Expansion and diversification of the Populus R2R3-MYB family of transcription factors

Plant Physiology

Volumn 149, Issue 2, 2009, Pages 981-993

  Wilkins, Olivia ^a   Nahal, Hardeep ^a   Foong, Justin ^a   Provart, Nicholas J ^a   Campbell, Malcolm M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNOLIOPHYTA; POPULUS; POPULUS TRICHOCARPA;

EID: 60249102826     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.132795     Document Type: Article

References (71)

1. 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: 63-78
2. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9: 1859-1868
3. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701
4. Bedon F, Grima-Pettenati J, Mackay J (2007) Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca). BMC Plant Biol 7: 17
5. BoerjanW, Ralph J, BaucherM(2003) Lignin biosynthesis. Annu Rev Plant Biol 54: 519-546
6. Bradshaw HD, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19: 306-313
7. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, et al (2001) Minimumin-formation about a microarray experiment (MIAME): toward standards for microarray data. Nat Genet 29: 365-371
8. Brown NP, Leroy C, Sander C (1998) MView: a web-compatible database search or multiple alignment viewer. Bioinformatics 14: 380-381
9. Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9: 49-56
10. Chang SJ, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 4
11. Chen YH, Yang XY, He K, Liu MH, Li JG, Gao ZF, Lin ZQ, Zhang YF, Wang XX, Qiu XM, et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60: 107-124
12. Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165: 886-894
13. Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Merillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140: 499-511
14. Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10: 1075-1082
15. Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis: duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137: 297-307
16. Feng CP, Andreasson E, Maslak A, Mock HP, Mattsson O, Mundy J (2004) Arabidopsis MYB68 in development and responses to environmental cues. Plant Sci 167: 1099-1107
17. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) Affy: analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315
18. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
19. Gocal GF, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, et al (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127: 1682-1693
20. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, et al (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43: 553-567
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: 814-827
22. Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Muller I, Voss U, Jurgens G, et al (2007) R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134: 1101-1110
23. 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: 155-171
24. Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35: 177-192
25. Ito M (2005) Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res 118: 61-69
26. Ito M, Araki S, Matsunaga S, Itoh T, Nishihama R, Machida Y, Doonan JH, Watanabe A (2001) G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13: 1891-1905
27. Jiang C, Gu X, Peterson T (2004) Identification of conserved gene structures and carboxy-terminal motifs in the Myb gene family of Arabidopsis and Oryza sativa L. ssp. indica. Genome Biol 5: R46
28. 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
29. Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41: 577-585
30. Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146: 623-635
31. 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: 255-270
32. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17: 2981-2992
33. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518
34. Keller T, Abbott J, Moritz T, Doerner P (2006) Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18: 598-611
35. Kranz H, Scholz K, Weisshaar B (2000) c-MYB oncogene-like genes encoding three MYB repeats occur in all major plant lineages. Plant J 21: 231-235
36. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, et al (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16: 263-276
37. Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189
38. Lipsick JS (1996) One billion years of Myb. Oncogene 13: 223-235
39. Matus JT, 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: 83
40. 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
41. Meissner RC, Jin H, Cominelli E, Denekamp M, Fuertes A, Greco R, Kranz HD, Penfield S, Petroni K, Urzainqui A, et al (1999) Function search in a large transcription factor gene family in Arabidopsis: assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Plant Cell 11: 1827-1840
42. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (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: 816-831
43. 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
44. Muller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18: 586-597
45. Ogata K, Morikawa S, Nakamura H, Hojo H, Yoshimura S, Zhang R, Aimoto S, Ametani Y, Hirata Z, Sarai A, et al (1995) Comparison of the free and DNA-complexed forms of the DNA-binding domain from c-Myb. Nat Struct Biol 2: 309-320
46. Okada M, Akimaru H, Hou DX, Takahashi T, Ishii S (2002) Myb controls G(2)/M progression by inducing cyclin B expression in the Drosophila eye imaginal disc. EMBO J 21: 675-684
47. Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67: 483-493
48. Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, et al (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36: 743-754
49. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C (2005) Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132: 359-370
50. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32: 701-712
51. 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
52. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31: 224-228
53. Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110
54. Rosinski JA, Atchley WR (1998) Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. J Mol Evol 46: 74-83
55. 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: 1064-1069
56. Shin B, Choi G, Yi H, Yang S, Cho I, Kim J, Lee S, Paek NC, Kim JH, Song PS (2002) AtMYB21, a gene encoding a flower-specific transcription factor, is regulated by COP1. Plant J 30: 23-32
57. 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
58. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456
59. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599
60. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139: 1840-1852
61. Tominaga R, Iwata M, Okada K, Wada T (2007) Functional analysis of the epidermal-specific MYB genes CAPRICE and WEREWOLF in Arabidopsis. Plant Cell 19: 2264-2277
62. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-northerns, expression angling, and promoter analyses. Plant J 43: 153-163
63. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604
64. Urao T, Noji M, Yamaguchi-Shinozaki K, Shinozaki K (1996) A transcriptional activation domain of AtMYB2, a drought-inducible Arabidopsis Myb-related protein. Plant J 10: 1145-1148
65. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2: e1326
66. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113-1116
67. Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12: 1474-1482
68. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "electronic fluorescent pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718
69. Yang XY, Li JG, Pei M, Gu H, Chen ZL, Qu LJ (2007) Over-expression of a flower-specific transcription factor gene AtMYB24 causes aberrant anther development. Plant Cell Rep 26: 219-228
70. Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, et al (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52: 528-538
71. Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19: 2776-2792