Skip to main content
SpringerLink
Log in

Genome-wide analysis of the R2R3-MYB transcription factor gene family in sweet orange (Citrus sinensis)

Molecular Biology Reports volume 41, pages 6769–6785 (2014)Cite this article

Abstract

MYB transcription factor represents one of the largest gene families in plant genomes. Sweet orange (Citrus sinensis) is one of the most important fruit crops worldwide, and recently the genome has been sequenced. This provides an opportunity to investigate the organization and evolutionary characteristics of sweet orange MYB genes from whole genome view. In the present study, we identified 100 R2R3-MYB genes in the sweet orange genome. A comprehensive analysis of this gene family was performed, including the phylogeny, gene structure, chromosomal localization and expression pattern analyses. The 100 genes were divided into 29 subfamilies based on the sequence similarity and phylogeny, and the classification was also well supported by the highly conserved exon/intron structures and motif composition. The phylogenomic comparison of MYB gene family among sweet orange and related plant species, Arabidopsis, cacao and papaya suggested the existence of functional divergence during evolution. Expression profiling indicated that sweet orange R2R3-MYB genes exhibited distinct temporal and spatial expression patterns. Our analysis suggested that the sweet orange MYB genes may play important roles in different plant biological processes, some of which may be potentially involved in citrus fruit quality. These results will be useful for future functional analysis of the MYB gene family in sweet orange.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. 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 USA 89(14):6428–6432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Kanei-Ishii C, Sarai A, Sawazaki T, Nakagoshi H, He DN, Ogata K, Nishimura Y, Ishii S (1990) The tryptophan cluster: a hypothetical structure of the DNA-binding domain of the myb protooncogene product. J Biol Chem 265(32):19990–19995

    CAS  PubMed  Google Scholar 

  6. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16(2):263–276

    Article  CAS  PubMed  Google Scholar 

  7. Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trends Genet 13(2):67–73

    Article  CAS  PubMed  Google Scholar 

  8. Paz-Ares J, Ghosal D, Wienand U, Peterson PA, 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 Central  CAS  PubMed  Google Scholar 

  9. Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17(3):705–721

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5(3):e1000430

    Article  PubMed Central  PubMed  Google Scholar 

  11. Muller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18(3):586–597

    Article  PubMed Central  PubMed  Google Scholar 

  12. Mu RL, Cao YR, Liu YF, Lei G, Zou HF, Liao Y, Wang HW, Zhang WK, Ma B, Du JZ, Yuan M, Zhang JS, Chen SY (2009) An R2R3-type transcription factor gene AtMYB59 regulates root growth and cell cycle progression in Arabidopsis. Cell Res 19(11):1291–1304

    Article  CAS  PubMed  Google Scholar 

  13. Wang X, Niu QW, Teng C, Li C, Mu J, Chua NH, Zuo J (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 19(2):224–235

    Article  CAS  PubMed  Google Scholar 

  14. Zhu J, Verslues PE, Zheng X, Lee B-H, Zhan X, Manabe Y, Sokolchik I, Zhu Y, Dong CH, Zhu JK (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci USA 102(28):9966–9971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Gao J, Zhang Z, Peng R, Xiong A, Xu J, Zhu B, Yao Q (2010) Forced expression of Mdmyb10, a myb transcription factor gene from apple, enhances tolerance to osmotic stress in transgenic Arabidopsis. Mol Biol Rep 38(1):205–211

    Article  PubMed  Google Scholar 

  16. Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63(7):2541–2556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Qin Y, Wang M, Tian Y, He W, Han L, Xia G (2012) Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol Biol Rep 39(6):7183–7192

    Article  CAS  PubMed  Google Scholar 

  18. Galis I, Simek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K (2006) A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. Plant J 46(4):573–592

    Article  CAS  PubMed  Google Scholar 

  19. Song SK, Ryu KH, Kang YH, Song JH, Cho YH, Yoo SD, Schiefelbein J, Lee MM (2011) Cell fate in the Arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiol 157(3):1196–1208

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. 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(5):814–827

    Article  CAS  PubMed  Google Scholar 

  22. Wei YL, Li JN, Lu J, Tang ZL, Pu DC, Chai YR (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

    Article  CAS  PubMed  Google Scholar 

  23. Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10(1):50

    Article  PubMed Central  PubMed  Google Scholar 

  24. Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24(3):1242–1255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2008) Expansion and diversification of the populus R2R3-MYB family of transcription factors. Plant Physiol 149(2):981–993

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  27. Du H, Feng BR, Yang SS, Huang YB, Tang YX (2012) The R2R3-MYB transcription factor gene family in maize. PLoS ONE 7(6):e37463

    Article  PubMed Central  PubMed  Google Scholar 

  28. Cao ZH, Zhang SZ, Wang RK, Zhang RF, Hao Y-J (2013) Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE 8(7):e69955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Du H, Yang SS, Liang Z, Feng BR, Liu L, Huang YB, Tang YX (2012) Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol 12(1):106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13(1):544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Tombuloglu H, Kekec G, Sakcali MS, Unver T (2013) Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genomics 288(3–4):141–155

    Article  CAS  PubMed  Google Scholar 

  32. Zhang L, Zhao G, Jia J, Liu X, Kong X (2011) Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. J Exp Bot 63(1):203–214

    Article  PubMed Central  PubMed  Google Scholar 

  33. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45(1):59–66

    Article  CAS  PubMed  Google Scholar 

  34. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K (2010) The Pfam protein families database. Nucleic Acids Res 38(suppl 1):D211–D222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39(suppl 2):W29–W37

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. de Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34(suppl 2):W362–W365

    Article  PubMed Central  PubMed  Google Scholar 

  37. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40(D1):D302–D305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31(13):3497–3500

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. 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(10):2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi chuan=Hereditas/Zhongguo yi chuan xue hui bian ji 29(8):1023

    Article  CAS  PubMed  Google Scholar 

  43. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(suppl 2):W202–W208

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  CAS  PubMed  Google Scholar 

  45. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee T-H, Jin H, Marler B, Guo H (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KLT, Salzberg SL, Feng L, Jones MR, Skelton RL, Murray JE, Chen C, Qian W, Shen J, Du P, Eustice M, Tong E, Tang H, Lyons E, Paull RE, Michael TP, Wall K, Rice DW, Albert H, Wang M-L, Zhu YJ, Schatz M, Nagarajan N, Acob RA, Guan P, Blas A, Wai CM, Ackerman CM, Ren Y, Liu C, Wang J, Wang J, Na J-K, Shakirov EV, Haas B, Thimmapuram J, Nelson D, Wang X, Bowers JE, Gschwend AR, Delcher AL, Singh R, Suzuki JY, Tripathi S, Neupane K, Wei H, Irikura B, Paidi M, Jiang N, Zhang W, Presting G, Windsor A, Navajas-Pérez R, Torres MJ, Feltus FA, Porter B, Li Y, Burroughs AM, Luo MC, Liu L, Christopher DA, Mount SM, Moore PH, Sugimura T, Jiang J, Schuler MA, Friedman V, Mitchell-Olds T, Shippen DE, dePamphilis CW, Palmer JD, Freeling M, Paterson AH, Gonsalves D, Wang L, Alam M (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452(7190):991–996

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Argout X, Salse J, Aury J-M, Guiltinan MJ, Droc G, Gouzy J, Allegre M, Chaparro C, Legavre T, Maximova SN, Abrouk M, Murat F, Fouet O, Poulain J, Ruiz M, Roguet Y, Rodier-Goud M, Barbosa-Neto JF, Sabot F, Kudrna D, Ammiraju JSS, Schuster SC, Carlson JE, Sallet E, Schiex T, Dievart A, Kramer M, Gelley L, Shi Z, Bérard A, Viot C, Boccara M, Risterucci AM, Guignon V, Sabau X, Axtell MJ, Ma Z, Zhang Y, Brown S, Bourge M, Golser W, Song X, Clement D, Rivallan R, Tahi M, Akaza JM, Pitollat B, Gramacho K, D’Hont A, Brunel D, Infante D, Kebe I, Costet P, Wing R, McCombie WR, Guiderdoni E, Quetier F, Panaud O, Wincker P, Bocs S, Lanaud C (2011) The genome of Theobroma cacao. Nat Genet 43(2):101–108

    Article  CAS  PubMed  Google Scholar 

  48. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193

    Article  CAS  PubMed  Google Scholar 

  49. Liu Q, Xu J, Liu Y, Zhao X, Deng X, Guo L, Gu J (2007) A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). J Exp Bot 58(15–16):4161–4171

    Article  CAS  PubMed  Google Scholar 

  50. Williams CE, Grotewold E (1997) Differences between plant and animal myb domains are fundamental for DNA binding activity, and chimeric myb domains have novel DNA binding specificities. J Biol Chem 272(1):563–571

    Article  CAS  PubMed  Google Scholar 

  51. Heine G, Hernandez J, Grotewold E (2004) Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. J Biol Chem 279(36):37878–37885

    Article  CAS  PubMed  Google Scholar 

  52. Stephan Guehmann GV, Kalkbrenner Frank, Moelling Karin (1992) Reduction of a conserved cys is essential for myb DNA-binding. Nucleic Acids Res 20(9):2279–2286

    Article  Google Scholar 

  53. Rabinowicz PD, Braun EL, Wolfe AD, Bowen B, Grotewold E (1999) Maize R2R3 myb genes: sequence analysis reveals amplification in the higher plants. Genetics 153(1):427–444

    PubMed Central  CAS  PubMed  Google Scholar 

  54. Dias A, Braun E, McMullen M, Grotewold E (2003) Recently duplicated maize R2R3 myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol 131(2):610–620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  57. Blanc G, Wolfea KH (2004) Functional divergence of duplicated genes formed by polyploidy during arabidopsis evolution. Plant Cell 16(7):1679–1691

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55(2):266–277

    Article  CAS  PubMed  Google Scholar 

  59. Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52(3):528–538

    Article  CAS  PubMed  Google Scholar 

  60. Xie Z, Li D, Wang L, Sack FD, Grotewold E (2010) Role of the stomatal development regulators FLP/MYB88 in abiotic stress responses. Plant J 64(5):731–739

    Article  CAS  PubMed  Google Scholar 

  61. Lai LB, Nadeau JA, Lucas J, Lee E-K, Nakagawa T, Zhao L, Geisler M, Sack FD (2005) The Arabidopsis R2R3 MYB proteins FOUR LIPS and MYB88 restrict divisions late in the stomatal cell lineage. Plant Cell 17(10):2754–2767

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K (2002) The tomato blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci USA 99(2):1064–1069

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15(1):63–78

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Maeda K, Kimura S, Demura T, Takeda J, Ozeki Y (2005) DcMYB1 acts as a transcriptional activator of the carrot phenylalanine ammonia-lyase gene (DcPAL1) in response to elicitor treatment, UV-B irradiation and the dilution effect. Plant Mol Biol 59(5):739–752

    Article  CAS  PubMed  Google Scholar 

  65. Zhang L, Zhao G, Jia J, Liu X, Kong X (2012) Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. J Exp Bot 63(1):203–214

    Article  PubMed Central  PubMed  Google Scholar 

  66. Moriguchi T, Kita M, Tomono Y, Endo-Inagaki T, Omura M (2001) Gene expression in flavonoid biosynthesis: correlation with flavonoid accumulation in developing citrus fruit. Physiol Plant 111(1):66–74

    Article  CAS  Google Scholar 

  67. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Lei Y, Liu YZ, Gu QQ, Yang XY, Deng XX, Chen JY (2012) Comparison of cell wall metabolism in the pulp of three cultivars of ‘Nanfeng’ tangerine differing in mastication trait. J Sci Food Agr 92(3):496–502

    Article  CAS  Google Scholar 

  69. Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol 56(2):255–270

    Article  CAS  PubMed  Google Scholar 

  70. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20(10):2763–2782

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Cultrone A, Cotroneo PS, Recupero GR (2009) Cloning and molecular characterization of R2R3-MYB and bHLH-MYC transcription factors from Citrus sinensis. Tree Genet Genomes 6(1):101–112

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  74. Chen YH, Yang XY, He K, Liu MH, Li JG, Gao ZF, Lin ZQ, Zhang YF, Wang XX, Qiu XM, Shen YP, Zhang L, Deng XH, Luo JC, Deng XW, Chen ZL, Gu HY, Qu LJ (2006) The myb transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice myb family. Plant Mol Biol 60(1):107–124

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31272148 and 31222047) and by the Fundamental Research Funds for the Central Universities.

Author information

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, 430070, China

    Chaoyang Liu, Xia Wang, Yuantao Xu, Xiuxin Deng & Qiang Xu

Authors
  1. Chaoyang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuantao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiuxin Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiang Xu.

Additional information

Chaoyang Liu and Xia Wang have contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Wang, X., Xu, Y. et al. Genome-wide analysis of the R2R3-MYB transcription factor gene family in sweet orange (Citrus sinensis) . Mol Biol Rep 41, 6769–6785 (2014). https://doi.org/10.1007/s11033-014-3563-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3563-1

Keywords

search

Navigation