FLOWERING LOCUS C EXPRESSOR family proteins regulate FLOWERING LOCUS C expression in both winter-annual and rapid-cycling Arabidopsis

Plant Physiology

Volumn 163, Issue 1, 2013, Pages 243-252

  Ding, Lei ^a   Kim, Sang Yeol ^a,b   Michaels, Scott D ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; FLX PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN;

ARABIDOPSIS; ARTICLE; COLD; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SEASON;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD TEMPERATURE; FLOWERS; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; SEASONS;

EID: 84883231107     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.223958     Document Type: Article

References (61)

1. Andersson CR, Helliwell CA, Bagnall DJ, Hughes TP, Finnegan EJ, Peacock WJ, Dennis ES (2008) The FLX gene of Arabidopsis is required for FRIdependent activation of FLC expression. Plant Cell Physiol 49: 191-200
2. Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605-612
3. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167
4. Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24: 591-599
5. Burn JE, Smyth DR, Peacock WJ, Dennis ES (1993) Genes conferring late flowering in Arabidopsis thaliana. Genetica 90: 147-155
6. Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20: 2586-2602
7. Chiang GC, Barua D, Kramer EM, Amasino RM, Donohue K (2009) Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106: 11661-11666
8. Choi K, Kim J, Hwang HJ, 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
9. Clarke JH, Dean C (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet 242: 81-89
10. Crevillén P, Dean C (2011) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14: 38-44
11. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHDpolycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105: 16831-16836
12. Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19: 74-83
13. DeYoung BJ, Qi D, Kim SH, Burke TP, Innes RW (2012) Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell Microbiol 14: 1071-1084
14. Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17: 1978-1983
15. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488
16. Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR, Dean C (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 17: 73-78
17. Gu X, Jiang D, Wang Y, Bachmair A, He Y (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J 57: 522-533
18. Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25: 989-994
19. He Y, Doyle MR, Amasino RM (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
20. Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79
21. Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J 21: 4327-4337
22. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733-739
23. 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
24. Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7: e1001330
25. 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
26. Kim DH, Sung S (2012) Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Curr Opin Plant Biol 15: 51-56
27. Kim S, Choi K, Park C, Hwang HJ, Lee I (2006) SUPPRESSOR OF FRIGIDA4, encoding a C2H2-Type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C. Plant Cell 18: 2985-2998
28. Kim SY, Michaels SD (2006) SUPPRESSOR OF FRI 4 encodes a nuclearlocalized protein that is required for delayed flowering in winter-annual Arabidopsis. Development 133: 4699-4707
29. Koo SC, BrackoO, ParkMS, Schwab R, Chun HJ, Park KM, Seo JS, Grbic V, Balasubramanian S, Schmid M, et al (2010) Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box Gene AGAMOUS-LIKE6. Plant J 62: 807-816
30. Koornneef M, Blankestijn-de Vries H, Hanhart C, Soppe W, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wildtype. Plant J 6: 911-919
31. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366-2376
32. Lee I, Michaels SD, Masshardt AS, Amasino RM (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
33. March-Díaz R, García-Domínguez M, Lozano-Juste J, León J, Florencio FJ, Reyes JC (2008) Histone H2A. Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53: 475-487
34. March-Díaz R, Reyes JC (2009) The beauty of being a variant: H2A. Z and the SWR1 complex in plants. Mol Plant 2: 565-577
35. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956
36. Michaels SD, Amasino RM (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
37. Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA 101: 3281-3285
38. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137: 149-156
39. Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L, Bernatavichute YV, Jacobsen SE, Fransz P, Dean C (2006) LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc Natl Acad Sci USA 103: 5012-5017
40. Napp-Zinn K (1987) Vernalization: environmental and genetic regulation. In JG Atherton, ed, Manipulation of Flowering. Butterworths, London, pp 123-132
41. Oh S, Zhang H, Ludwig P, van Nocker S (2004) A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell 16: 2940-2953
42. Park S, Oh S, Ek-Ramos J, van Nocker S (2010) PLANT HOMOLOGOUS TO PARAFIBROMIN is a component of the PAF1 complex and assists in regulating expression of genes within H3K27ME3-enriched chromatin. Plant Physiol 153: 821-831
43. Salathia N, Davis SJ, Lynn JR, Michaels SD, Amasino RM, Millar AJ (2006) FLOWERING LOCUS C-dependent and-independent regulation of the circadian clock by the autonomous and vernalization pathways. BMC Plant Biol 6: 10
44. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
45. Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDAESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132: 5471-5478
46. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301: 1230-1233
47. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11: 445-458
48. Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164
49. Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006a) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38: 706-710
50. Sung S, Schmitz RJ, Amasino RM (2006b) A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20: 3244-3248
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. Takase T, Yasuhara M, Geekiyanage S, Ogura Y, Kiyosue T (2007) Overexpression of the chimeric gene of the floral regulator CONSTANS and the EAR motif repressor causes late flowering in Arabidopsis. Plant Cell Rep 26: 815-821
53. Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3: e86
54. Veley KM, Michaels SD (2008) Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiol 147: 682-695
55. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, et al (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438
56. 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. Proc Natl Acad Sci USA 103: 14631-14636
57. Xu L, Menard R, Berr A, Fuchs J, Cognat V, Meyer D, Shen WH (2008) 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
58. Yamamoto YY, Matsui M, Ang LH, Deng XW (1998) Role of a COP1 interactive protein in mediating light-regulated gene expression in Arabidopsis. Plant Cell 10: 1083-1094
59. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
60. Yu X, Michaels SD (2010) The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLOWERING LOCUS C chromatin. Plant Physiol 153: 1074-1084
61. Zhang H, van Nocker S (2002) The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C. Plant J 31: 663-673