Skip to main content
Log in

A review of target gene specificity of flavonoid R2R3-MYB transcription factors and a discussion of factors contributing to the target gene selectivity

  • Review
  • Published:
Frontiers in Biology

Abstract

Flavonoid biosynthetic genes are often coordinately regulated in a temporal manner during flower or fruit development, resulting in specific accumulation profiles of flavonoid compounds. R2R3-MYB-type transcription factors (TFs) “recruit” a set of biosynthetic genes to produce flavonoids, and, therefore, R2R3-MYBs are responsible for the coordinated expression of structural genes. Although a wealth of information regarding the identified and functionally characterized R2R3-MYBs that are involved in flavonoid accumulation is available to date, this is the first review on the global regulation of MYB factors in the flavonoid pathway. The data presented in this review demonstrate that anthocyanin, flavone/flavonol/3-deoxyflavonoid (FFD), proanthocyanidin (PA), and isoflavonoid are independently regulated by different subgroups of R2R3-MYBs. Furthermore, FFD-specific R2R3-MYBs have a preference for early biosynthetic genes (EBGs) as their target genes; anthocyanin-specific R2R3-MYBs from dicot species essentially regulate late biosynthetic genes (LBGs); the remaining R2R3-MYBs have a wider range of target gene specificity. To elucidate the nature of the differential target gene specificity between R2R3-MYBs, we analyzed the DNA binding domain (also termed the MYB-domain) of R2R3-MYBs and the distribution of the recognition cis-elements. We identified four conserved amino acid residues located in or just before helix-3 of dicot anthocyanin R2R3-MYBs that might account for the different recognition DNA sequence and subsequently the different target gene specificity to the remaining R2R3-MYB TFs.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aharoni A, De Vos C H, Wein M, Sun Z, Greco R, Kroon A, Mol J N, O’Connell A P (2001). The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J, 28(3): 319–332

    PubMed  CAS  Google Scholar 

  • Akagi T, Ikegami A, Tsujimoto T, Kobayashi S, Sato A, Kono A, Yonemori K (2009). DkMyb4 is a Myb transcription factor involved in proanthocyanidin biosynthesis in persimmon fruit. Plant Physiol, 151(4): 2028–2045

    PubMed  CAS  Google Scholar 

  • Akagi T, Ikegami A, Yonemori K (2010). DkMyb2 wound-induced transcription factor of persimmon (Diospyros kaki Thunb.), contributes to proanthocyanidin regulation. Planta, 232(5): 1045–1059

    PubMed  CAS  Google Scholar 

  • Albert NW, Lewis D H, Zhang H, Schwinn K E, Jameson P E, Davies K M (2011). Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. Plant J, 65(5): 771–784

    PubMed  CAS  Google Scholar 

  • Allan A C, Hellens R P, Laing W A (2008). MYB transcription factors that colour our fruit. Trends Plant Sci, 13(3): 99–102

    PubMed  CAS  Google Scholar 

  • Ang L H, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng X W (1998). Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell, 1(2): 213–222

    PubMed  CAS  Google Scholar 

  • Ballester A R, Molthoff J, de Vos R, Hekkert Bt, Orzaez D, Fernández-Moreno J P, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A (2010). Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol, 152(1): 71–84

    PubMed  CAS  Google Scholar 

  • Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007). Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol, 48(7): 958–970

    PubMed  CAS  Google Scholar 

  • Baudry A, Heim M A, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004). TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J, 39(3): 366–380

    PubMed  CAS  Google Scholar 

  • Boddu J, Jiang C, Sangar V, Olson T, Peterson T, Chopra S (2006). Comparative structural and functional characterization of sorghum and maize duplications containing orthologous myb transcription regulators of 3-deoxyflavonoid biosynthesis. Plant Mol Biol, 60(2): 185–199

    PubMed  CAS  Google Scholar 

  • Boddu J, Svabek C, Ibraheem F, Jones A D, Chopra S (2005). Characterization of a deletion allele of a sorghum Myb gene yellow seed1 showing loss of 3-deoxyflavonoids. Plant Sci, 169(3): 542–552

    CAS  Google Scholar 

  • Bogs J, Downey M O, Harvey J S, Ashton A R, Tanner G J, Robinson S P (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

    PubMed  CAS  Google Scholar 

  • Bogs J, Jaffé F W, Takos A M, Walker A R, Robinson S P (2007). The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol, 143(3): 1347–1361

    PubMed  CAS  Google Scholar 

  • Borevitz J O, Xia Y, Blount J, Dixon R A, Lamb C (2000). Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 12(12): 2383–2394

    PubMed  CAS  Google Scholar 

  • Borovsky Y, Oren-Shamir M, Ovadia R, De Jong W, Paran I (2004). The A locus that controls anthocyanin accumulation in pepper encodes a MYB transcription factor homologous to Anthocyanin2 of Petunia. Theor Appl Genet, 109(1): 23–29

    PubMed  CAS  Google Scholar 

  • Boss P K, Davies C, Robinson S P (1996). 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 

  • Bovy A, de Vos R, Kemper M, Schijlen E, Almenar Pertejo M, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S, Santos-Buelga C, van Tunen A (2002). High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell, 14(10): 2509–2526

    PubMed  CAS  Google Scholar 

  • Bushman B S, Snook M E, Gerke J P, Szalma S J, Berhow M A, Houchins K E, McMullen M D (2002). Two loci exert major effects on chlorogenic acid synthesis in maize silks. Crop Sci, 42(5): 1669–1678

    CAS  Google Scholar 

  • Chiou C Y, Yeh K W (2008). Differential expression of MYB gene (OgMYB1) determines color patterning in floral tissue of Oncidium Gower Ramsey. Plant Mol Biol, 66(4): 379–388

    PubMed  CAS  Google Scholar 

  • Chiu L W, Li L (2012). Characterization of the regulatory network of BoMYB2 in controlling anthocyanin biosynthesis in purple cauliflower. Planta, 236(4): 1153–1164

    PubMed  CAS  Google Scholar 

  • Chiu L W, Zhou X, Burke S, Wu X, Prior R L, Li L (2010). The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiol, 154(3): 1470–1480

    PubMed  CAS  Google Scholar 

  • Cocciolone S M, Nettleton D, Snook M E, Peterson T (2005). Transformation of maize with the p1 transcription factor directs production of silk maysin, a corn earworm resistance factor, in concordance with a hierarchy of floral organ pigmentation. Plant Biotechnol J, 3(2): 225–235

    PubMed  CAS  Google Scholar 

  • Cone K C, Burr F A, Burr B (1986). Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci U S A, 83(24): 9631–9635

    PubMed  CAS  Google Scholar 

  • Cone K C, Cocciolone SM, Burr F A, Burr B (1993). Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell, 5(12): 1795–1805

    PubMed  CAS  Google Scholar 

  • Czemmel S, Heppel S C, Bogs J (2012). R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma, 249(S2 Suppl 2): S109–S118

    PubMed  Google Scholar 

  • Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris N N, Walker A R, Robinson S P, Bogs J (2009). The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiol, 151(3): 1513–1530

    PubMed  CAS  Google Scholar 

  • Dare A P, Schaffer R J, Lin-Wang K, Allan A C, Hellens R P (2008). Identification of a cis-regulatory element by transient analysis of coordinately regulated genes. Plant Methods, 4(1): 17

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Deluc L, Bogs J, Walker A R, Ferrier T, Decendit A, Merillon J M, Robinson S P, 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

    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

    PubMed  CAS  Google Scholar 

  • Dhaubhadel S, Li X (2010). A new client for 14-3-3 proteins: GmMYB176, an R1 MYB transcription factor. Plant Signal Behav, 5(7): 921–923

    PubMed  CAS  Google Scholar 

  • Dhaubhadel S, McGarvey B D, Williams R, Gijzen M (2003). Isoflavonoid biosynthesis and accumulation in developing soybean seeds. Plant Mol Biol, 53(6): 733–743

    PubMed  CAS  Google Scholar 

  • Dixon R A, Xie D Y, Sharma S B (2005). Proanthocyanidins—a final frontier in flavonoid research? New Phytol, 165(1): 9–28

    PubMed  CAS  Google Scholar 

  • Downey M O, Harvey J S, Robinson S P (2003a). Analysis of tannins in seeds and skins of Shiraz grapes throughout berry development. Aust J Grape Wine Res, 9(1): 15–27

    CAS  Google Scholar 

  • Downey MO, Harvey J S, Robinson S P (2003b). Synthesis of flavonols and expression of flavonol synthase genes in the developing grape berries of Shiraz and Chardonnay (Vitis vinifera L.). Aust J Grape Wine Res, 9(2): 110–121

    CAS  Google Scholar 

  • Du H, Feng B R, Yang S S, Huang Y B, Tang Y X (2012a). The R2R3-MYB transcription factor gene family in maize. PLoS One, 7(6): e37463

    PubMed  Google Scholar 

  • Du H, Huang Y, Tang Y (2010). Genetic and metabolic engineering of isoflavonoid biosynthesis. Appl Microbiol Biotechnol, 86(5): 1293–1312

    PubMed  CAS  Google Scholar 

  • Du H, Yang S S, Liang Z, Feng B R, Liu L, Huang Y B, Tang Y X (2012b). Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol, 12(1): 106

    PubMed  CAS  Google Scholar 

  • Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul J M, Alboresi A, Weisshaar B, Lepiniec L (2008). MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J, 55(6): 940–953

    PubMed  CAS  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci, 15(10): 573–581

    PubMed  CAS  Google Scholar 

  • Elomaa P, Uimari A, Mehto M, Albert V A, Laitinen R A, Teeri T H (2003). Activation of anthocyanin biosynthesis in Gerbera hybrida (Asteraceae) suggests conserved protein-protein and protein-promoter interactions between the anciently diverged monocots and eudicots. Plant Physiol, 133(4): 1831–1842

    PubMed  CAS  Google Scholar 

  • Espley R V, Hellens R P, Putterill J, Stevenson D E, Kutty-Amma S, Allan A C (2007). Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J, 49(3): 414–427

    PubMed  CAS  Google Scholar 

  • Falcone Ferreyra M L, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K, Casati P, Grotewold E (2010). Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J, 62(1): 77–91

    PubMed  Google Scholar 

  • Falcone Ferreyra M L, Rius S P, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3: Article 222

  • Feldbrügge M, Sprenger M, Hahlbrock K, Weisshaar B (1997). PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J, 11(5): 1079–1093

    PubMed  Google Scholar 

  • Feng S, Wang Y, Yang S, Xu Y, Chen X (2010). Anthocyanin biosynthesis in pears is regulated by a R2R3-MYB transcription factor PyMYB10. Planta, 232(1): 245–255

    PubMed  CAS  Google Scholar 

  • Ferrer J L, Austin M B, Stewart C Jr, Noel J P (2008). Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol Biochem, 46(3): 356–370

    PubMed  CAS  Google Scholar 

  • Frampton J, Gibson T J, Ness S A, Döderlein G, Graf T (1991). Proposed structure for the DNA-binding domain of the Myb oncoprotein based on model building and mutational analysis. Protein Eng, 4(8): 891–901

    PubMed  CAS  Google Scholar 

  • Fujiwara H, Tanaka Y, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Nakao M, Fukui Y, Yamaguchi M, Ashikari T, Kusumi T (1998). cDNA cloning, gene expression and subcellular localization of anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Plant J, 16(4): 421–431

    PubMed  CAS  Google Scholar 

  • Gabrielsen O S, Sentenac A, Fromageot P (1991). Specific DNA binding by c-Myb: evidence for a double helix-turn-helix-related motif. Science, 253(5024): 1140–1143

    PubMed  CAS  Google Scholar 

  • Gao J, Shen X, Zhang Z, Peng R, Xiong A, Xu J, Zhu B, Zheng J, Yao Q (2011). The myb transcription factor MdMYB6 suppresses anthocyanin biosynthesis in transgenic Arabidopsis. Plant Cell Tissue Organ Cult, 106(2): 235–242

    CAS  Google Scholar 

  • Goff S A, Cone K C, Chandler V L (1992). Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev, 6(5): 864–875

    PubMed  CAS  Google Scholar 

  • Goff S A, Cone K C, Fromm M E (1991). Identification of functional domains in the maize transcriptional activator C1: comparison of wild-type and dominant inhibitor proteins. Genes Dev, 5(2): 298–309

    PubMed  CAS  Google Scholar 

  • Gong Z Z, Yamazaki M, Saito K (1999). A light-inducible Myb-like gene that is specifically expressed in red Perilla frutescens and presumably acts as a determining factor of the anthocyanin forma. Mol Gen Genet, 262(1): 65–72

    PubMed  CAS  Google Scholar 

  • Gonzalez A, Zhao M, Leavitt J M, Lloyd A M (2008). Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J, 53(5): 814–827

    PubMed  CAS  Google Scholar 

  • Grotewold E (2006). The genetics and biochemistry of floral pigments. Annu Rev Plant Biol, 57(1): 761–780

    PubMed  CAS  Google Scholar 

  • Grotewold E, Athma P, Peterson T (1991). Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc Natl Acad Sci U S A, 88(11): 4587–4591

    PubMed  CAS  Google Scholar 

  • Grotewold E, Chamberlin M, Snook M, Siame B, Butler L, Swenson J, Maddock S, St Clair G, Bowen B (1998). Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell, 10(5): 721–740

    PubMed  CAS  Google Scholar 

  • Grotewold E, Drummond B J, Bowen B, Peterson T (1994). The mybhomologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell, 76(3): 543–553

    PubMed  CAS  Google Scholar 

  • Hancock K R, Collette V, Fraser K, Greig M, Xue H, Richardson K, Jones C, Rasmussen S (2012). Expression of the R2R3-MYB transcription factor TaMYB14 from Trifolium arvense activates proanthocyanidin biosynthesis in the legumes Trifolium repens and Medicago sativa. Plant Physiol, 159(3): 1204–1220

    PubMed  CAS  Google Scholar 

  • 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 light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol, 57(2): 155–171

    PubMed  CAS  Google Scholar 

  • Heppel S C, Jaffé F W, Takos A M, Schellmann S, Rausch T, Walker A R, Bogs J (2013). Identification of key amino acids for the evolution of promoter target specificity of anthocyanin and proanthocyanidin regulating MYB factors. Plant Mol Biol, 82(4–5): 457–471

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hichri I, Deluc L, Barrieu F, Bogs J, Mahjoub A, Regad F, Gallois B, Granier T, Trossat-Magnin C, Gomès E, Lauvergeat V (2011b). A single amino acid change within the R2 domain of the VvMYB5b transcription factor modulates affinity for protein partners and target promoters selectivity. BMC Plant Biol, 11(1): 117

    PubMed  CAS  Google Scholar 

  • Huang W, Sun W, Lv H, Luo M, Zeng S, Pattanaik S, Yuan L, Wang Y (2013). A R2R3-MYB transcription factor from Epimedium sagittatum regulates the flavonoid biosynthetic pathway. PLoS One, 8(8): e70778

    PubMed  CAS  Google Scholar 

  • Ikegami A, Eguchi S, Kitajima A, Inoue K, Yonemori K (2007). Identification of genes involved in proanthocyanidin biosynthesis of persimmon (Diospyros kaki) fruit. Plant Sci, 172(5): 1037–1047

    CAS  Google Scholar 

  • Jackson D, Culianez-Macia F, Prescott A G, Roberts K, Martin C (1991). Expression patterns of myb genes from Antirrhinum flowers. Plant Cell, 3(2): 115–125

    PubMed  CAS  Google Scholar 

  • Jia L, Clegg M T, Jiang T (2004). Evolutionary dynamics of the DNAbinding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol, 134(2): 575–585

    PubMed  CAS  Google Scholar 

  • Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000). Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J, 19(22): 6150–6161

    PubMed  CAS  Google Scholar 

  • Jung C S, Griffiths H M, De Jong D M, Cheng S, Bodis M, Kim T S, De Jong W S (2009). The potato developer (D) locus encodes an R2R3 MYB transcription factor that regulates expression of multiple anthocyanin structural genes in tuber skin. Theor Appl Genet, 120(1): 45–57

    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

    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

    PubMed  CAS  Google Scholar 

  • Kong Q, Pattanaik S, Feller A, Werkman J R, Chai C, Wang Y, Grotewold E, Yuan L (2012). Regulatory switch enforced by basic helix-loop-helix and ACT-domain mediated dimerizations of the maize transcription factor R. Proc Natl Acad Sci U S A, 109(30): E2091–E2097

    PubMed  CAS  Google Scholar 

  • Lai Y S, Shimoyamada Y, Nakayama M, Yamagishi M (2012). Pigment accumulation and transcription of LhMYB12 and anthocyanin biosynthesis genes during flower development in the Asiatic hybrid lily (Lilium spp.). Plant Sci, 193–194: 136–147

    PubMed  Google Scholar 

  • Laitinen R A, Ainasoja M, Broholm S K, Teeri T H, Elomaa P (2008). Identification of target genes for a MYB-type anthocyanin regulator in Gerbera hybrida. J Exp Bot, 59(13): 3691–3703

    PubMed  CAS  Google Scholar 

  • Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng X W (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell, 19(3): 731–749

    PubMed  CAS  Google Scholar 

  • Lesnick M L, Chandler V L (1998). Activation of the maize anthocyanin gene a2 is mediated by an element conserved in many anthocyanin promoters. Plant Physiol, 117(2): 437–445

    PubMed  CAS  Google Scholar 

  • Li L, Ban Z J, Li X H, Wu M Y, Wang A L, Jiang Y Q, Jiang Y H (2012a). Differential expression of anthocyanin biosynthetic genes and transcription factor PcMYB10 in pears (Pyrus communis L.). PLoS One, 7(9): e46070

    PubMed  CAS  Google Scholar 

  • Li Z T, Gmitter F G, Grosser J W, Chen C, Gray D J (2012b). Isolation and characterization of a novel anthocyanin-promoting MYBA gene family in Citrus. Tree Genet Genomes, 8(4): 675–685

    Google Scholar 

  • Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens R P, Allan A C (2010). An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol, 10(1): 50

    PubMed  Google Scholar 

  • Liu Y (2010) Molecular analysis of genes involved in the synthesis of proanthocyanidins in Theobroma cacao. PhD Dissertation (USA: The Pennsylvania State University).

    Google Scholar 

  • Lüscher B, Eisenman R N (1990). New light on Myc and Myb. Part II. Myb. Genes Dev, 4(12B 12b): 2235–2241

    Google Scholar 

  • Mackova Z, Koblovska R, Lapcik O (2006). Distribution of isoflavonoids in non-leguminous taxa- an update. Phytochemistry, 67(9): 849–855

    PubMed  CAS  Google Scholar 

  • Mano H, Ogasawara F, Sato K, Higo H, Minobe Y (2007). Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiol, 143(3): 1252–1268

    PubMed  CAS  Google Scholar 

  • Martens S, Mithöfer A (2005). Flavones and flavone synthases. Phytochemistry, 66(20): 2399–2407

    PubMed  CAS  Google Scholar 

  • Martens S, Preuss A, Matern U (2010). Multifunctional flavonoid dioxygenases: flavonol and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry, 71(10): 1040–1049

    PubMed  CAS  Google Scholar 

  • Martin C, Gerats T (1993). Control of pigment biosynthesis genes during petal development. Plant Cell, 5(10): 1253–1264

    PubMed  CAS  Google Scholar 

  • Martin C, Prescott A, Mackay S, Bartlett J, Vrijlandt E (1991). Control of anthocyanin biosynthesis in flowers of Antirrhinum majus. Plant J, 1(1): 37–49

    PubMed  CAS  Google Scholar 

  • 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, Wagner D R (2003). Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell, 15(8): 1689–1703

    PubMed  CAS  Google Scholar 

  • Matsui K, Umemura Y, Ohme-Takagi M (2008). AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J, 55(6): 954–967

    PubMed  CAS  Google Scholar 

  • Matus J T, Loyola R, Vega A, Peña-Neira A, Bordeu E, Arce-Johnson P, Alcalde J A (2009). Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J Exp Bot, 60(3): 853–867

    PubMed  CAS  Google Scholar 

  • Matus J T, Poupin M J, Cañón P, Bordeu E, Alcalde J A, Arce-Johnson P (2010). Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.). Plant Mol Biol, 72(6): 607–620

    PubMed  CAS  Google Scholar 

  • Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005). The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol, 138(2): 1083–1096

    PubMed  CAS  Google Scholar 

  • Mellway R D, Tran L T, Prouse M B, Campbell M M, Constabel C P (2009). The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol, 150(2): 924–941

    PubMed  CAS  Google Scholar 

  • Miranda M, Ralph S G, Mellway R, White R, Heath M C, Bohlmann J, Constabel C P (2007). The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant Microbe Interact, 20(7): 816–831

    PubMed  CAS  Google Scholar 

  • Mol J, Grotewold E, Koes R (1998). How genes paint flowers and seeds. Trends Plant Sci, 3(6): 212–217

    Google Scholar 

  • Morita Y, Saitoh M, Hoshino A, Nitasaka E, Iida S (2006). Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant Cell Physiol, 47(4): 457–470

    PubMed  CAS  Google Scholar 

  • Morohashi K, Casas M I, Falcone Ferreyra M L, Mejía-Guerra M K, Pourcel L, Yilmaz A, Feller A, Carvalho B, Emiliani J, Rodriguez E, Pellegrinet S, McMullen M, Casati P, Grotewold E (2012). A genome-wide regulatory framework identifies maize pericarp color1 controlled genes. Plant Cell, 24(7): 2745–2764

    PubMed  CAS  Google Scholar 

  • Moyano E, Martínez-Garcia J F, Martin C (1996). Apparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in antirrhinum flowers. Plant Cell, 8(9): 1519–1532

    PubMed  CAS  Google Scholar 

  • Nakatsuka T, Haruta K S, Pitaksutheepong C, Abe Y, Kakizaki Y, Yamamoto K, Shimada N, Yamamura S, Nishihara M (2008). Identification and characterization of R2R3-MYB and bHLH transcription factors regulating anthocyanin biosynthesis in gentian flowers. Plant Cell Physiol, 49(12): 1818–1829

    PubMed  CAS  Google Scholar 

  • Nakatsuka T, Nishihara M, Mishiba K, Yamamura S (2005). Temporal expression of flavonoid biosynthesis-related genes regulates flower pigmentation in gentian plants. Plant Sci, 168(5): 1309–1318

    CAS  Google Scholar 

  • Nakatsuka T, Saito M, Yamada E, Fujita K, Kakizaki Y, Nishihara M (2012). Isolation and characterization of GtMYBP3 and GtMYBP4, orthologues of R2R3-MYB transcription factors that regulate early flavonoid biosynthesis, in gentian flowers. J Exp Bot, 63(18): 6505–6517

    PubMed  CAS  Google Scholar 

  • Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000). The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell, 12(10): 1863–1878

    PubMed  CAS  Google Scholar 

  • Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001). The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell, 13(9): 2099–2114

    PubMed  CAS  Google Scholar 

  • Nishihara M, Nakatsuka T (2011). Genetic engineering of flavonoid pigments to modify flower color in floricultural plants. Biotechnol Lett, 33(3): 433–441

    PubMed  CAS  Google Scholar 

  • Niu S S, Xu C J, Zhang WS, Zhang B, Li X, Lin-Wang K, Ferguson I B, Allan A C, Chen K S (2010). Coordinated regulation of anthocyanin biosynthesis in Chinese bayberry (Myrica rubra) fruit by a R2R3 MYB transcription factor. Planta, 231(4): 887–899

    PubMed  CAS  Google Scholar 

  • Noda N, Kanno Y, Kato N, Kazuma K, Suzuki M (2004). Regulation of gene expression involved in flavonol and anthocyanin biosynthesis during petal development in lisianthus (Eustoma grandiflorum). Physiol Plant, 122(3): 305–313

    CAS  Google Scholar 

  • Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y (1992). Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci U S A, 89(14): 6428–6432

    PubMed  CAS  Google Scholar 

  • Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y (1994). Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell, 79(4): 639–648

    PubMed  CAS  Google Scholar 

  • Osier T L, Lindroth R L (2001). Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol, 27(7): 1289–1313

    PubMed  CAS  Google Scholar 

  • Palapol Y, Ketsa S, Lin-Wang K, Ferguson I B, Allan A C (2009). A MYB transcription factor regulates anthocyanin biosynthesis in mangosteen (Garcinia mangostana L.) fruit during ripening. Planta, 229(6): 1323–1334

    PubMed  CAS  Google Scholar 

  • Pattanaik S, Kong Q, Zaitlin D, Werkman J R, Xie C H, Patra B, Yuan L (2010). Isolation and functional characterization of a floral tissuespecific R2R3 MYB regulator from tobacco. Planta, 231(5): 1061–1076

    PubMed  CAS  Google Scholar 

  • Paz-Ares J, Ghosal D, Wienand U, Peterson P A, Saedler H (1987). The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J, 6(12): 3553–3558

    PubMed  CAS  Google Scholar 

  • Peel G J, Pang Y, Modolo L V, Dixon R A (2009). The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago. Plant J, 59(1): 136–149

    PubMed  CAS  Google Scholar 

  • Peters D J, Constabel C P (2002). Molecular analysis of herbivoreinduced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J, 32(5): 701–712

    PubMed  CAS  Google Scholar 

  • Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006). PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell, 18(5): 1274–1291

    PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R (1999). Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell, 11(8): 1433–1444

    PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing J F, van der Woude K, Mol J N, Koes R (1998). Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J, 13(4): 475–488

    PubMed  CAS  Google Scholar 

  • Rabinowicz P D, Braun E L, Wolfe A D, Bowen B, Grotewold E (1999). Maize R2R3 Myb genes: Sequence analysis reveals amplification in the higher plants. Genetics, 153(1): 427–444

    PubMed  CAS  Google Scholar 

  • Ravaglia D, Espley R V, Henry-Kirk R A, Andreotti C, Ziosi V, Hellens R P, Costa G, Allan A C (2013). Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biol, 13(1): 68

    PubMed  CAS  Google Scholar 

  • Roth B A, Goff S A, Klein T M, Fromm M E (1991). C1- and Rdependent expression of the maize Bz1 gene requires sequences with homology to mammalian myb and myc binding sites. Plant Cell, 3(3): 317–325

    PubMed  CAS  Google Scholar 

  • Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L (2006). Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta, 224(1): 96–107

    PubMed  CAS  Google Scholar 

  • Sablowski R W, Moyano E, Culianez-Macia F A, Schuch W, Martin C, Bevan M (1994). A flower-specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. EMBO J, 13(1): 128–137

    PubMed  CAS  Google Scholar 

  • Saikumar P, Murali R, Reddy E P (1990). Role of tryptophan repeats and flanking amino acids in Myb-DNA interactions. Proc Natl Acad Sci U S A, 87(21): 8452–8456

    PubMed  CAS  Google Scholar 

  • Sainz M B, Grotewold E, Chandler V L (1997). Evidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins. Plant Cell, 9(4): 611–625

    PubMed  CAS  Google Scholar 

  • Saito R, Fukuta N, Ohmiya A, Itoh Y, Ozeki Y, Kuchitsu K, Nakayama M (2006). Regulation of anthocyanin biosynthesis involved in the formation of marginal picotee petals in Petunia. Plant Sci, 170(4): 828–834

    CAS  Google Scholar 

  • Sasaki M, Ogata K, Hatanaka H, Nishimura Y (2000). Backbone dynamics of the c-Myb DNA-binding domain complexed with a specific DNA. J Biochem, 127(6): 945–953

    PubMed  CAS  Google Scholar 

  • Schaart J G, Dubos C, Romero De La Fuente I, van Houwelingen A M, de Vos R C, Jonker H H, Xu W, Routaboul J M, Lepiniec L, Bovy A G (2013). Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits. New Phytol, 197(2): 454–467

    PubMed  CAS  Google Scholar 

  • Schröder G, Brown J W, Schröder J (1988). Molecular analysis of resveratrol synthase. cDNA, genomic clones and relationship with chalcone synthase. Eur J Biochem, 172(1): 161–169

    Google Scholar 

  • Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006). A small family of MYBregulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell, 18(4): 831–851

    PubMed  CAS  Google Scholar 

  • Sharma M, Chai C, Morohashi K, Grotewold E, Snook M E, Chopra S (2012). Expression of flavonoid 3′-hydroxylase is controlled by P1, the regulator of 3-deoxyflavonoid biosynthesis in maize. BMC Plant Biol, 12(1): 196

    PubMed  CAS  Google Scholar 

  • Solano R, Fuertes A, Sánchez-Pulido L, Valencia A, Paz-Ares J (1997). A single residue substitution causes a switch from the dual DNA binding specificity of plant transcription factor MYB.Ph3 to the animal c-MYB specificity. J Biol Chem, 272(5): 2889–2895

    CAS  Google Scholar 

  • Solano R, Nieto C, Avila J, Cañas L, Diaz I, Paz-Ares J (1995). Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J, 14(8): 1773–1784

    PubMed  CAS  Google Scholar 

  • Spelt C, Quattrocchio F, Mol J N, Koes R (2000). anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell, 12(9): 1619–1632

    PubMed  CAS  Google Scholar 

  • Springob K, Nakajima J, Yamazaki M, Saito K (2003). Recent advances in the biosynthesis and accumulation of anthocyanins. Nat Prod Rep, 20(3): 288–303

    PubMed  CAS  Google Scholar 

  • Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007). Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J, 50(4): 660–677

    PubMed  CAS  Google Scholar 

  • Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie A R, Weisshaar B (2010). Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation. New Phytol, 188(4): 985–1000

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tahirov T H, Sato K, Ichikawa-Iwata E, Sasaki M, Inoue-Bungo T, Shiina M, Kimura K, Takata S, Fujikawa A, Morii H, Kumasaka T, Yamamoto M, Ishii S, Ogata K (2002). Mechanism of c-Myb-C/EBP beta cooperation from separated sites on a promoter. Cell, 108(1): 57–70

    PubMed  CAS  Google Scholar 

  • Takos A M, Jaffé F W, Jacob S R, Bogs J, Robinson S P, Walker A R (2006). Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol, 142(3): 1216–1232

    PubMed  CAS  Google Scholar 

  • Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia F A, Roberts K, Martin C (1998). The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell, 10(2): 135–154

    PubMed  CAS  Google Scholar 

  • Tanaka Y, Brugliera F, Chandler S (2009). Recent progress of flower colour modification by biotechnology. Int J Mol Sci, 10(12): 5350–5369

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Tuerck J A, Fromm M E (1994). Elements of the maize A1 promoter required for transactivation by the anthocyanin B/C1 or phlobaphene P regulatory genes. Plant Cell, 6(11): 1655–1663

    PubMed  CAS  Google Scholar 

  • Uimari A, Strommer J (1997). Myb26: a MYB-like protein of pea flowers with affinity for promoters of phenylpropanoid genes. Plant J, 12(6): 1273–1284

    PubMed  CAS  Google Scholar 

  • Verdier J, Zhao J, Torres-Jerez I, Ge S, Liu C, He X, Mysore K S, Dixon R A, Udvardi M K (2012). MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. Proc Natl Acad Sci U S A, 109(5): 1766–1771

    PubMed  CAS  Google Scholar 

  • Waiss A C, Chan B G, Elliger C A, Wiseman B R, McMillian W W, Widstrom N W, Zuber M S, Keaster A J (1979). Maysin, a flavone glycoside from corn silks with antibiotic activity toward corn earworm. J Econ Entomol, 72: 256–258

    CAS  Google Scholar 

  • Wang X (2011). Structure, function, and engineering of enzymes in isoflavonoid biosynthesis. Funct Integr Genomics, 11(1): 13–22

    PubMed  CAS  Google Scholar 

  • Wei Y L, Li J N, Lu J, Tang Z L, Pu D C, Chai Y R (2007). Molecular cloning of Brassica napus TRANSPARENT TESTA 2 gene family encoding potential MYB regulatory proteins of proanthocyanidin biosynthesis. Mol Biol Rep, 34(2): 105–120

    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

    CAS  Google Scholar 

  • Winkel-Shirley B (2002). Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol, 5(3): 218–223

    PubMed  CAS  Google Scholar 

  • Xie D Y, Dixon R A (2005). Proanthocyanidin biosynthesis-still more questions than answers? Phytochemistry, 66(18): 2127–2144

    PubMed  CAS  Google Scholar 

  • Yamagishi M, Shimoyamada Y, Nakatsuka T, Masuda K (2010). Two R2R3-MYB genes, homologs of Petunia AN2, regulate anthocyanin biosyntheses in flower Tepals, tepal spots and leaves of asiatic hybrid lily. Plant Cell Physiol, 51(3): 463–474

    PubMed  CAS  Google Scholar 

  • Yi J, Derynck M R, Li X, Telmer P, Marsolais F, Dhaubhadel S (2010). A single-repeat MYB transcription factor, GmMYB176, regulates CHS8 gene expression and affects isoflavonoid biosynthesis in soybean. Plant J, 62(6): 1019–1034

    PubMed  CAS  Google Scholar 

  • Yoshida K, Iwasaka R, Kaneko T, Sato S, Tabata S, Sakuta M (2008). Functional differentiation of Lotus japonicus TT2s, R2R3-MYB transcription factors comprising a multigene family. Plant Cell Physiol, 49(2): 157–169

    PubMed  CAS  Google Scholar 

  • Zhang B, Hu Z, Zhang Y, Li Y, Zhou S, Chen G (2012). A putative functional MYB transcription factor induced by low temperature regulates anthocyanin biosynthesis in purple kale (Brassica Oleracea var. acephala f. tricolor). Plant Cell Rep, 31(2): 281–289

    PubMed  Google Scholar 

  • Zhang P, Chopra S, Peterson T (2000). A segmental gene duplication generated differentially expressed myb-homologous genes in maize. Plant Cell, 12(12): 2311–2322

    PubMed  CAS  Google Scholar 

  • Zhang P, Wang Y, Zhang J, Maddock S, Snook M, Peterson T (2003). A maize QTL for silk maysin levels contains duplicated Mybhomologous genes which jointly regulate flavone biosynthesis. Plant Mol Biol, 52(1): 1–15

    PubMed  CAS  Google Scholar 

  • Zhao L, Gao L, Wang H, Chen X, Wang Y, Yang H, Wei C, Wan X, Xia T (2013). The R2R3-MYB, bHLH, WD40, and related transcription factors in flavonoid biosynthesis. Funct Integr Genomics, 13(1): 75–98

    PubMed  CAS  Google Scholar 

  • Zifkin M, Jin A, Ozga J A, Zaharia L I, Schernthaner J P, Gesell A, Abrams S R, Kennedy J A, Constabel C P (2012). Gene expression and metabolite profiling of developing highbush blueberry fruit indicates transcriptional regulation of flavonoid metabolism and activation of abscisic acid metabolism. Plant Physiol, 158(1): 200–224

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Huanxiu Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lai, Y., Li, H. & Yamagishi, M. A review of target gene specificity of flavonoid R2R3-MYB transcription factors and a discussion of factors contributing to the target gene selectivity. Front. Biol. 8, 577–598 (2013). https://doi.org/10.1007/s11515-013-1281-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-013-1281-z

Keywords

Navigation