A novel R2R3-MYB transcription factor regulates light-mediated floral and vegetative anthocyanin pigmentation patterns in Lilium regale

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• 作者：Masumi Yamagishi
• 关键词：Basic helix ; loop ; helix 2 ; Bud ; blush ; Color pattern ; Lily ; LrMYB15 ; Transcriptional regulation
• 刊名：Molecular Breeding
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：36
• 期：1
• 全文大小：957 KB
• 参考文献：Abe H, Nakano M, Nakatsuka A, Nakayama M, Koshioka M, Yamagishi M (2002) Genetic analysis of floral anthocyanin pigmentation traits in Asiatic hybrid lily using molecular linkage maps. Theor Appl Genet 105:1175–1182CrossRef PubMed
  Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in Petunia. J Exp Bot 60:2191–2202PubMedCentral CrossRef PubMed
  Albert NW, Arathoon S, Collette VE, Schwinn KE, Jameson PE, Lewis DH, Zhang H, Davies KM (2010) Activation of anthocyanin synthesis in Cymbidium orchids: variability between known regulators. Plant Cell Tissue Organ Cult 100:355–360CrossRef
  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 65:771–784CrossRef PubMed
  Asano Y (1989) Lilium L. In: Tsukamoto Y (ed) The grand dictionary of horticulture, vol 5. Syogakukan, Tokyo, pp 198–209 (in Japanese)
  Bai Y, Pattanaik S, Patra B, Werkman JR, Xie CH, Yuan L (2011) Flavonoid-related basic helix–loop–helix regulators, NtAn1a and NtAn1b, of tobacco have originated from two ancestors and are functionally active. Planta 234:363–375CrossRef PubMed
  Baudry A, Caboche M, Lepinlec L (2006) TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana. Plant J 46:768–779CrossRef PubMed
  Bird R (1991) Lilies. Chartwell Books Inc., Secaucus
  Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Opin Plant Biol 8:272–279CrossRef PubMed
  Comber HF (1949) A new classification of the genus Lilium. In: Lily yearbook, vol 13. Royal Horticultural Society, London, pp 85–105
  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 39:619–638CrossRef
  Du J, Rietman H, Vleeshouwers V (2014) Agroinfiltration and PVX agroinfiltration in potato and Nicotiana benthamiana. J Vis Exp 83:e50971PubMed
  Ferreyra MLF, Rius SP, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222
  Fraser LG, Seal AG, Montefiori M, McGhie TK, Tsang GK, Datson PM, Hilario E, Marsh HE, Dunn JK, Hellens RP, Davies KM, McNeilage MA, De Silva HN, Allan AC (2013) An R2R3 MYB transcription factor determines red petal colour in an Actinidia (kiwifruit) hybrid population. BMC Genom 14:28CrossRef
  Glover BJ, Walker RH, Moyroud E, Brockington SF (2013) How to spot a flower. New Phytol 197:687–689CrossRef PubMed
  Gong ZZ, 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 formation. Mol Gen Genet 262:65–72PubMed
  Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827CrossRef PubMed
  Gould KS (2004) Nature’s Swiss Army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotech 2004:314–320CrossRef
  Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780CrossRef PubMed
  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 62:2465–2483CrossRef PubMed
  Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231CrossRef
  Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18:477–483CrossRef PubMed
  Jiang R, Tian J, Song T, Zhang J, Yao Y (2014) The Malus crabapple transcription factor McMYB10 regulates anthocyanin biosynthesis during petal coloration. Sci Hortic 166:42–49CrossRef
  Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) MYB-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215:924–933CrossRef PubMed
  Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242CrossRef PubMed
  Koseki M, Goto K, Masuta C, Kanazawa A (2005) The star-type color pattern in Petunia hybrida ‘Red Star’ flowers is induced by sequence-specific degradation of chalcone synthase RNA. Plant Cell Physiol 46:1879–1883CrossRef PubMed
  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 193–194:136–147CrossRef PubMed
  Lai Y, Li H, Yamagishi M (2013) A review of target gene specificity of flavonoid R2R3-MYB transcription factors and a discussion of factors contributing to the target gene selectivity. Frontiers Biol 8:577–598CrossRef
  Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948CrossRef PubMed
  Leslie AC (1982) The international lily register, 3rd edn. The Royal Horticultural Society, London
  Lim KB, van Tuyl JM (2006) Lily: Lilium hybrids. In: Anderson NO (ed) Flower breeding and genetics: issues, challenges and opportunities for the 21st century. Springer, Dordrecht, pp 513–532
  Lim KB, Barba-Gonzalez R, Zhou S, Ramanna MS, van Tuyl JM (2008) Interspecific hybridization in lily (Lilium): Taxonomic and commercial aspects of using species hybrids in breeding. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology, vol V. Global Science Books Ltd., Kagawa, pp 146–151
  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408CrossRef PubMed
  Maier A, Schrader A, Kokkelink L, Falke C, Welter B, Iniesto E et al (2013) Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74:638–651CrossRef PubMed
  Morita Y, Ryoko S, Ban Y, Tanikawa N, Kuchitsu K, Ando T et al (2012) Tandemly arranged chalcone synthase A genes contribute to the spatially regulated expression of siRNA and the natural bicolor floral phenotype in Petunia hybrida. Plant J 70:739–749CrossRef PubMed
  Nakatsuka A, Izumi Y, Yamagishi M (2003) Spatial and temporal expression of chalcone synthase and dihydroflavonol 4-reductase genes in the Asiatic hybrid lily. Plant Sci 165:759–767CrossRef
  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 121:84–91CrossRef
  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 63:6505–6517PubMedCentral CrossRef PubMed
  Nørbæk R, Kondo T (1999) Anthocyanins from flowers of Lilium (Liliaceae). Phytochem 50:1181–1184CrossRef
  Ohno S, Hosokawa M, Kojima M, Kitamura Y, Hoshino A, Tatsuzawa F et al (2011) Simultaneous post-transcriptional gene silencing of two different chalcone synthase genes resulting in pure white flowers in the octoploid dahlia. Planta 234:945–958CrossRef PubMed
  Pattanaik S, Kong Q, Zaitlin D, Werkman JR, Xie CH, Patra B et al (2010) Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco. Planta 231:1061–1076CrossRef PubMed
  Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181:219–229CrossRef PubMed
  Piazza P, Procissi A, Jenkins GI, Tonelli C (2002) Members of the c1/pl1 regulatory gene family mediate the response of maize aleurone and mesocotyl to different light qualities and cytokinins. Plant Physiol 128:1077–1086PubMedCentral CrossRef PubMed
  Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J et al (1999) Molecular analysis of the anthocyanin2 gene of Petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444PubMedCentral CrossRef PubMed
  Sainz MB, Grotewold E, Chandler VL (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 9:611–625PubMedCentral CrossRef PubMed
  Saito R, Fukuta N, Ohmiya A, Itoh Y, Ozeki Y, Kuchitsu K et al (2006) Regulation of anthocyanin biosynthesis involved in the formation of marginal picotee petals in Petunia. Plant Sci 170:828–834CrossRef
  Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMed
  Schaefer HM, Schaefer V, Levey DJ (2004) How plant–animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584CrossRef
  Schwinn K, Venail J, Sang Y, Mackay S, Alm V, Butelli E et al (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851PubMedCentral CrossRef PubMed
  Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE, Jameson PE et al (2011) The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytol 189:602–615CrossRef PubMed
  Smyth DR, Kongsuwan K, Wisudharomn S (1989) A survey of C-band patterns in chromosomes of Lilium (Liliaceae). Plant Syst Evol 163:53–69CrossRef
  Spelt C, Quattrocchio F, Mol JN, Koes R (2000) anthocyanin1 of petunia encodes a basic helix–loop–helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12:1619–1632PubMedCentral CrossRef PubMed
  Suzuki K, Tasaki K, Yamagishi M (2015) Two distinct spontaneous mutations involved in white flower development in Lilium speciosum. Mol Breed 35:193CrossRef
  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 142:1216–1232PubMedCentral CrossRef PubMed
  Tateishi N, Ozaki Y, Okubo H (2010) White marginal picotee formation in the petals of Camellia japonica ‘Tamanoura’. J Jpn Soc Hort Sci 79:207–214CrossRef
  Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493PubMedCentral CrossRef PubMed
  Yamagishi M (2011) Oriental hybrid lily Sorbonne homologue of LhMYB12 regulates anthocyanin biosyntheses in flower tepals and tepal spots. Mol Breed 28:381–389CrossRef
  Yamagishi M (2013) How genes paint lily flowers: regulation of colouration and pigmentation patterning. Sci Hortic 163:27–37CrossRef
  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 51:463–474CrossRef PubMed
  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 30:913–925CrossRef
  Yamagishi M, Ihara H, Arakawa K, Toda S, Suzuki K (2014a) The origin of the LhMYB12 gene, which regulates anthocyanin pigmentation of tepals, in oriental and Asiatic hybrid lilies (Lilium spp.). Sci Hortic 174:119–125CrossRef
  Yamagishi M, Toda S, Tasaki K (2014b) 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 201:1009–1020CrossRef PubMed
  Yuan Y-W, Sagawa JM, Frost L, Vela JP, Bradshaw HD Jr (2014) Transcriptional control of floral anthocyanin pigmentation in monkeyflowers (Mimulus). New Phytol 204:1013–1027PubMedCentral CrossRef PubMed
  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 40:22–34CrossRef PubMed
  Zoratti L, Karppinen K, Escobar AL, Häggman H, Jaakola L (2014) Light-controlled flavonoid biosynthesis in fruits. Front Plant Sci 5:534PubMedCentral CrossRef PubMed
  
• 作者单位：Masumi Yamagishi (1)
  
  1. Research Faculty of Agriculture, Hokkaido University, N9W9, Kita-ku, Sapporo, 060-8589, Japan
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Sciences
  
• 出版者：Springer Netherlands
• ISSN：1572-9788

文摘

Color patterns in angiosperm flowers are produced by spatially and temporally restricted deposition of pigments. Many Lilium species show anthocyanin pigmentation of the whole tepal, which is regulated by the MYB12/basic helix-loop-helix 2 (bHLH2) transcription factor complex. However, in Lilium regale pigment deposition is restricted to light-exposed surfaces of the flower buds, leaves, and bracts. Investigation of how the unique color patterns of L. regale are regulated led to the identification and isolation of a novel R2R3-MYB gene, LrMYB15. In stable and transient transformation assays in tobacco, LrMYB15 stimulated transcription of anthocyanin biosynthesis genes, indicating that it is involved in the positive regulation of anthocyanins. In L. regale, anthocyanin biosynthesis genes and LrMYB15 were expressed in the outer tepals, leaves, and bracts that accumulated anthocyanin pigments. In contrast, LrbHLH2, another regulatory gene for anthocyanin biosynthesis, was transcribed in all organs irrespective of anthocyanin accumulation. These results indicate that LrMYB15 principally determines the unique anthocyanin color patterns of L. regale. In addition, LrMYB15 transcription ceased completely when plants were kept in shaded conditions and the colors of the flower buds faded, indicating that transcription of this gene is under the control of light. R2R3-MYB genes that regulate light-induced anthocyanin accumulation on exposed petal surfaces have been isolated in eudicots. The results here indicate that R2R3-MYB genes exhibiting similar (but not identical) functions are conserved between monocots and eudicots and that transcriptional regulation is a major mechanism for generating restricted pigment deposition in the flowers of a wide range of angiosperm species.