Heterologous expression of gentian MYB1R transcription factors suppresses anthocyanin pigmentation in tobacco flowers

Plant Cell Reports

Volumn 32, Issue 12, 2013, Pages 1925-1937

  Nakatsuka, Takashi ^a   Yamada, Eri ^b   Saito, Misa ^b   Fujita, Kohei ^b   Nishihara, Masahiro ^b  

^a SHIZUOKA UNIVERSITY   (Japan)

^b IWATE BIOTECHNOLOGY RESEARCH CENTER   (Japan)

Author keywords

Antagonistic transcription factor; Anthocyanin biosynthesis; Floral pigmentation; Japanese gentian; MYB1R

Indexed keywords

GENTIANA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

ANTHOCYANIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENTIAN; METABOLISM; MOLECULAR GENETICS; PHENOTYPE; PHYLOGENY; PIGMENTATION; PLANT GENE; PROMOTER REGION; PROTEIN BINDING; SEQUENCE ALIGNMENT; TIME; TOBACCO; TRANSGENIC PLANT; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; ANTHOCYANINS; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENTIANA; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYLOGENY; PIGMENTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ALIGNMENT; TIME FACTORS; TOBACCO; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84888033320     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1504-4     Document Type: Article

References (55)

1. Aharoni A, De Vos CH, Wein M, Sun Z, Greco R, Kroon A, Mol JN, O'Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28: 319-332.
2. 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.
3. Baudry A, Heim MA, 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: 366-380.
4. Baudry A, Caboche M, Lepiniec 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: 768-779.
5. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2394.
6. Chen B, Wang X, Hu Y, Wang Y, Lin Z (2004) Ectopic expression of a c1-1 allele from maize inhibits pigment formation in the flower of transgenic tobacco. Mol Biotechnol 26: 187-192.
7. Cocciolone SM, Nettleton D, Snook ME, 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: 225-235.
8. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
9. Davies K (2009) Modifying anthocyanin production in flowers. In: Gould K, Davies K, Winefield C (eds) Anthocyanins, biosynthesis, functions, and applications. Springer, New York, pp 49-83.
10. Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul JM, Alboresi A, Weisshaar B, Lepiniec L (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 55: 940-953.
11. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trend Plant Sci 15: 573-581.
12. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66: 94-116.
13. Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543-553.
14. Grotewold E, Sainz MB, Tagliani L, Hernandez JM, Bowen B, Chandler VL (2000) Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLH cofactor R. Proc Natl Acad Sci USA 97: 13579-13584.
15. Han Y, Vimolmangkang S, Soria-Guerra RE, Korban SS (2012) Introduction of apple ANR genes into tobacco inhibits expression of both CHI and DFR genes in flowers, leading to loss of anthocyanin. J Exp Bot 63: 2437-2447.
16. Hanumappa H, Choi G, Ryu S, Choi G (2007) Modulation of flower colour by rationally designed dominant-negative chalcone synthase. J Exp Bot 58: 2471-2478.
17. Hartmann U, Valentine WJ, Christie JM, Hays J, Jenkins GI, Weisshaar B (1998) Identification of UV/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system. Plant Mol Biol 36: 741-754.
18. Hemm MR, Herrmann KM, Chapple C (2001) AtMYB4: a transcription factor general in the battle against UV. Trend Plant Sci 6: 135-136.
19. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that induce the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733-739.
20. Horsch RB, Fry JE, Hoffmann NL, Eicholtz D, Rogers SG, Fraley RT (1985) A simple method for transferring genes into plants. Science 227: 1229-1231.
21. 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: 6150-6161.
22. Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trend Plant Sci 10: 236-242.
23. Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC (2012) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10: 50.
24. Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trend Genet 13: 67-73.
25. 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: 954-967.
26. 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: 1083-1096.
27. Mitsuda N, Hiratsu K, Todaka D, Nakashima K, Yamaguchi-Shinozaki K, Ohme-Takagi M (2006) Efficient production of male and female sterile plants by expression of a chimeric repressor in Arabidopsis and rice. Plant Biotechnol J 4: 325-332.
28. Nakamura N, Fukuchi-Mizutani M, Miyazaki K, Suzuki K, Tanaka Y (2006) RNAi suppression of the anthocyanin synthase gene in Torenia hybrid yields white flowers with higher frequency and better stability than antisense ad sense suppression. Plant Biotechnol 23: 13-17.
29. 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: 1309-1318.
30. Nakatsuka T, Abe Y, Kakizaki Y, Yamamura S, Nishihara M (2007) Production of red-flowered plants by genetic engineering of multiple flavonoid biosynthetic genes. Plant Cell Rep 26: 1951-1959.
31. Nakatsuka T, Haruta KS, 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: 1818-1829.
32. Nakatsuka T, Saito M, Yamada E, Nishihara M (2011) Production of picotee-type flowers in Japanese gentian by CRES-T. Plant Biotechnol 28: 173-180.
33. 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: 6505-6517.
34. Nishihara M, Nakatsuka T (2011) Genetic engineering of flavonoid pigments to modify flower color in floricultural plants. Biotechnol Lett 33: 433-441.
35. Nishihara M, Nakatsuka T, Yamamura S (2005) Flavonoid components and flower color change in transgenic tobacco plants by suppression of chalcone isomerase gene. FEBS Lett 579: 6074-6078.
36. Pattanaik S, Kong Q, Zaitlin D, Werkman JR, Xie CH, Patra B, Yuan L (2010) Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco. Planta 231: 1061-1076.
37. 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: 1433-1444.
38. Quattrocchio F, Baudry A, Lepiniec L, Grotewold E (2006) The regulation of flavonoid biosynthesis. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 97-122.
39. Ramsay NA, Glover (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trend Plant Sci 10: 63-70.
40. Salvatierra A, Pimentel P, Moya-Leon MA, Herrera R (2013) Increased accumulation of anthocyanins in Fragaria chiloensis fruits by transient suppression of FcMYB1 gene. Phytochemistry 90: 25-36.
41. Shikata M, Narumi T, Yamaguchi H, Sasaki K, Aida R, Oshima Y, Takiguchi Y, Ohme-Takagi M, Mitsuda N, Ohtsubo N (2011) Efficient production of novel floral traits in torenia by collective transformation with chimeric repressors of Arabidopsis transcription factors. Plant Biotechnol 28: 189-199.
42. 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: 1619-1632.
43. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456.
44. 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: 660-677.
45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
46. Tanaka Y, Brugliera F, Kalc G, Senior M, Dyson B, Nakamura N, Katsumoto Y, Chandler S (2010) Flower color modification by engineering of the flavonoid biosynthetic pathway: practical perspectives. Biosci Biotechnol Biochem 74: 1760-1769.
47. Tsuda S, Fukui Y, Nakamura N, Katsumoto Y, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Ohira K, Ueyama Y, Ohkawa H, Holton TA, Kusumi T, Tanaka Y (2004) Flower color modification of Petunia hybrid commercial varieties by metabolic engineering. Plant Biotechnol 21: 377-386.
48. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113-1116.
49. Winkel BSJ (2006) The biosynthesis of flavonoid. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 71-96.
50. Xu W, Grain D, Gourrierec JL, Harscoët E, Berger A, Jauvion V, Scagnelli A, Berger N, Bidzinski P, Kelemen Z, Salsac F, Baudry A, Routaboul JM, Lepiniec L, Dubos C (2013) Regulation of flavonoid biosynthesis involves an unexpected complex transcriptional regulation of TT8 expression, in Arabidopsis. New Phytol 198: 59-70.
51. Yuan YW, Sagawa JM, Young RC, Christensen BJ (2013) Genetic dissection of a major anthocyanin QTL contributing to pollinator-mediated reproductive isolation between sister species of Mimulus. Genetics 194: 255-263.
52. Zhang W, Ning G, Lv H, Liao L, Bao M (2009) Single MYB-type transcription factor AtCAPRICE: a new efficient tool to engineer the production of anthocyanin in tobacco. Biochem Biophy Res Comm 388: 742-747.
53. Zhu HF, Fitzsimmons K, Khandelwal A, Kranz RG (2009) CPC, a single-repeat R3 MYB, is a negative regulator of anthocyanin biosynthesis in Arabidopsis. Mol Plant 2: 790-802.
54. Zhu L, Shan H, Chen S, Jiang J, Gu C, Zhou G, Chen Y, Song A, Chen F (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.
55. 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.