Skip to main content
SpringerLink
Log in

R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Flavonoids compose one of the most abundant and important subgroups of secondary metabolites with more than 6,000 compounds detected so far in higher plants. They are found in various compositions and concentrations in nearly all plant tissues. Besides the attraction of pollinators and dispersers to fruits and flowers, flavonoids also protect against a plethora of stresses including pathogen attack, wounding and UV irradiation. Flavonoid content and composition of fruits such as grapes, bilberries, strawberries and apples as well as food extracts such as green tea, wine and chocolate have been associated with fruit quality including taste, colour and health-promoting effects. To unravel the beneficial potentials of flavonoids on fruit quality, research has been focused recently on the molecular basis of flavonoid biosynthesis and regulation in economically important fruit-producing plants such as grapevine (Vitis vinifera L.). Transcription factors and genes encoding biosynthetic enzymes have been characterized, studies that set a benchmark for future research on the regulatory networks controlling flavonoid biosynthesis and diversity. This review summarizes recent advances in the knowledge of regulatory cascades involved in flavonoid biosynthesis in grapevine. Transcriptional regulation of flavonoid biosynthesis during berry development is highlighted, with a particular focus on MYB transcription factors as molecular clocks, key regulators and powerful biotechnological tools to identify novel pathway enzymes to optimize flavonoid content and composition in grapes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams DO (2006) Phenolics and ripening in grape berries. Am J Enol Vitic 57(3):249–256

    CAS  Google Scholar 

  • Ali K, Maltese F, Zyprian E, Rex M, Choi YH, Verpoorte R (2009) NMR metabolic fingerprinting based identification of grapevine metabolites associated with downy mildew resistance. J Agric Food Chem 57(20):9599–9606

    Article  PubMed  CAS  Google Scholar 

  • Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13(3):99–102

    Article  PubMed  CAS  Google Scholar 

  • Bagchi D, Bagchi M, Stohs SJ, Das DK, Ray SD, Kuszynski CA, Joshi SS, Pruess HG (2000) Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention. Toxicology 148(2–3):187–197

    Article  PubMed  CAS  Google Scholar 

  • Bagchi D, Sen CK, Ray SD, Das DK, Bagchi M, Preuss HG, Vinson JA (2003) Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat Res Fundam Mol Mech Mutagen 523–524:87–97

    Article  Google Scholar 

  • Bailly C, Cormier F, Bao Do C (1997) Characterization and activities of S-adenosyl-l-methionine:cyanidin 3-glucoside 3′-O-methyltransferase in relation to anthocyanin accumulation in Vitis vinifera cell suspension cultures. Plant Sci 122(1):81–89

    Article  CAS  Google Scholar 

  • Baranac JM, Petranović NA, Dimitrić-Marković JM (1997) Spectrophotometric study of anthocyan copigmentation reactions. 4. Malvin and apigenin 7-glucoside. J Agric Food Chem 45(5):1701–1703

    Article  CAS  Google Scholar 

  • Bogs J, Downey MO, Harvey JS, Ashton AR, Tanner GJ, Robinson SP (2005) Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol 139(2):652–663

    Article  PubMed  CAS  Google Scholar 

  • Bogs J, Ebadi A, McDavid D, Robinson SP (2006) Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development. Plant Physiol 140(1):279–291

    Article  PubMed  CAS  Google Scholar 

  • Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143(3):1347–1361

    Article  PubMed  CAS  Google Scholar 

  • Boss PK, Davies C, Robinson SP (1996a) 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 111(4):1059–1066

    PubMed  CAS  Google Scholar 

  • Boss PK, Davies C, Robinson SP (1996b) Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Mol Biol 32(3):565–569

    Article  PubMed  CAS  Google Scholar 

  • Boulton R (2001) The copigmentation of anthocyanins and its role in the color of red wine: a critical review. Am J Enol Vitic 52(2):67–87

    CAS  Google Scholar 

  • Boyer J, Liu RH (2004) Apple phytochemicals and their health benefits. Nutr J 3:5

    Article  PubMed  Google Scholar 

  • Braidot E, Zancani M, Petrussa E, Peresson C, Bertolini A, Patui S, Macrì F, Vianello A (2008) Transport and accumulation of flavonoids in grapevine (Vitis vinifera L.). Plant Signal Behav 3(9):626–632

    Article  PubMed  Google Scholar 

  • Brugliera F, Barri-Rewell G, Holton TA, Mason JG (1999) Isolation and characterization of a flavonoid 3′-hydroxylase cDNA clone corresponding to the Ht1 locus of Petunia hybrida. Plant J 19(4):441–451

    Article  PubMed  CAS  Google Scholar 

  • 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 Online 16(5):1191–1205

    Article  CAS  Google Scholar 

  • Cadot Y, Miñana-Castelló MT, Chevalier M (2006) Anatomical, histological, and histochemical changes in grape seeds from Vitis vinifera L. cv Cabernet franc during fruit development. J Agric Food Chem 54(24):9206–9215

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30(11):1381–1399

    Article  PubMed  CAS  Google Scholar 

  • Castellarin SD, Gambetta GA, Wada H, Shackel KA, Matthews MA (2011) Fruit ripening in Vitis vinifera: spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis. J Exp Bot 62(12):4345–4354

    Article  PubMed  CAS  Google Scholar 

  • Conde C, Silva P, Fontes N, Dias ACP, Tavares RM, Sousa MJ, Agasse A, Delrot S, Gerós H (2007) Biochemical changes throughout grape berry development and fruit and wine quality. Food 1(1):1–22

    Google Scholar 

  • Cutanda-Perez M-C, Ageorges A, Gomez C, Vialet S, Terrier N, Romieu C, Torregrosa L (2009) Ectopic expression of VlmybA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport. Plant Mol Biol 69(6):633–648

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 151(3):1513–1530

    Article  PubMed  CAS  Google Scholar 

  • Dai GH, Andary C, Mondolot-Cosson L, Boubals D (1995) Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiol Mol Plant Pathol 46(3):177–188

    Article  Google Scholar 

  • Delgado R, Martín P, del Álamo M, González M-R (2004) Changes in the phenolic composition of grape berries during ripening in relation to vineyard nitrogen and potassium fertilisation rates. J Sci Food Agric 84(7):623–630

    Article  CAS  Google Scholar 

  • Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde J-P, Mérillon J-M, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140(2):499–511

    Article  PubMed  CAS  Google Scholar 

  • Deluc L, Bogs J, Walker AR, Ferrier T, Decendit A, Merillon J-M, Robinson SP, Barrieu F (2008) The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanidin biosynthesis in developing grape berries. Plant Physiol 147(4):2041–2053

    Article  PubMed  CAS  Google Scholar 

  • Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, Pelletier G, Delseny M (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J 19(4):387–398

    Article  PubMed  CAS  Google Scholar 

  • Dimitrić Marković JM, Baranac JM, Brdarić TP (2005) Electronic and infrared vibrational analysis of cyanidin–quercetin copigment complex. Spectrochim Acta A Mol Biomol Spectrosc 62(1–3):673–680

    Article  PubMed  Google Scholar 

  • Dixon RA, Pasinetti GM (2010) Flavonoids and isoflavonoids: from plant biology to agriculture and neuroscience. Plant Physiol 154(2):453–457

    Article  PubMed  CAS  Google Scholar 

  • Doshi P, Adsule P, Banerjee K (2006) Phenolic composition and antioxidant activity in grapevine parts and berries (Vitis vinifera L.) cv. Kishmish Chornyi (Sharad Seedless) during maturation. Int J Food Sci Technol 41:1–9

    CAS  Google Scholar 

  • Downey MO, Harvey JS, Robinson SP (2003a) Analysis of tannins in seeds and skins of Shiraz grapes throughout berry development. Australian Journal of Grape and Wine Research 9(1):15–27

    Article  CAS  Google Scholar 

  • Downey MO, Harvey JS, Robinson SP (2003b) 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(2):110–121

    Article  CAS  Google Scholar 

  • Downey MO, Harvey JS, Robinson SP (2004) The effect of bunch shading on berry development and flavonoid accumulation in Shiraz grapes. Australian J Grape Wine Res 10(1):55–73

    Article  CAS  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49(3):414–427

    Article  PubMed  CAS  Google Scholar 

  • Ford CM, Boss PK, Høj PB (1998) Cloning and characterization of Vitis viniferaUDP-glucose:flavonoid 3-O-glucosyltransferase, a homologue of the enzyme encoded by the maize bronze-1locus that may primarily serve to glucosylate anthocyanidins in vivo. J Biol Chem 273(15):9224–9233

    Article  PubMed  CAS  Google Scholar 

  • Fournier-Level A, Le Cunff L, Gomez C, Doligez A, Ageorges A, Roux C, Bertrand Y, Souquet J-M, Cheynier V, This P (2009) Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study. Genetics 183(3):1127–1139

    Article  PubMed  CAS  Google Scholar 

  • Fujita A, Goto-Yamamoto N, Aramaki I, Hashizume K (2006) Organ-specific transcription of putative flavonol synthase genes of grapevine and effects of plant hormones and shading on flavonol biosynthesis in grape berry skins. Biosci Biotechnol Biochem 70(3):632–638

    Article  PubMed  CAS  Google Scholar 

  • Gerhäuser C, Klimo K, Heiss E, Neumann I, Gamal-Eldeen A, Knauft J, Liu G-Y, Sitthimonchai S, Frank N (2003) Mechanism-based in vitro screening of potential cancer chemopreventive agents. Mutation Re(Gerhäuser et al.)search/Fundamental and Molecular Mechanisms of Mutagenesis 523-524 (0):163-172

  • Goto-Yamamoto N, Wan GH, Masaki K, Kobayashi S (2002) Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera). Plant Sci 162(6):867–872

    Article  CAS  Google Scholar 

  • Grotewold E (2006) The science of flavonoids. Springer, Berlin

    Book  Google Scholar 

  • Guidoni S, Ferrandino A, Novello V (2008) Effects of seasonal and agronomical practices on skin anthocyanin profile of Nebbiolo grapes. Am J Enol Vitic 59(1):22–29

    CAS  Google Scholar 

  • Häkkinen SH, Törrönen AR (2000) Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: influence of cultivar, cultivation site and technique. Food Res Int 33(6):517–524

    Article  Google Scholar 

  • Hichri I, Heppel SC, Pillet J, Léon C, Czemmel S, Delrot S, Lauvergeat V, Bogs J (2010) The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol Plant 3(3):509–523

    Article  PubMed  CAS  Google Scholar 

  • Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 62(8):2465–2483

    Article  PubMed  CAS  Google Scholar 

  • Hmamouchi M, Es-Safi N, Lahrichi M, Fruchier A, Essassi EM (1996) Flavones and flavonols in leaves of some Moroccan Vitis vinifera cultivars. Am J Enol Vitic 47(2):186–192

    CAS  Google Scholar 

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7(7):1071–1083

    PubMed  CAS  Google Scholar 

  • Holton TA, Brugliera F, Lester DR, Tanaka Y, Hyland CD, Menting JGT, Lu C-Y, Farcy E, Stevenson TW, Cornish EC (1993) Cloning and expression of cytochrome P450 genes controlling flower colour. Nature 366(6452):276–279

    Article  PubMed  CAS  Google Scholar 

  • Hugueney P, Provenzano S, Verriès 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 Physiol 150(4):2057–2070

    Article  PubMed  CAS  Google Scholar 

  • Jaakola L, Määttä K, Pirttilä AM, Törrönen R, Kärenlampi S, Hohtola A (2002) Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Physiol 130(2):729–739

    Article  PubMed  CAS  Google Scholar 

  • Kennedy JA, Hayasaka Y, Vidal S, Waters EJ, Jones GP (2001) Composition of grape skin proanthocyanidins at different stages of berry development. J Agric Food Chem 49(11):5348–5355

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215(6):924–933

    Article  PubMed  CAS  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10(5):236–242

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M (1990) Mutations affecting the testa colour in Arabidopsis. Arabid Inf Serv 27:1–4

    Google Scholar 

  • Lea U, Slimestad R, Smedvig P, Lillo C (2007) Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway. Planta 225(5):1245–1253

    Article  PubMed  CAS  Google Scholar 

  • Lee KW, Kang NJ, Heo Y-S, Rogozin EA, Pugliese A, Hwang MK, Bowden GT, Bode AM, Lee HJ, Dong Z (2008) Raf and MEK protein kinases are direct molecular targets for the chemopreventive effect of quercetin, a major flavonol in red wine. Cancer Res 68(3):946–955

    Article  PubMed  CAS  Google Scholar 

  • Liu RH (2004) Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134(12):3479S–3485S

    PubMed  CAS  Google Scholar 

  • Lloyd A, Walbot V, Davis R (1992) Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science 258(5089):1773–1775

    Article  PubMed  CAS  Google Scholar 

  • Marles MAS, Ray H, Gruber MY (2003) New perspectives on proanthocyanidin biochemistry and molecular regulation. Phytochemistry 64(2):367–383

    Article  PubMed  CAS  Google Scholar 

  • Martens S, Teeri T, Forkmann G (2002) Heterologous expression of dihydroflavonol 4-reductases from various plants. FEBS Lett 531(3):453–458

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Butelli E, Petroni K, Tonelli C (2011) How can research on plants contribute to promoting human health? The Plant Cell Online 23(5):1685–1699

    Article  CAS  Google Scholar 

  • Mattivi F, Guzzon R, Vrhovsek U, Stefanini M, Velasco R (2006) Metabolite profiling of grape: flavonols and anthocyanins. J Agric Food Chem 54(20):7692–7702

    Article  PubMed  CAS  Google Scholar 

  • Matus J, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8(1):83

    Article  PubMed  Google Scholar 

  • Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci 89(15):7213–7217

    Article  PubMed  CAS  Google Scholar 

  • Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58(8):1935–1945

    Article  PubMed  CAS  Google Scholar 

  • Nassiri-Asl M, Hosseinzadeh H (2009) Review of the pharmacological effects of Vitis vinifera (grape) and its bioactive compounds. Phytother Res 23(9):1197–1204

    Article  PubMed  CAS  Google Scholar 

  • 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 Online 22(8):2856–2871

    Article  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12(12):556–563

    Article  PubMed  CAS  Google Scholar 

  • Price SF, Breen PJ, Valladao M, Watson BT (1995) Cluster sun exposure and quercetin in Pinot noir grapes and wine. Am J Enol Vitic 46(2):187–194

    CAS  Google Scholar 

  • Ristic R, Bindon K, Francis LI, Herderich MJ, Iland PG (2010) Flavonoids and C13-norisoprenoids in Vitis vinifera L. cv. Shiraz: relationships between grape and wine composition, wine colour and wine sensory properties. Australian Journal of Grape and Wine Research 16(3):369–388

    Article  CAS  Google Scholar 

  • Robinson SP, Davies C (2000) Molecular biology of grape berry ripening. Australian Journal of Grape and Wine Research 6(2):175–188

    Article  CAS  Google Scholar 

  • Sánchez-Moreno C, Cao G, Ou B, Prior RL (2003) Anthocyanin and proanthocyanidin content in selected white and red wines. Oxygen radical absorbance capacity comparison with nontraditional wines obtained from Highbush blueberry. J Agric Food Chem 51(17):4889–4896

    Article  PubMed  Google Scholar 

  • Sompornpailin K, Makita Y, Yamazaki M, Saito K (2002) A WD-repeat-containing putative regulatory protein in anthocyanin biosynthesis in Perilla frutescens. Plant Mol Biol 50(3):485–495

    Article  PubMed  CAS  Google Scholar 

  • Souquet J-M, Cheynier V, Brossaud F, Moutounet M (1996) Polymeric proanthocyanidins from grape skins. Phytochemistry 43(2):509–512

    Article  CAS  Google Scholar 

  • Souquet J-M, Labarbe B, Le Guernevé C, Cheynier V, Moutounet M (2000) Phenolic composition of grape stems. J Agric Food Chem 48(4):1076–1080

    Article  PubMed  CAS  Google Scholar 

  • Stewart AJ, Chapman W, Jenkins GI, Graham I, Martin T, Crozier A (2001) The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant Cell Environ 24(11):1189–1197

    Article  CAS  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Current Opin Plant Biol 4(5):447–456

    Article  CAS  Google Scholar 

  • Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006a) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142(3):1216–1232

    Article  PubMed  CAS  Google Scholar 

  • Takos AM, Ubi BE, Robinson SP, Walker AR (2006b) Condensed tannin biosynthesis genes are regulated separately from other flavonoid biosynthesis genes in apple fruit skin. Plant Sci 170(3):487–499

    Article  CAS  Google Scholar 

  • Terrier N, Torregrosa L, Ageorges A, Vialet S, Verriès C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149(2):1028–1041

    Article  PubMed  CAS  Google Scholar 

  • This P, Lacombe T, Cadle-Davidson M, Owens C (2007) Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1. TAG. Theor Appl Genet 114(4):723–730

    Article  PubMed  Google Scholar 

  • Thompson EP, Davies JM, Glover BJ (2010) Identifying the transporters of different flavonoids in plants. Plant Signal & Behavior 5(7):860–863

    Article  CAS  Google Scholar 

  • Traka MH, Mithen RF (2011) Plant science and human nutrition: challenges in assessing health-promoting properties of phytochemicals. Plant Cell 23(7):2483–2497

    Article  PubMed  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20

    Article  PubMed  CAS  Google Scholar 

  • Vvedenskaya IO, Rosen RT, Guido JE, Russell DJ, Mills KA, Vorsa N (2003) Characterization of flavonols in cranberry (Vaccinium macrocarpon) powder. J Agric Food Chem 52(2):188–195

    Article  Google Scholar 

  • Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J 49(5):772–785

    Article  PubMed  CAS  Google Scholar 

  • Weisshaar B, Jenkins GI (1998) Phenylpropanoid biosynthesis and its regulation. Curr Opin Plant Biol 1(3):251–257

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493

    Article  PubMed  CAS  Google Scholar 

  • Yamane T, Jeong ST, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57(1):54–59

    CAS  Google Scholar 

  • Yamasaki H, Uefuji H, Sakihama Y (1996) Bleaching of the red anthocyanin induced by superoxide radical. Arch Biochem Biophys 332(1):183–186

    Article  PubMed  CAS  Google Scholar 

  • Ylstra B, Touraev A, Moreno RMB, Stöger E, van Tunen AJ, Vicente O, Mol JNM, Heberle-Bors E (1992) Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol 100(2):902–907

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40(1):22–34

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to apologize to those colleagues whose work could not be cited due to space constraints. We wish to thank the Bundesministerium für Bildung und Forschung (BMBF) and its GABI initiative for financial support.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Centre for Organismal Studies Heidelberg (COS Heidelberg), Im Neuenheimer Feld 360, 69120, Heidelberg, Germany

    Stefan Czemmel & Simon C. Heppel

  2. Dienstleistungszentrum Ländlicher Raum (DLR) Rheinpfalz, Viticulture and Enology group, Breitenweg 71, 67435, Neustadt/W, Germany

    Jochen Bogs

  3. Fachhochschule Bingen, Berlinstr. 109, 55411, Bingen am Rhein, Germany

    Jochen Bogs

Authors
  1. Stefan Czemmel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon C. Heppel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jochen Bogs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefan Czemmel.

Additional information

Handling Editor: Kang Chong

Rights and permissions

Reprints and permissions

About this article

Cite this article

Czemmel, S., Heppel, S.C. & Bogs, J. R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 249 (Suppl 2), 109–118 (2012). https://doi.org/10.1007/s00709-012-0380-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-012-0380-z

Keywords

Search

Navigation