Arabidopsis trithorax-related3/set domain group2 is required for the winter-annual habit of arabidopsis thaliana

Plant and Cell Physiology

Volumn 53, Issue 5, 2012, Pages 834-846

  Yun, Jae Young ^a   Tamada, Yosuke ^a,b,c   Kang, Ye Eun ^a   Amasino, Richard M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

ARABIDOPSIS TRITHORAX; Flowering; FLOWERING LOCUS C; Histone methylation; Winter annual Arabidopsis

Indexed keywords

ARABIDOPSIS PROTEIN; ATXR3 PROTEIN, ARABIDOPSIS; FLF PROTEIN, ARABIDOPSIS; FRI PROTEIN, ARABIDOPSIS; HISTONE; MADS DOMAIN PROTEIN; METHYLTRANSFERASE;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CHROMATIN; FLOWER; GENE EXPRESSION REGULATION; GENETIC EPISTASIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHYLATION; MUTATION; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLANT GENE; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; SEASON; TIME;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; EPISTASIS, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HISTONES; MADS DOMAIN PROTEINS; METHYLATION; METHYLTRANSFERASES; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SEASONS; TIME FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; DROSOPHILA TRITHORAX;

EID: 84861063480     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs021     Document Type: Article

References (62)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657. (Pubitemid 36927950)
2. Alvarez-Venegas, R. and Avramova, Z. (2001) Two Arabidopsis homologs of the animal trithorax genes: a new structural domain is a signature feature of the trithorax gene family. Gene 271: 215-221. (Pubitemid 32545398)
3. Alvarez-Venegas, R., Pien, S., Sadder, M., Witmer, X., Grossniklaus, U. and Avramova, Z. (2003) ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr. Biol. 13: 627-637. (Pubitemid 36453310)
4. Avramova, Z. (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int. J. Dev. Biol. 53: 371-381.
5. Baumbusch, L.O., Thorstensen, T., Krauss, V., Fischer, A., Naumann, K., Assalkhou, R. et al. (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 29: 4319-4333. (Pubitemid 33064772)
6. Berr, A., McCallum, E.J., Menard, R., Meyer, D., Fuchs, J., Dong, A. et al. (2010) Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development. Plant Cell 22: 3232-3248.
7. Berr, A., Xu, L., Gao, J., Cognat, V., Steinmetz, A., Dong, A. et al. (2009) SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol. 151: 1476-1485.
8. Buzas, D.M., Robertson, M., Finnegan, E.J. and Helliwell, C.A. (2011) Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis polycomb target gene FLC. Plant J. 65: 872-881.
9. Buzas, D.M., Tamada, Y. and Kurata, T. (2012) FLC: a hidden polycomb response element shows up in silence. Plant Cell Physiol. 53, 10.1093/pcp/PCR163.
10. Cao, Y., Dai, Y., Cui, S. and Ma, L. (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20: 2586-2602. (Pubitemid 352844578)
11. Choi, K., Kim, J., Hwang, H.J., Kim, S., Park, C., Kim, S.Y. et al. (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23: 289-303.
12. Chouard, P. (1960) Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11: 191-238.
13. Collins, R.E., Tachibana, M., Tamaru, H., Smith, K.M., Jia, D., Zhang, X. et al. (2005) In vitro and in vivo analyses of a Phe/Tyr switch controlling product specificity of histone lysine methyltransferases. J. Biol. Chem. 280: 5563-5570. (Pubitemid 40280034)
14. Couture, J.F., Dirk, L.M., Brunzelle, J.S., Houtz, R.L. and Trievel, R.C. (2008) Structural origins for the product specificity of SET domain protein methyltransferases. Proc. Natl Acad. Sci. USA 105: 20659-20664.
15. Gendrel, A.V., Lippman, Z., Martienssen, R. and Colot, V. (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat. Methods 2: 213-218. (Pubitemid 41122129)
16. Gu, X., Jiang, D., Wang, Y., Bachmair, A. and He, Y. (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J. 57: 522-533.
17. Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704. (Pubitemid 37365050)
18. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59: 307-321.
19. Guo, L., Yu, Y., Law, J.A. and Zhang, X. (2010) SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis. Proc. Natl Acad. Sci. USA 107: 18557-18562.
20. He, Y., Doyle, M.R. and Amasino, R.M. (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18: 2774-2784. (Pubitemid 39507770)
21. Jiang, D., Gu, X. and He, Y. (2009) Establishment of the winterannual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21: 1733-1746.
22. Jiang, D., Kong, N.C., Gu, X., Li, Z. and He, Y. (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet. 7: e1001330.
23. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R. and Dean, C. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
24. Johnson, L., Cao, X. and Jacobsen, S. (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12: 1360-1367. (Pubitemid 34915537)
25. Katoh, K., Kuma, K., Toh, H. and Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518. (Pubitemid 40360980)
26. Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S. and Amasino, R. (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17: 3301-3310.
27. Kim, S.Y. and Michaels, S.D. (2006) SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis. Development 133: 4699-4707. (Pubitemid 46063082)
28. Ko, J.H., Mitina, I., Tamada, Y., Hyun, Y., Choi, Y., Amasino, R.M. et al. (2010) Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J. 29: 3208-3215.
29. Kofler, M.M. and Freund, C. (2006) The GYF domain. FEBS J. 273: 245-256.
30. Koornneef, M., Blankestijn-de Vries, H., Hanhart, C.J., Soppe, W. and Peeters, T. (1994) The phenotype of some late-Fowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J. 6: 911-919. (Pubitemid 124000316)
31. Krogan, N.J., Dover, J., Wood, A., Schneider, J., Heidt, J., Boateng, M.A. et al. (2003) The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11: 721-729. (Pubitemid 36385125)
32. Lee, I. and Amasino, R.M. (1995) Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108: 157-162.
33. Lee, I., Michaels, S.D., Masshardt, A.S. and Amasino, R.M. (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6: 903-909. (Pubitemid 124000315)
34. Li, B., Carey, M. and Workman, J.L. (2007) The role of chromatin during transcription. Cell 128: 707-719. (Pubitemid 46273570)
35. Liu, C., Lu, F., Cui, X. and Cao, X. (2010) Histone methylation in higher plants. Annu. Rev. Plant Biol. 61: 395-420.
36. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H. et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37: D205-D210.
37. Martin-Trillo, M., Lazaro, A., Poethig, R.S., Gomez-Mena, C., Pineiro, M.A., Martinez-Zapater, J.M. et al. (2006) EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development 133: 1241-1252.
38. Michaels, S.D. and Amasino, R.M. (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
39. Michaels, S.D. and Amasino, R.M. (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13: 935-941. (Pubitemid 32375911)
40. Napp-Zinn, K. (1979) On the genetical basis of vernalization requirement in Arabidopsis thaliana (L.) Heynh. In La Physiologie de la Floraison. Edited by Champagnat, P. and Jaques, R. pp. 217-220. Colloques Internationaux du Centre National de la Recherche Scientifique Paris.
41. Ng, D.W., Wang, T., Chandrasekharan, M.B., Aramayo, R., Kertbundit, S. and Hall, T.C. (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochim. Biophys. Acta 1769: 316-329. (Pubitemid 46855950)
42. Oh, S., Park, S. and van Nocker, S. (2008) Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet. 4: e1000077.
43. Papp, B. and Muller, J. (2006) Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 20: 2041-2054. (Pubitemid 44157456)
44. Pien, S., Fleury, D., Mylne, J.S., Crevillen, P., Inze, D., Avramova, Z. et al. (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20: 580-588. (Pubitemid 352843994)
45. Ratcliffe, O.J., Kumimoto, R.W., Wong, B.J. and Riechmann, J.L. (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15: 1159-1169. (Pubitemid 36579975)
46. Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L. and Riechmann, J.L. (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126: 122-132. (Pubitemid 32532866)
47. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M. et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599. (Pubitemid 30641039)
48. Saleh, A., Alvarez-Venegas, R. and Avramova, Z. (2008a) Dynamic and stable histone H3 methylation patterns at the Arabidopsis FLC and AP1 loci. Gene 423: 43-47.
49. Saleh, A., Alvarez-Venegas, R., Yilmaz, M., Le, O., Hou, G., Sadder, M. et al. (2008b) The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20: 568-579. (Pubitemid 352843993)
50. Samson, F., Brunaud, V., Balzergue, S., Dubreucq, B., Lepiniec, L., Pelletier, G. et al. (2002) FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res. 30: 94-97. (Pubitemid 34679514)
51. Schmitges, F.W., Prusty, A.B., Faty, M., Stutzer, A., Lingaraju, G.M., Aiwazian, J. et al. (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42: 330-341.
52. Schmitz, R.J., Tamada, Y., Doyle, M.R., Zhang, X. and Amasino, R.M. (2009) Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol. 149: 1196-1204.
53. Scortecci, K., Michaels, S.D. and Amasino, R.M. (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol. Biol. 52: 915-922. (Pubitemid 37181486)
54. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J. et al. (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11: 445-458.
55. Springer, N.M., Napoli, C.A., Selinger, D.A., Pandey, R., Cone, K.C., Chandler, V.L. et al. (2003) Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol. 132: 907-925. (Pubitemid 36715089)
56. Suganuma, T. and Workman, J.L. (2008) Crosstalk among histone modifications. Cell 135: 604-607.
57. Tamada, Y., Yun, J.Y., Woo, S.C. and Amasino, R.M. (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21: 3257-3269.
58. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
59. Woody, S.T., Austin-Phillips, S., Amasino, R.M. and Krysan, P.J. (2007) The WiscDsLox T-DNA collection: an arabidopsis community resource generated by using an improved highthroughput T-DNA sequencing pipeline. J. Plant Res. 120: 157-165.
60. Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.P., Steinmetz, A. et al. (2008) Di-and tri-but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol. Cell. Biol. 28: 1348-1360. (Pubitemid 351214136)
61. Xu, L., Menard, R., Berr, A., Fuchs, J., Cognat, V., Meyer, D. et al. (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J. 57: 279-288.
62. Zhao, Z., Yu, Y., Meyer, D., Wu, C. and Shen, W.H. (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7: 1256-1260.