Combinatorial functions of diverse histone methylations in Arabidopsis thaliana flowering time regulation

New Phytologist

Volumn 201, Issue 1, 2014, Pages 312-322

  Shafiq, Sarfraz ^a   Berr, Alexandre ^a   Shen, Wen Hui ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Arabidopsis thaliana; Chromatin; FLOWERING LOCUS C (FLC); FLOWERING LOCUS T (FT); Histone demethylase; Histone methyltransferase

Indexed keywords

DATE (TIME); DICOTYLEDON; ENZYME ACTIVITY; FLOWERING; FUNCTIONAL ROLE; GENE EXPRESSION; INHIBITION; METHYLATION; PHENOTYPE; PHYTOCHEMISTRY; PROTEIN;

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; FT PROTEIN, ARABIDOPSIS; HISTONE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; MADS DOMAIN PROTEIN; METHYLTRANSFERASE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN; ENZYMOLOGY; FLOWER; FLOWERING LOCUS C (FLC); FLOWERING LOCUS T (FT); GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHYLATION; MUTATION; PHENOTYPE; PLANT DEVELOPMENT; PLANT GENE;

ARABIDOPSIS THALIANA; CHROMATIN; FLOWERING LOCUS C (FLC); FLOWERING LOCUS T (FT); HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; FLOWERS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HISTONES; MADS DOMAIN PROTEINS; METHYLATION; METHYLTRANSFERASES; MUTATION; PHENOTYPE; PLANT DEVELOPMENT;

EID: 84888303098     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12493     Document Type: Article

References (63)

1. Alvarez-Venegas R, Sadder M, Hlavacka A, Baluska F, Xia Y, Lu G, Firsov A, Sarath G, Moriyama H, Dubrovsky JG et al. 2006. The Arabidopsis homolog of trithorax, ATX1, binds phosphatidylinositol 5-phosphate, and the two regulate a common set of target genes. Proceedings of the National Academy of Sciences, USA 103: 6049-6054.
2. Amasino R. 2010. Seasonal and developmental timing of flowering. Plant Journal 61: 1001-1013.
3. Angel A, Song J, Dean C, Howard M. 2011. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476: 105-108.
4. Berendzen K, Searle I, Ravenscroft D, Koncz C, Batschauer A, Coupland G, Somssich IE, Ulker B. 2005. A rapid and versatile combined DNA/RNA extraction protocol and its application to the analysis of a novel DNA marker set polymorphic between Arabidopsis thaliana ecotypes Col-0 and Landsberg erecta. Plant Methods 1: 4.
5. Berr A, McCallum EJ, Alioua A, Heintz D, Heitz T, Shen W-H. 2010. Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiology 154: 1403-1414.
6. Berr A, Shafiq S, Shen W-H. 2011. Histone modifications in transcriptional activation during plant development. Biochimica et Biophysica Acta 1809: 567-576.
7. Berr A, Xu L, Gao J, Cognat V, Steinmetz A, Dong A, Shen W-H. 2009. SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiology 151: 1476-1485.
8. Buzas DM, Robertson M, Finnegan EJ, Helliwell CA. 2011. Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis polycomb target gene FLC. Plant Journal 65: 872-881.
9. Buzas DM, Tamada Y, Kurata T. 2012. FLC: a hidden polycomb response element shows up in silence. Plant and Cell Physiology 53: 785-793.
10. Choi J, Hyun Y, Kang MJ, In Yun H, Yun JY. 2009. Resetting and regulation of Flowering Locus C expression during Arabidopsis reproductive development. Plant Journal 57: 918-931.
11. Choi K, Kim J, Hwang H-J, Kim S, Park C, Kim SY, Lee I. 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. Coustham V, Li P, Strange A, Lister C, Song J, Dean C. 2012. Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337: 584-587.
13. Crevillen P, Dean C. 2011. Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Current Opinion in Plant Biology 14: 38-44.
14. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C. 2008. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proceedings of the National Academy of Sciences, USA 105: 16831-16836.
15. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES. 2011. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 6680-6685.
16. Dong G, Ma DP, Li J. 2008. The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochemical and Biophysical Research Communications 373: 659-664.
17. Doyle MR, Amasino RM. 2009. A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiology 151: 1688-1697.
18. Farrona S, Thorpe FL, Engelhorn J, Adrian J, Dong X, Sarid-Krebs L, Goodrich J, Turck F. 2011. Tissue-specific expression of FLOWERING LOCUS T in Arabidopsis is maintained independently of polycomb group protein repression. Plant Cell 23: 3204-3214.
19. Finnegan EJ, Dennis ES. 2007. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Current Biology 17: 1978-1983.
20. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G. 1997. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44-51.
21. Grini PE, Thorstensen T, Alm V, Vizcay-Barrena G, Windju SS, Jørstad TS, Wilson ZA, Aalen RB. 2009. The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS ONE 4: e7817.
22. He Y. 2012. Chromatin regulation of flowering. Trends in Plant Sciences 17: 556-562.
23. Helliwell CA, Robertson M, Finnegan EJ, Buzas DM, Dennis ES. 2011. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE 6: e21513.
24. Helliwell CA, Wood CC, Robertson M, Peacock WJ, Dennis ES. 2006. The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant Journal 46: 183-192.
25. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79.
26. Hoppmann V, Thorstensen T, Kristiansen PE, Veiseth SV, Rahman MA, Finne K, Aalen RB, Aasland R. 2011. The CW domain, a new histone recognition module in chromatin proteins. EMBO Journal 30: 1932-1952.
27. Jeong J-H, Song H-R, Ko J-H, Jeong Y-M, Kwon YE, Seol JH, Amasino RM, Noh B, Noh Y-S. 2009. Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS ONE 4: e8033.
28. Jiang D, Gu X, He Y. 2009. Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21: 1733-1746.
29. Jiang D, Wang Y, Wang Y, He Y. 2008. Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3: e3404.
30. Jiang D, Yang W, He Y, Amasino RM. 2007. Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19: 2975-2987.
31. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
32. Kim SY, He Y, Jacob Y, Noh Y-S, Michaels S, 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.
33. Ko J-H, Mitina I, Tamada Y, Hyun Y, Choi Y, Amasino RM, Noh B, Noh Y-S. 2010. Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO Journal 29: 3208-3215.
34. Kobayashi Y, Weigel D. 2007. Move on up, it's time for change-mobile signals controlling photoperiod-dependent flowering. Genes & Development 21: 2371-2384.
35. Kwon CS, Lee D, Choi G, Chung W. 2009. Histone occupancy-dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. Plant Journal 60: 112-121.
36. Lee J, Lee I. 2010. Regulation and function of SOC1, a flowering pathway integrator. Journal of Experimental Botany 61: 2247-2254.
37. Liu F, Quesada V, Crevillen P, Baurle I, Swiezewski S, Dean C. 2007. The Arabidopsis RNA-binding protein FCA requires a Lysine-Specific Demethylase 1 homolog to downregulate FLC. Molecular Cell 28: 398-407.
38. Lopez-Vernaza M, Yang S, Muller R, Thorpe F, de Leau E, Goodrich J. 2012. Antagonistic roles of SEPALLATA3, FT and FLC genes as targets of the polycomb group gene CURLY LEAF. PLoS ONE 7: e30715.
39. Lu F, Cui X, Zhang S, Jenuwein T, Cao X. 2011. Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nature Genetics 43: 715-719.
40. Lu F, Cui X, Zhang S, Liu C, Cao X. 2010. JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Research 20: 387-390.
41. Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U. 2008. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20: 580-588.
42. Pien S, Grossniklaus U. 2007. Polycomb group and trithorax group proteins in Arabidopsis. Biochimica et Biophysica Acta 1769: 375-382.
43. Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L et al. 2011. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO Journal 30: 1928-1938.
44. Saleh A, Al-Abdallat A, Ndamukong I, Alvarez-Venegas R, Avramova Z. 2007. The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish 'bivalent chromatin marks' at the silent AGAMOUS locus. Nucleic Acids Research 35: 6290-6296.
45. Saleh A, Alvarez-Venegas R, Yilmaz M, Le O, Hou G, Sadder M, Al-Abdallat A, Xia Y, Lu G, Ladunga I et al. 2008. The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20: 568-579.
46. Schmitges FW, Prusty AB, Faty M, Stützer A, Lingaraju GM, Aiwazian J, Sack R, Hess D, Li L, Zhou S et al. 2011. Histone methylation by PRC2 is inhibited by active chromatin marks. Molecular Cell 42: 330-341.
47. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. 2007. Genome regulation by Polycomb and Trithorax proteins. Cell 128: 735-745.
48. Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G. 2006. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes & Development 20: 898-912.
49. Sheldon CC, Hills MJ, Lister C, Dean C, Dennis ES, Peacock WJ. 2008. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proceedings of the National Academy of Sciences, USA 105: 2214-2219.
50. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953.
51. Swiezewski S, Liu F, Magusin A, Dean C. 2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462: 799-802.
52. Tamada Y, Yun J-Y, Woo SC, Amasino RM. 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.
53. Tang X, Lim M-H, Pelletier J, Tang M, Nguyen V, Keller WA, Tsang EWT, Wang A, Rothstein SJ, Harada JJ et al. 2012. Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. Journal of Experimental Botany 63: 1391-1404.
54. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
55. Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA. 2006. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proceedings of the National Academy of Sciences, USA 103: 14631-14636.
56. Xu L, Shen W-H. 2008. Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Current Biology 18: 1966-1971.
57. Xu L, Zhao Z, Dong A, Soubigou-Taconnat L, Renou J-P, Steinmetz A, Shen W-H. 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. Molecular and Cellular Biology 28: 1348-1360.
58. Yang H, Han Z, Cao Y, Fan D, Li H, Mo H, Feng Y, Liu L, Wang Z, Yue Y et al. 2012. A companion cell-dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression. PLoS Genetics 8: e1002664.
59. Yang W, Jiang D, Jiang J, He Y. 2010. A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant Journal 62: 663-673.
60. Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH. 2005. CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiology 139: 770-778.
61. Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B. 2011. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. Journal of Biological Chemistry 286: 7983-7989.
62. Yun H, Hyun Y, Kang MJ, Noh YS, Noh B, Choi Y. 2011. Identification of regulators required for the reactivation of FLOWERING LOCUS C during Arabidopsis reproduction. Planta 234: 1237-1250.
63. Zhao Z, Yu Y, Meyer D, Wu C, Shen W-H. 2005. Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nature Cell Biology 7: 1256-1260.