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Roles of R2R3-MYB transcription factors in transcriptional regulation of anthocyanin biosynthesis in horticultural plants

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Abstract

Key message

This review contains functional roles of MYB transcription factors in the transcriptional regulation of anthocyanin biosynthesis in horticultural plants. This review describes potential uses of MYB TFs as tools for metabolic engineering for anthocyanin production.

Abstract

Anthocyanins (ranging from red to blue) are controlled by specific branches of the anthocyanin biosynthetic pathway and are mostly visible in ornamentals, fruits, and vegetables. In the present review, we describe which R2R3-MYB transcription factors (TFs) control the transcriptional regulation of anthocyanin structural genes involved in the specific branches of the anthocyanin biosynthetic pathway in various horticultural plants (e.g., ornamentals, fruits, and vegetables). In addition, some MYBs responsible for anthocyanin accumulation in specific tissues are described. Moreover, we highlight the phylogenetic relationships of the MYBs that suppress or promote anthocyanin synthesis in horticultural crops. Enhancement of anthocyanin synthesis via metabolic genetic engineering of anthocyanin MYBs, which is described in the review, is indicative of the potential use of the mentioned anthocyanin-related MYBs as tools for anthocyanin production. Therefore, the MYBs would be suitable for metabolic genetic engineering for improvement of flower colors, fruit quality, and vegetable nutrients.

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References

  • Aharoni A, Ric De CH, Wein M, Sun ZK, Greco R, Kroon A, Mol JNM, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and Xavonol accumulation in transgenic tobacco. Plant J 28:319–332

    Article  CAS  PubMed  Google Scholar 

  • Ai TN, Naing AH, Arun M, Lim SH, Kim CK (2016) Sucrose-induced anthocyanin accumulation in vegetative tissue of petunia plants requires anthocyanin regulatory transcription factors. Plant Sci 252:144–150

    Article  CAS  PubMed  Google Scholar 

  • Ai TN, Naing AH, Arun M, Jeon SM, Kim CK (2017) Expression of RsMYB1 in petunia enhances anthocyanin production in vegetative and floral tissues. Sci Hortic 214:58–65

    Article  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 232:1045–1059

    Article  CAS  PubMed  Google Scholar 

  • Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in petunia. J Exp Bot 60:2191–2202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albert NW, Arathoon S, Collette VE, Schwinn KE, Jameson PE, Lewis DH (2010) Activation of anthocyanin synthesis in Cymbidium orchids: variability between known regulators. Plant Cell Tiss Organ Cult 100:355–360

    Article  CAS  Google Scholar 

  • Albert NW, Lewis DH, Zhang H, Schwinn KE, Jameson PE, Davies KM (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 65:771–784

    Article  CAS  PubMed  Google Scholar 

  • Albert NW, Davies KM, Lewis DH, Zhang H, Montefiori M, Brendolise C (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26:962–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • An XH, Tian Y, Chen KQ, Liu XJ, Liu DD, Xie XB (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol 56:650–662

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 48:958–970

    Article  CAS  PubMed  Google Scholar 

  • Ben ZMM, Negre-Zakharov F, Masci T, Ovadis M, Shklarman E (2008) Interlinking showy traits: co-engineering of scent and colour biosynthesis in flowers. Plant Biotechnol 6:403–415

    Article  CAS  Google Scholar 

  • Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borovsky Y, Oren-Shamir M, Ovadia R, Jong WD, 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 109:23–29

    Article  CAS  PubMed  Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S (2008) Enrichment of tomato fruit with health promoting anthocyanins by expression of select transcription factors. Nat Biotech 26:1301–1308

    Article  CAS  Google Scholar 

  • Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavallini E, Zenoni S, Finezzo L, Guzzo F, Zamboni A, Avesani L (2014) Functional diversification of grapevine MYB5a and MYB5b in the control of flavonoid biosynthesis in a petunia anthocyanin regulatory mutant. Plant Cell Physiol 55:517–534

    Article  CAS  PubMed  Google Scholar 

  • Cavallini E, Matus JT, Finezzo L, Zenoni S, Loyola R, Guzzo F (2015) The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol 167:1448–1470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chagné D, Lin-Wang K, Espley RV, Volz RK, How NM, Rouse S (2013) An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol 161:225–239

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui B, Hu Z, Zhang Y, Hu J, Yin W, Feng Y (2016) Anthocyanins and flavonols are responsible for purple color of Lablab purpureus (L.) sweet pods. Plant Physio Biochem 103:183–190

    Article  CAS  Google Scholar 

  • Davies KM, Albert NW, Schwinn KE (2012) From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct Plant Biol 39:619–638

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elomaa P, Uimari A, Mehto M, Albert VA, Laitinen RAE, Teeri TH (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 133:1831–1842

    Article  CAS  PubMed  PubMed Central  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 49:414–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  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 232:245–255

    Article  CAS  PubMed  Google Scholar 

  • Feng K, Xu ZS, Que F, Liu JX, Wang F, Xiong AS (2018) An R2R3MYB transcription factor, OjMYB1, functions in anthocyanin biosynthesis in Oenanthe javanica. Planta 247:301–315

    Article  CAS  PubMed  Google Scholar 

  • Fraser LG, Seal AG, Montefiori M, McGhie TK, Tsang GK, Datson PM (2013) An R2R3 MYB transcription factor determines red petal colour in an Actinidia (kiwifruit) hybrid population. BMC Genom 14:28

    Article  CAS  Google Scholar 

  • Griesbach RJ, Klein TM (1993) In situ genetic complementation of a flower color mutant in Doritis pulherrima (Orchidaceae). Lindleyana 8:223–226

    Google Scholar 

  • He Q, Zhang ZF, Zhang LG (2016) Anthocyanin accumulation, antioxidant ability and stability, and a transcriptional analysis of anthocyanin biosynthesis in purple heading Chinese cabbage (Brassica rapa L. ssp. Pekinensis). J Food Chem 64:132–145

    Article  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 62:2465–2483

    Article  CAS  PubMed  Google Scholar 

  • Hou DX (2003) Potential mechanisms of cancer chemoprevention by anthocyanins. Curr Mol Med 3:149–159

    Article  CAS  PubMed  Google Scholar 

  • Hsu CC, Chen YY, Tsai WC, Chen WH, Chen HH (2015) Three R2R3-MYB transcription factors regulate distinct floral pigmentation patterning in Phalaenopsis orchids. Plant Physiol 133:1831–1842

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang YF, Vialet S, Guiraud JL, Torregrosa L, Bertrand Y, Cheynier V (2014) A negative MYB regulator of proanthocyanidin accumulation, identified through expression quantitative locus mapping in the grape berry. New Phytol 201:795–809

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Khaldun ABM, Lv H, Du L, Zhang C, Wang Y (2016) Isolation and functional characterization of a R2R3-MYB regulator of the anthocyanin biosynthetic pathway from Epimedium sagittatum. Plant Cell Rep 35:883–894

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Shen J, Liu H, Li F, Ding N, Gao C (2015) Small tandem target mimic-mediated blockage of microRNA858 induces anthocyanin accumulation in tomato. Planta 242:283–293

    Article  CAS  PubMed  Google Scholar 

  • Jin W, Wang H, Li M, Wang J, Yang Y, Zhang X (2016) The R2R3 MYB transcription factor PavMYB10. 1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L.). Plant Biotechnol J 14:2120–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung CS, Griffiths HM, De Jong DM, Cheng S, Bodis M (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 120:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadomura-Ishikawa Y, Miyawaki K, Takahashi A (2015) RNAi-mediated silencing and overexpression of the FaMYB1 gene and its effect on anthocyanin accumulation in strawberry fruit. Biol Plantarum 59:677–685

    Article  CAS  Google Scholar 

  • Kee ES, Naing AH, Lim SH, Han JS, Kim CK (2016) MYB transcription factor isolated from Raphanus sativus enhances anthocyanin accumulation in chrysanthemum cultivars. 3 Biotech 6:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiferle C, Fantini E, Bassolino L, Povero G, Spelt C, Buti S et al (2015) Tomato R2R3-MYB proteins SlANT1 and SlAN2: same protein activity, different roles. PLoS ONE 10:e0136365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klatsky AL (2002) Alcohol and cardiovascular diseases: a historical overview. Ann N Y Acad Sci 957:7–15

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kortstee AJ, Khan SA, Helderman C, Trindade LM, Wu Y, Visser RG (2011) Anthocyanin production as a potential visual selection marker during plant transformation. Transgenic Res 20:1253–1264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Lai B, Li XJ, Hu B, Qin YH, Huang XM, Wang HC (2014) LcMYB1 is a key determinant of differential anthocyanin accumulation among genotypes, tissues, developmental phases and ABA and light stimuli in Litchi chinensis. PLoS ONE 9:e86293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Laitinen RAE, Ainasoja M, Broholm SK, Teeri TH, Elomaa P (2008) Identification of target genes for a MYB-type anthocyanin regulator in Gerbera hybrida. J Exp Bot 59:3691–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li JG, Li HL, Peng SQ (2011) Three r2r3-myb transcription factor genes from capsicum annuum showing differential expression during fruit ripening. Afr J Biotechnol 10:8267–8274

    Article  CAS  Google Scholar 

  • Li L, Ban Z, Li X, Wu M, Wang A, Jiang Y (2012) Differential expression of anthocyanin biosynthetic genes and transcription factor PcMYB10 in pears (Pyruscommunis L.). PLoS ONE 7:e46070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Qui J, Yang G, Haung S, Yin J (2016) Isolation and characterization of a R2R3-MYB transcription factor gene related to anthocyanin biosynthesis in the spathes of Anthurium andraeanum (Hort.). Plant Cell Rep 35:2151–2165

    Article  CAS  PubMed  Google Scholar 

  • Li C, Qui J, Ding L, Huang M, Huang S, Yang G (2017) Anthocyanin biosynthesis regulation of DhMYB2 and DhbHLH1 in Dendrobium hybrids petals. Plant Physiol Biochem 112:335–345

    Article  CAS  PubMed  Google Scholar 

  • Lila MA (2004) Anthocyanins and human health: an in vitro investigative approach. J Biomed Biotechnol 5:306–313

    Article  Google Scholar 

  • Lim SH, Song JH, Kim DH, Kim JK, Lee JY, Kim YM (2016) Activation of anthocyanin biosynthesis by expression of the radish R2R3-MYB transcription factor gene RsMYB1. Plant Cell Rep 35:641–653

    Article  CAS  PubMed  Google Scholar 

  • Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10:50

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X, Xiang L, Yin X, Grierson D, Li F, Chen K (2015) The identification of a MYB transcription factor controlling anthocyanin biosynthesis regulation in chrysanthemum flowers. Sci Hortic 194:278–285

    Article  CAS  Google Scholar 

  • Liu Y, Lin-Wang K, Espley RV, Wang L, Yang H, Yu B (2016) Functional diversification of the potato R2R3 MYB anthocyanin activators AN1, MYBA1, and MYB113 and their interaction with basic helix-loop-helix cofactors. J Exp Bot 67:2159–2176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowry DB, Sheng CC, Lasky JR, Willis JH (2012) Five anthocyanin polymorphisms are associated with an R2R3-MYB cluster in Mimulus guttatus (Phrymaceae). Am J Bot 99:82–91

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Pooler M, Griesbach R (2008) Ratio of Myc and Myb transcription factors regulates anthocaynin production in orchid flowers. J Am Soc Hortic Sci 133:133–138

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15:1689–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco (2014) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J Exp Bot 65:401–417

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Wang JR, Wang GD, Liang XQ, Li XD, Meng QW (2015) An R2R3-MYB gene, LeAN2, positively regulated the thermo-tolerance in transgenic tomato. J Plant Physiol 175:1–8

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 47:457–470

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naing AH, Ai TN, Jeon SM, Park KI, Lim KM, Kim CK (2015) Expression of RsMYB1 in chrysanthemum regulates key anthocyanin biosynthetic genes. Elect J of Biotechnol 18:359–364

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakatsuka A, Yamagishi M, Nakano M, Tasaki K, Kobayashi N (2009) Light-induced expression of basic helix–loop–helix genes involved in anthocyanin biosynthesis in flowers and leaves of Asiatic hybrid lily. Sci Hortic 121:84–91

    Article  CAS  Google Scholar 

  • Nishijima T, Morita Y, Sasaki K, Nakayama M, Yamaguchi H, Ohtsubo N (2013) A torenia (Torenia fournieri Lind. ex Fourn.) novel mutant ‘flecked’ produces variegated flowers by insertion of a DNA transposon into an R2R3-MYB gene. J Japanese Soc Horticult Sci 82:39–50

    Article  CAS  Google Scholar 

  • Niu SS, Xu CJ, Zhang WS, Zhang B, Li X, Lin-Wang K (2009) Coordinated regulation of anthocyanin biosynthesis in Chinese bayberry (Myrica rubra) fruit by a R2R3 MYB transcription factor. Planta 6:101–112

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Park NI, Xu H, Li X, Jang IH, Park S, Ahn GH (2011) Anthocyanin accumulation and expression of anthocyanin biosynthetic genes in radish (Raphanus sativus). J Agri Food Chem 59:6034–6039

    Article  CAS  Google Scholar 

  • Pérez-Díaz JR, Pérez-Díaz J, Madrid-Espinoza J, González-Villanueva E, Moreno Y, Ruiz-Lara S (2015) New member of the R2R3-MYB transcription factors family in grapevine suppresses the anthocyanin accumulation in the flowers of transgenic tobacco. Plant Mol Biol 90:63–76

    Article  PubMed  CAS  Google Scholar 

  • Pervaiz S (2003) Resveratrol: from grapevines to mammalian biology. FASEB J 17:1975–1985

    Article  CAS  PubMed  Google Scholar 

  • Pierantoni L, Dondini L, Franceschi PD, Musacchi S, Winkel BSJ, Sansavini S (2010) Mapping of an anthocyanin-regulating MYB transcription factor and its expression in red and green pear, Pyrus communis. Plant Physiol Bioch 48:1020–1026

    Article  CAS  Google Scholar 

  • Quattrocchio F, Wing JF, Leppen HTC, Mol JNM, Koes RE (1993) Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5:1497–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quattrocchio F, Wing JF, van der Woude K, Mol JNM, 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 13:475–488

    Article  CAS  PubMed  Google Scholar 

  • Rahim MA, Busatto N, Trainotti L (2014) Regulation of anthocyanin biosynthesis in peach fruits. Planta 240:913–929

    Article  CAS  PubMed  Google Scholar 

  • Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70

    Article  CAS  PubMed  Google Scholar 

  • Ravaglia D, Espley RV, Henry-Kirk RA, Andreotti C, Ziosi V, Hellens RP (2013) Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biol 13:68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvatierra A, Pimentel P, Moya-León MA, Herrera R (2013) Increased accumulation of anthocyanins in Fragaria chiloensis fruits by transient suppression of FcMYB1 gene. Phytochemistry 90:25–36

    Article  CAS  PubMed  Google Scholar 

  • Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwinn KE, Boase MR, Bradley JM, Lewis DH, Deroles SC, Martin CR (2014) MYB and bHLH transcription factor transgenes increase anthocyanin pigmentation in petunia and lisianthus plants, and the petunia phenotypes are strongly enhanced under field conditions. Front Plant Sci 5:603

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwinn KE, Ngo H, Kenel F, Brummell DA, Albert NW, McCallum JA (2016) The onion (Allium cepa L.) R2R3-MYB gene MYB1 regulates anthocyanin biosynthesis. Front Plant Sci 7:1865

    Article  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE, Jameson PE (2011) The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytol 189:602–615

    Article  CAS  PubMed  Google Scholar 

  • Shen X, Zhao K, Liu L, Zhang K, Yuan H, Liao X (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physio 55:862–880

    Article  CAS  Google Scholar 

  • Sooriyapathirana S, Khan A, Sebolt A, Wang D, Bushakra J, Lin-Wang K (2010) QTL analysis and candidate gene mapping for skin and flesh colour in sweet cherry fruit (Prunus avium L.). Tree Genet Genomes 6:821–832

    Article  Google Scholar 

  • Spelt C, Quattrocchio F, Mol JNM, Koes R (2000) Anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12:1619–1631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starkevič P, Paukštytė J, Kazanavičiūtė V, Denkovskienė E, Stanys V, Bendokas V (2015) Expression and anthocyanin biosynthesis-modulating potential of sweet cherry (Prunus avium L.) MYB10 and bHLH genes. PLoS ONE 10:e0126991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun SS, Gugger PF, Wang QF, Chen JM (2016) Identification of a R2R3-MYB gene regulating anthocyanin biosynthesis and relationships between its variation and flower color difference in lotus (Nelumbo Adans.). PeerJ 4:e2369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki K, Suzuki T, Nakatsuka T, Dohra H, Yamagishi M, Matsuyama K (2016) RNA-seq-based evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies (Lilium spp.). BMC Genom 17:611

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telias A, Lin-Wang K, Stevenson DE, Cooney JM, Hellens RP, Allan AC (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11:93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Tian J, Peng Z, Zhang J, Song TT, Wan HH, Zhang ML (2015) McMYB10 regulates coloration via activating McF3′H and later structural genes in ever-red leaf crabapple. Plant Biotechnol J 13:948–961

    Article  CAS  PubMed  Google Scholar 

  • Vimolmangkang S, Han Y, Wei G, Korban SS (2013) An apple MYB transcription factor, MdMYB3, is involved in regulation of anthocyanin biosynthesis and flower development. BMC Plant Biol 13:176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walker AR, Elizabeth L, Jochen B, Debra AJ, Mc D, Mark RT (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J 49:772–785

    Article  CAS  PubMed  Google Scholar 

  • Wu XM, Lim SH, Yang WC (2003) Characterization, expression and phylogenetic study of R2R3-MYB genes in orchid. Plant Mol Biol 51:959–972

    Article  CAS  PubMed  Google Scholar 

  • Xie QL, Hu ZL, Zhang YJ, Tian SB, Wang ZJ, Zhao ZP (2014) Accumulation and molecular regulation of anthocyanin in purple tumorous stem mustard (Brassica juncea var. tumida Tsen et Lee). J Agric Food Chem 62:7813–7821

    Article  CAS  PubMed  Google Scholar 

  • Xu ZS, Feng K, Que F, Wang F, Xiong AS (2017) A MYB transcription factor, DcMYB6, is involved in regulating anthocyanin biosynthesis in purple carrot taproots. Sci Rep 7:4532

    Article  CAS  Google Scholar 

  • Yamagishi M (2011) Oriental hybrid lily Sorbonne homologue of LhMYB12 regulates anthocyanin biosyntheses in flower tepals and tepal spots. Mol Breed 28:381–389

    Article  CAS  Google Scholar 

  • Yamagishi M (2016) A novel R2R3-MYB transcription factor regulates light-mediated floral and vegetative anthocyanin pigmentation patterns in Lilium regale. Mol Breed 36:1–14

    Article  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 51:463–474

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi M, Yoshida Y, Nakayama M (2012) The transcription factor LhMYB12 determines anthocyanin pigmentation in the tepals of Asiatic hybrid lilies (Lilium spp.) and regulates pigment quantity. Mol Breed 30:913–925

    Article  CAS  Google Scholar 

  • Yamagishi M, Toda S, Tasaki K (2014) The novel allele of the LhMYB12 gene is involved in splatter-type spot formation on the flower tepals of Asiatic hybrid lilies (Lilium spp.). New Phytol 201:1009–1020

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Ma D, Constabel CP (2015) The MYB182 protein downregulates proanthocyanidin and anthocyanin biosynthesis in poplar by repressing both structural and regulatory flavonoid genes. Plant Physiol 167:693–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Chiu LW, Li L (2009) Transcriptional regulation of anthocyanin biosynthesis in red cabbage. Planta 230:1141–1153

    Article  CAS  PubMed  Google Scholar 

  • Yuan YW, Sagawa JM, Frost L, Vela JP, Bradshaw HD (2014) Transcriptional control of floral anthocyanin pigmentation in monkeyflowers (Mimulus). New Phytol 204:1013–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan YW, Rebocho AB, Sagawa JM, Stanley LE, Bradshaw HD (2016) Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species. Proc Natl Acad Sci USA 113:2448–2453

    Article  CAS  PubMed  Google Scholar 

  • Zhang YJ, Hu ZL, Chu GH, Huang C, Tian SB, Zhao ZP (2014) Anthocyanin accumulation and molecular analysis of anthocyanin biosynthesis-associated genes in eggplant (Solanum melongena L.). J Agric Food Chem 62:2906–2912

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Hu Z, Zhu M, Zhu Z, Wang Z, Tian S (2015a) Anthocyanin accumulation and molecular analysis of correlated genes in Purple Kohlrabi (Brassica oleracea var. gongylodes L.). J Agric Food Chem 63:4160–4169

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Li DW, Jin JH, Yin YX, Zhang HX, Chai WG (2015b) VIGS approach reveals the modulation of anthocyanin biosynthetic genes by CaMYB in chili pepper leaves. Front Plant Sci 6:500

    PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Chu G, Hu Z, Gao Q, Cui B, Tian S (2016) Genetically engineered anthocyanin pathway for high health-promoting pigment production in eggplant. Mol Breed 36:54

    Article  CAS  Google Scholar 

  • Zhang Q, Hao R, Xu Z, Yang W, Wang J, Cheng T (2017) Isolation and functional characterization of a R2R3-MYB regulator of Prunus mume anthocyanin biosynthetic pathway. Plant Cell Tiss Organ Cult 131:417–429

    Article  CAS  Google Scholar 

  • Zhou Y, Zhou H, Lin-Wang K, Vimolmangkang S, Espley RV, Wang L (2014) Transcriptome analysis and transient transformation suggest an ancient duplicated MYB transcription factor as a candidate gene for leaf red coloration in peach. BMC Plant Biol 14:388

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou H, Lin-Wang K, Wang H, Gu C, Dare AP, Espley RV (2015) Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant J 82:105–121

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Peng Q, Zhao J, Owiti A, Ren F, Liao L (2016) Multiple R2R3-MYB transcription tactors involved in the regulation of anthocyanin accumulation in peach flower. Front Plant Sci 7:1557

    PubMed  PubMed Central  Google Scholar 

  • Zhu L, Shan H, Chen S, Jiang J, Gu C, Zhou G (2013) The heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB1 alters lignin composition and represses flavonoid synthesis in Arabidopsis thaliana. PLoS ONE 8:e65680

    Article  CAS  PubMed  PubMed Central  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 40:22–34

    Article  CAS  PubMed  Google Scholar 

  • Zuluaga DL, Gonzali S, Loreti E, Pucciariello C, Degl’Innocenti ED, Guidi L (2008) Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. Funct Plant Biol 35:606–618

    Article  CAS  Google Scholar 

  • Zvi MMB, Shklarman E, Masci T, Kalev H, Debener T, Shafir S (2012) PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. New Phytol 195:334–335

    Article  CAS  Google Scholar 

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Acknowledgements

This work was carried out with the support of “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01368505)” Rural Development Administration, Republic of Korea. We sincerely thank to Dr. Khaing Thandar Soe (Seoul National University, South Korea) for her kind assistance in collection of difficult-to-access articles.

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  1. Department of Horticultural Science, Kyungpook National University, Daegu, 41566, Republic of Korea

    Aung Htay Naing & Chang Kil Kim

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  1. Aung Htay Naing
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  2. Chang Kil Kim
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AHN collected the literature and wrote the manuscript; CKK advised and assisted with the writing of the manuscript.

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Correspondence to Chang Kil Kim.

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Naing, A.H., Kim, C.K. Roles of R2R3-MYB transcription factors in transcriptional regulation of anthocyanin biosynthesis in horticultural plants. Plant Mol Biol 98, 1–18 (2018). https://doi.org/10.1007/s11103-018-0771-4

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  • DOI: https://doi.org/10.1007/s11103-018-0771-4

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