-871.
2. Kitamura, S. Transport of Flavonoids: From Cytosolic Synthesis to Vacuolar Accumulation. In Science of Flavonoids; Grotewold, E., Ed.; Springer: Berlin, Germany, 2006; pp. 123-146.
3. Castellarin, S.D.; Di Gaspero, G.; Marconi, R.; Nonis, A.; Peterlunger, E.; Paillard, S.; Adam-Blondon, A.F.; Testolin, R. Colour variation in red grapevines (Vitis vinifera L.): Genomic organisation, expression of flavonoid 3'-hydroxylase, flavonoid 3',5'-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocyanins in berry skin. BMC Genom. 2006, 7, doi:10.1186/1471-2164-7-12.
4. Conde, C.; Silva, P.; Fontes, N.; Dias, A.C.P.; Tavares, R.M.; Sousa, M.J.; Agasse, A.; Delrot, S.; Geros, H. Biochemical changes throughout grape berry development and fruit and wine quality. Food 2007, 1, 1-22.
5. Bogs, J.; Ebadi, A.; McDavid, D.; Robinson, S.P. Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiol. 2006, 140, 279-291.
6. Springob, K.; Nakajima, J.; Yamazaki, M.; Saito, K. Recent advances in the biosynthesis and accumulation of anthocyanins. Nat. Prod. Rep. 2003, 20, 288-303.
7. Zhao, J.; Huhman, D.; Shadle, G.; He, X.Z.; Sumner, L.W.; Tang, Y.H.; Dixon, R.A. MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. Plant Cell 2011, 23, 1536-1555.
8. Boss, P.K.; Davies, C.; Robinson, S.P. Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv shiraz grape berries and the implications for pathway regulation. Plant Physiol. 1996, 111, 1059-1066.
9. Famiani, F.; Walker, R.P.; Tecsi, L.; Chen, Z.H.; Proietti, P.; Leegood, R.C. An immunohistochemical study of the compartmentation of metabolism during the development of grape (Vitis vinifera L.) berries. J. Exp. Bot. 2000, 51, 675-683.
10. Yazaki, K. Transporters of secondary metabolites. Curr. Opin. Plant Biol. 2005, 8, 301-307.
11. Markham, K.R.; Gould, K.S.; Winefield, C.S.; Mitchell, K.A.; Bloor, S.J.; Boase, M.R. Anthocyanic vacuolar inclusions-Their nature and significance in flower colouration. Phytochemistry 2000, 55, 327-336.
12. Lecas, M.; Brillouet, J.M. Cell-wall composition of grape berry skins. Phytochemistry 1994, 35, 1241-1243.
13. Gagne, S.; Saucier, C.; Geny, L. Composition and cellular localization of tannins in cabernet sauvignon skins during growth. J. Agric. Food Chem. 2006, 54, 9465-9471.
14. Grotewold, E. The challenges of moving chemicals within and out of cells: Insights into the transport of plant natural products. Planta 2004, 219, 906-909.
15. Martinoia, E.; Maeshima, M.; Neuhaus, H.E. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 2007, 58, 83-102.
16. He, F.; Mu, L.; Yan, G.L.; Liang, N.N.; Pan, Q.H.; Wang, J.; Reeves, M.J.; Duan, C.Q. Biosynthesis of anthocyanins and their regulation in colored grapes. Molecules 2010, 15, 9057-9091.
17. Conn, S.; Franco, C.; Zhang, W. Characterization of anthocyanic vacuolar inclusions in Vitis vinifera L. cell suspension cultures. Planta 2010, 231, 1343-1360.
18. Terrier, N.; Glissant, D.; Grimplet, J.; Barrieu, F.; Abbal, P.; Couture, C.; Ageorges, A.; Atanassova, R.; Leon, C.; Renaudin, J.P.; et al. Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 2005, 222, 832-847.
19. Ageorges, A.; Fernandez, L.; Vialet, S.; Merdinoglu, D.; Terrier, N.; Romieu, C. Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci. 2006, 170, 372-383.
20. Stafford, H.A. Possible multienzyme complexes regulating the formation of C6-C3 phenolic compounds and lignins in higher plants. Recent Adv. Phytochem. 1974, 8, 53-79.
21. Winkel, B.S.J. Metabolic channeling in plants. Annu. Rev. Plant Biol. 2004, 55, 85-107.
22. Kuhn, B.M.; Geisler, M.; Bigler, L.; Ringli, C. Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol. 2011, 156, 585-595.
23. Ono, E.; Fukuchi-Mizutani, M.; Nakamura, N.; Fukui, Y.; Yonekura-Sakakibara, K.; Yamaguchi, M.; Nakayama, T.; Tanaka, T.; Kusumi, T.; Tanaka, Y. Yellow flowers generated by expression of the aurone biosynthetic pathway. Proc. Natl. Acad. Sci. USA 2006, 103, 11075-11080.
24. Saslowsky, D.E.; Warek, U.; Winkel, B.S.J. Nuclear localization of flavonoid enzymes in Arabidopsis. J. Biol. Chem. 2005, 280, 23735-23740.
25. Toda, K.; Kuroiwa, H.; Senthil, K.; Shimada, N.; Aoki, T.; Ayabe, S.; Shimada, S.; Sakuta, M.; Miyazaki, Y.; Takahashi, R. The soybean F3'H protein is localized to the tonoplast in the seed coat hilum. Planta 2012, 236, 79-89.
26. Wang, H.L.; Wang, W.; Zhang, P.; Pan, Q.H.; Zhan, J.C.; Huang, W.D. Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Sci. 2010, 179, 103-113.
27. Tian, L.; Wan, S.B.; Pan, Q.H.; Zheng, Y.J.; Huang, W.D. A novel plastid localization of chalcone synthase in developing grape berry. Plant Sci. 2008, 175, 431-436.
28. Wang, H.L.; Wang, W.; Li, H.; Zhang, P.; Zhan, J.C.; Huang, W.D. Expression and tissue and subcellular localization of anthocyanidin synthase (ANS) in grapevine. Protoplasma 2011, 248, 267-279.
29. Castellarin, S.D.; di Gaspero, G. Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines. BMC Plant Biol. 2007, 7, doi:10.1186/1471-2229-7-46.
30. Bogs, J.; Downey, M.O.; Harvey, J.S.; Ashton, A.R.; Tanner, G.J.; Robinson, S.P. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol. Biochem. 2005, 139, 652-663.
31. Zhao, J.; Pang, Y.Z.; Dixon, R.A. The mysteries of proanthocyanidin transport and polymerization. Plant Physiol. 2010, 153, 437-443.
32. Pourcel, L.; Routaboul, J.M.; Kerhoas, L.; Caboche, M.; Lepiniec, L.; Debeaujon, I. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 2005, 17, 2966-2980.
33. Gomez, C.; Terrier, N.; Torregrosa, L.; Vialet, S.; Fournier-Level, A.; Verries, C.; Souquet, J.M.; Mazauric, J.P.; Klein, M.; Cheynier, V.; et al. Grapevine MATE-type proteins act as vacuolar H-dependent acylated anthocyanin transporters. Plant Physiol. 2009, 150, 402-415.
34. Nozue, M.; Yamada, K.; Nakamura, T.; Kubo, H.; Kondo, M.; Nishimura, M. Expression of a vacuolar protein (VP24) in anthocyanin-producing cells of sweet potato in suspension culture. Plant Physiol. 1997, 115, 1065-1072.
35. Martinoia, E.; Klein, M.; Geisler, M.; Bovet, L.; Forestier, C.; Kolukisaoglu, U.; Muller-Rober, B.; Schulz, B. Multifunctionality of plant ABC transporters-More than just detoxifiers. Planta 2002, 214, 345-355.
36. Klein, M.; Burla, B.; Martinoia, E. The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett. 2006, 580, 1112-1122.
37. Zhao, J.; Dixon, R.A. The 'ins' and 'outs' of flavonoid transport. Trends Plant Sci. 2010, 15, 72-80.
38. Martinoia, E.; Meyer, S.; de Angeli, A.; Nagy, R. Vacuolar transporters in their physiological context. Annu. Rev. Plant Biol. 2012, 63, 183-213.
39. Kanga, J.; Parka, J.; Choia, H.; Burlab, B.; Kretzschmarb, T.; Leea, Y.; Martinoia, E. Plant ABC transporters. Arabidopsis B. 2011, 9, doi:10.1199/tab.0153.
40. Rea, P.A. Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 2007, 58, 347-375.
41. Klein, M.; Martinoia, E.; Hoffmann-Thoma, G.; Weissenbock, G. A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: Regulation of glucuronide uptake by glutathione and its conjugates. Plant J. 2000, 21, 289-304.
42. Goodman, C.D.; Casati, P.; Walbot, V. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 2004, 16, 1812-1826.
43. Mueller, L.A.; Goodman, C.D.; Silady, R.A.; Walbot, V. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol. 2000, 123, 1561-1570.
44. Marrs, K.A.; Alfenito, M.R.; Lloyd, A.M.; Walbot, V. A glutathione-S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 1995, 375, 397-400.
45. Alfenito, M.R.; Souer, E.; Goodman, C.D.; 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.
46. Koes, R.; Verweij, W.; Quattrocchio, F. Flavonoids: A colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 2005, 10, 236-242.
47. Larsen, E.S.; Alfenito, M.R.; Briggs, W.R.; Walbot, V. A carnation anthocyanin mutant is complemented by the glutathione S-transferases encoded by maize BZ2 and petunia AN9. Plant Cell Rep. 2003, 21, 900-904.
48. 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.
49. Francisco, R.M.; Regalado, A.; Ageorges, A.S.; Burla, B.J.; Bassin, B.; Eisenach, C.; Zarrouk, O.; Vialet, S.; Marlin, T.R.S.; Chaves, M.M.; et al. ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides. Plant Cell 2013, 25, 1840-1854.
50. Zhao, J.; Dixon, R.A. Mate transporters facilitate vacuolar uptake of epicatechin 3'-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 2009, 21, 2323-2340.
51. Mathews, H.; Clendennen, S.K.; Caldwell, C.G.; Liu, X.L.; Connors, K.; Matheis, N.; Schuster, D.K.; Menasco, D.J.; Wagoner, W.; Lightner, J.; et al. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 2003, 15, 1689-1703.
52. Marinova, K.; Kleinschmidt, K.; Weissenbock, G.; Klein, M. Flavonoid biosynthesis in barley primary leaves requires the presence of the vacuole and controls the activity of vacuolar flavonoid transport. Plant Physiol. 2007, 144, 432-444.
53. Frangne, N.; Eggmann, T.; Koblischke, C.; Weissenbock, G.; Martinoia, E.; Klein, M. Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H-antiport and ATP-binding cassette-type mechanisms. Plant Physiol. 2002, 128, 726-733.
54. Passamonti, S.; Cocolo, A.; Braidot, E.; Petrussa, E.; Peresson, C.; Medic, N.; Macri, F.; Vianello, A. Characterization of electrogenic bromosulfophthalein transport in carnation petal microsomes and its inhibition by antibodies against bilitranslocase. FEBS J. 2005, 272, 3282-3296.
55. Nicolin, V.; Grill, V.; Micali, F.; Narducci, P.; Passamonti, S. Immunolocalisation of bilitranslocase in mucosecretory and parietal cells of the rat gastric mucosa. J. Mol. Histol. 2005, 36, 45-50.
56. Passamonti, S.; Terdoslavich, M.; Margon, A.; Cocolo, A.; Medic, N.; Micali, F.; Decorti, G.; Franko, M. Uptake of bilirubin into HEPG2 cells assayed by thermal lens spectroscopy-Bilitranslocase. FEBS J. 2005, 272, 5522-5535.
57. Jones, S. An overview of the basic helix-loop-helix proteins. Genome Biol. 2004, 5, doi:10.1186/gb-2004-5-6-226.
58. Heim, M.A.; Jakoby, M.; Werber, M.; Martin, C.; Weisshaar, B.; Bailey, P.C. The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 2003, 20, 735-747.
59. Hichri, I.; Barrieu, F.; Bogs, J.; Kappel, C.; Delrot, S.; Lauvergeat, V. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 2011, 62, 2465-2483.
60. Stracke, R.; Werber, M.; Weisshaar, B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 2001, 4, 447-456.
61. Czemmel, S.; Heppel, S.C.; Bogs, J. R2R3 MYB transcription factors: Key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 2012, 249, 109-118.
62. DeVetten, N.; Quattrocchio, F.; Mol, J.; Koes, R. The AN11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Gen. Dev. 1997, 11, 1422-1434.
63. Quattrocchio, F.; Bauldry, A.; Lepiniec, L.; Grotewold, E. The Regulation of Flavonoid Biosynthesis. In The Science of Flavonoids; Grotewold, E., Ed.; Springer: New York, NY, USA, 2006; pp. 97-122.
64. Nesi, N.; Jond, C.; Debeaujon, I.; Caboche, M.; Lepiniec, L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 2001, 13, 2099-2114.
65. Poustka, F.; Irani, N.G.; Feller, A.; Lu, Y.; Pourcel, L.; Frame, K.; Grotewold, E. A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol. 2007, 145, 1323-1335.
66. Sun, Y.; Li, H.; Huang, J.R. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol. Plant 2012, 5, 387-400.
67. Zhang, H.B.; Wang, L.; Deroles, S.; Bennett, R.; Davies, K. New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biol. 2006, 6, doi:10.1186/1471-2229-6-29.
68. Grotewold, E.; Chamberlin, M.; Snook, M.; Siame, B.; Butler, L.; Swenson, J.; Maddock, S.; Clair, G.S.; Bowen, B. Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 1998, 10, 721-740.
69. Nozue, M.; Yasuda, H. Occurrence of anthocyanoplasts in cell-suspension cultures of sweet-potato. Plant Cell Rep. 1985, 4, 252-255.
70. Grotewold, E.; Davies, K. Trafficking and sequestration of anthocyanins. Nat. Prod. Commun. 2008, 3, 1251-1258.
71. Snyder, B.A.; Nicholson, R.L. Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 1990, 248, 1637-1639.
72. Mueller, L.A.; Walbot, V. Models for Vacuolar Sequestration of Anthocyanins. In Regulation of Phytochemicals by Molecular Techniques; Romeo, J.T., Saunders, J.A., Matthews, B.F., Eds.; Pergamon: New York, NY, USA, 2001; pp. 297-312.
73. Lin, Y.; Irani, N.G.; Grotewold, E. Sub-cellular trafficking of phytochemicals explored using auto-fluorescent compounds in maize cells. BMC Plant Biol. 2003, 19, 10-12.
74. Pourcel, L.; Irani, N.G.; Lu, Y.H.; Riedl, K.; Schwartz, S.; Grotewold, E. The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol. Plant 2010, 3, 78-90.
75. Pecket, R.C.; Small, C.J. Occurrence, location and development of anthocyanoplasts. Phytochemistry 1980, 19, 2571-2576.
76. Dinter, A.; Berger, E.G. Golgi-disturbing agents. Histochem. Cell Biol. 1998, 109, 571-590.
77. Abrahams, S.; Lee, E.; Walker, A.R.; Tanner, G.J.; Larkin, P.J.; Ashton, A.R. The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant J. 2003, 35, 624-636.
78. Malsam, J.; Kreye, S.; Sollner, T.H. Membrane fusion: Snares and regulation. Cell. Mol. Life Sci. 2008, 65, 2814-2832.
79. Lipka, V.; Kwon, C.; Panstruga, R. SNARE-ware: The role of SNARE-domain proteins in plant biology. Annu. Rev. Cell Dev. Biol. 2007, 23, 147-174.
80. Meyer, D.; Pajonk, S.; Micali, C.; O'Connell, R.; Schulze-Lefert, P. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. 2009, 57, 986-999.
81. Saslowsky, D.; Winkel-Shirley, B. Localization of flavonoid enzymes in Arabidopsis roots. Plant J. 2001, 27, 37-48.
82. Buer, C.S.; Muday, G.K. The TRANSPARENT TESTA4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 2004, 16, 1191-1205.
83. Kaltenbach, M.; Schroder, G.; Schmelzer, E.; Lutz, V.; Schroder, J. Flavonoid hydroxylase from Catharanthus roseus: cDNA, heterologous expression, enzyme properties and cell-type specific expression in plants. Plant J. 1999, 19, 183-193.
84. Brown, D.E.; Rashotte, A.M.; Murphy, A.S.; Normanly, J.; Tague, B.W.; Peer, W.A.; Taiz, L.; Muday, G.K. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 2001, 126, 524-535.
85. Subramanian, S.; Stacey, G.; Yu, O. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J. 2006, 48, 261-273.
86. Akiyama, K.; Matsuzaki, K.; Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435, 824-827.
87. Juszczuk, I.M.; Wiktorowska, A.; Malusa, E.; Rychter, A.M. Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.). Plant Soil 2004, 267, 41-49.
88. Besseau, S.; Hoffmann, L.; Geoffroy, P.; Lapierre, C.; Pollet, B.; Legrand, M. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 2007, 19, 148-162.
89. Peer, W.A.; Murphy, A.S.Flavonoids and A Auxin transport: Modulators or regulators? Trends Plant Sci. 2007, 12, 556-563.
90. Buer, C.S.; Muday, G.K.; Djordjevic, M.A. Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol. 2007, 145, 478-490.
91. Buer, C.S.; Muday, G.K.; Djordjevic, M.A. Implications of long-distance flavonoid movement in Arabidopsis thaliana. Plant Signal. Behav. 2008, 3, 415-417.
92. Lewis, D.R.; Wu, G.S.; Ljung, K.; Spalding, E.P. Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 multidrug resistance-like transporter. Plant J. 2009, 60, 91-101.
93. Gomez, C.; Conejero, G.; Torregrosa, L.; Cheynier, V.; Terrier, N.; Ageorges, A. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of ANTHOMATE transporters and GST. Plant J. 2011, 67, 960-970.
94. Zhang, W.; Conn, S.; Franco, C. Characterisation of anthocyanin transport and storage in Vitis vinifera L. cv. Gamay freaux cell suspension cultures. J. Biotechnol. 2007, 131, S208-S208.
95. Conn, S.; Curtin, C.; Bezier, A.; Franco, C.; Zhang, W. Purification, molecular cloning, and characterization of glutathione S-transferases (GSTs) from pigmented Vitis vinifera L. cell suspension cultures as putative anthocyanin transport proteins. J. Exp. Bot. 2008, 59, 3621-3634.
96. Cutanda-Perez, M.C.; Ageorges, A.; Gomez, C.; Vialet, S.; Terrier, N.; Romieu, C.; Torregrosa, L. Ectopic expression of VLMYBA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport. Plant Mol. Biol. 2009, 69, 633-648.
97. Zhang, J.W.; Ma, H.Q.; Feng, J.D.; Zeng, L.; Wang, Z.; Chen, S.W. Grape berry plasma membrane proteome analysis and its differential expression during ripening. J. Exp. Bot. 2008, 59, 2979-2990.
98. Conn, S.; Zhang, W.; Franco, C. Anthocyanic vacuolar inclusions (AVIs) selectively bind acylated anthocyanins in Vitis vinifera L. (grapevine) suspension culture. Biotechnol. Lett. 2003, 25, 835-839.
99. Braidot, E.; Petrussa, E.; Bertolini, A.; Peresson, C.; Ermacora, P.; Loi, N.; Terdoslavich, M.; Passamonti, S.; Macri, F.; Vianello, A. Evidence for a putative flavonoid translocator similar to mammalian bilitranslocase in grape berries (Vitis vinifera L.) during ripening. Planta 2008, 228, 203-213.
100. Grimplet, J.; Deluc, L.G.; Tillett, R.L.; Wheatley, M.D.; Schlauch, K.A.; Cramer, G.R.; Cushman, J.C. Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genom. 2007, 8, doi:10.1186/1471-2164-8-187.
101. Bertolini, A.; Peresson, C.; Petrussa, E.; Braidot, E.; Passamonti, S.; Macri, F.; Vianello, A. Identification and localization of the bilitranslocase homologue in white grape berries (Vitis vinifera L.) during ripening. J. Exp. Bot. 2009, 60, 3861-3871.
102. Zhang, X.Y.; Wang, X.L.; Wang, X.F.; Xia, G.H.; Pan, Q.H.; Fan, R.C.; Wu, F.Q.; Yu, X.C.; Zhang, D.P. 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.
103. Klein, M.; Weissenbock, G.; Dufaud, A.; Gaillard, C.; Kreuz, K.; Martinoia, E. Different energization mechanisms drive the vacuolar uptake of a flavonoid glucoside and a herbicide glucoside. J. Biol. Chem. 1996, 271, 29666-29671.
104. Deluc, L.; Barrieu, F.; Marchive, C.; Lauvergeat, V.; Decendit, A.; Richard, T.; Carde, J.P.; Merillon, J.M.; Hamdi, S. Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol. 2006, 140, 499-511.
105. Terrier, N.; Torregrosa, L.; Ageorges, A.; Vialet, S.; Verries, C.; Cheynier, V.; Romieu, C. Ectopic expression of vvmybpa2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol. 2009, 149, 1028-1041.
106. Winkel-Shirley, B. Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 2002, 5, 218-223.
107. Belhadj, A.; Telef, N.; Saigne, C.; Cluzet, S.; Barrieu, F.; Hamdi, S.; Merillon, J.M. Effect of methyl jasmonate in combination with carbohydrates on gene expression of pr proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol. Biochem. 2008, 46, 493-499.
108. Zhang, W.; Curtin, C.; Kikuchi, M.; Franco, C. Integration of jasmonic acid and light irradiation for enhancement of anthocyanin biosynthesis in vitis vinifera suspension cultures. Plant Sci. 2002, 162, 459-468.
109. Repka, V.; Fischerova, I.; Silharova, K. Methyl jasmonate is a potent elicitor of multiple defense responses in grapevine leaves and cell-suspension cultures. Biol. Plant. 2004, 48, 273-283.
110. Rozema, J.; vandeStaaij, J.; Bjorn, L.O.; Caldwell, M. UV-b as an environmental factor in plant life: Stress and regulation. Trends Ecol. Evol. 1997, 12, 22-28.
111. Downey, M.O.; Harvey, J.S.; Robinson, S.P. The effect of bunch shading on berry development and flavonoid accumulation in Shiraz grapes. Austr. J. Grape Wine Res. 2004, 10, 55-73.
112. Agati, G.; Azzarello, E.; Pollastri, S.; Tattini, M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012, 196, 67-76.
113. Cortell, J.M.; Kennedy, J.A. Effect of shading on accumulation of flavonoid compounds in (Vitis vinifera L.) pinot noir fruit and extraction in a model system. J. Agric. Food Chem. 2006, 54, 8510-8520.
114. Matus, J.T.; Loyola, R.; Vega, A.; Pena-Neira, A.; Bordeu, E.; Arce-Johnson, P.; Alcalde, J.A. Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of vitis vinifera. J. Exp. Bot. 2009, 60, 853-867.
115. Koyama, K.; Ikeda, H.; Poudel, P.R.; Goto-Yamamoto, N. Light quality affects flavonoid biosynthesis in young berries of cabernet sauvignon grape. Phytochemistry 2012, 78, 54-64.
116. Pastore, C.; Zenoni, S.; Fasoli, M.; Pezzotti, M.; Tornielli, G.B.; Filippetti, I. Selective defoliation affects plant growth, fruit transcriptional ripening program and flavonoid metabolism in grapevine. BMC Plant Biol. 2013, 13, doi:10.1186/1471-2229-13-30.
117. Zheng, Y.; Li, J.H.; Xin, H.P.; Wang, N.; Guan, L.; Wu, B.H.; Li, S.H. Anthocyanin profile and gene expression in berry skin of two red Vitis vinifera grape cultivars that are sunlight dependent versus sunlight independent. Austr. J. Grape Wine Res. 2013, 19, 238-248.
118. Azuma, A.; Yakushiji, H.; Koshita, Y.; Kobayashi, S. Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 2012, 236, 1067-1080.
119. Chalker-Scott, L. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 1999, 70, 1-9.
120. Choi, S.; Kwon, Y.R.; Hossain, M.A.; Hong, S.W.; Lee, B.H.; Lee, H. A mutation in ELA1, an age-dependent negative regulator of PAP1/MYB75, causes UV- and cold stress-tolerance in Arabidopsis thaliana seedlings. Plant Sci. 2009, 176, 678-686.
121. Spayd, S.E.; Tarara, J.M.; Mee, D.L.; Ferguson, J.C. Separation of sunlight and temperature effects on the composition of Vitis vinifera cv. Merlot berries. Am. J. Enol. Vit. 2002, 53, 171-182.
122. Mori, K.; Sugaya, S.; Gemma, H. Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci. Hortic. 2005, 105, 319-330.
123. Yamane, T.; Jeong, S.T.; Goto-Yamamoto, N.; Koshita, Y.; Kobayashi, S. Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am. J. Enol. Vit. 2006, 57, 54-59.
124. Mori, K.; Goto-Yamamoto, N.; Kitayama, M.; Hashizume, K. Loss of anthocyanins in red-wine grape under high temperature. J. Exp. Bot. 2007, 58, 1935-1945.
125. Matthews, M.A.; Anderson, M.M. Fruit ripening in Vitis vinifera L.-Responses to seasonal water deficits. Am. J. Enol. Vit. 1988, 39, 313-320.
126. Ojeda, H.; Andary, C.; Kraeva, E.; Carbonneau, A.; Deloire, A. Influence of pre- and postveraison water deficit on synthesis and concentration of skin phenolic compounds during berry growth of Vitis vinifera cv. Shiraz. Am. J. Enol. Vit. 2002, 53, 261-267.
127. Roby, G.; Harbertson, J.F.; Adams, D.A.; Matthews, M.A. Berry size and vine water deficits as factors in winegrape composition: Anthocyanins and tannins. Austr. J. Grape Wine Res. 2004, 10, 100-107.
128. Kennedy, J.A.; Matthews, M.A.; Waterhouse, A.L. Effect of maturity and vine water status on grape skin and wine flavonoids. Am. J. Enol. Vit. 2002, 53, 268-274.
129. Castellarin, S.D.; Matthews, M.A.; di Gaspero, G.; Gambetta, G.A. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 2007, 227, 101-112.