Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development

Plant Journal

Volumn 57, Issue 5, 2009, Pages 918-931

  Choi, Jean ^a   Hyun, Youbong ^a   Kang, Min Jeong ^a   In Yun, Hye ^a   Yun, Jae Young ^b   Lister, Clare ^c   Dean, Caroline ^c   Amasino, Richard M ^a,b   Noh, Bosl ^a,d   Noh, Yoo Sun ^a   Choi, Yeonhee ^a  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c JOHN INNES CENTRE   (United Kingdom)

^d Gyeongsang National University   (South Korea)

Author keywords

Embryogenesis; Epigenetic resetting; FLC regulators; FLOWERING LOCUS C; Gametogenesis; Vernalization

Indexed keywords

ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN; PLANT RNA;

ALLELE; ARABIDOPSIS; ARTICLE; CROSS BREEDING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PRENATAL DEVELOPMENT; TRANSGENIC PLANT;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CROSSES, GENETIC; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, PLANT;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 61349090400     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03776.x     Document Type: Article

References (52)

1. Ausin, I., Alonso-Blanco, C., Jarillo, J.A., Ruiz-Garcia, L. Martinez-Zapater, J.M. (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36, 162 166.
2. Bastow, R., Mylne, J.S., Lister, C., Lippman, Z., Martienssen, R.A. Dean, C. (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature, 427, 164 167.
3. Baurle, I. Dean, C. (2006) The timing of developmental transitions in plants. Cell, 125, 655 664.
4. Baurle, I., Smith, L., Baulcombe, D.C. Dean, C. (2007) Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science, 318, 109 112.
5. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E. Fischer, R.L. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell, 110, 33 42.
6. Choi, K., Kim, S., Kim, S.Y., Kim, M., Hyun, Y., Lee, H., Choe, S., Kim, S.G., Michaels, S. Lee, I. (2005) SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell, 17, 2647 2660.
7. Choi, K., Park, C., Lee, J., Oh, M., Noh, B. Lee, I. (2007) Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development, 134, 1931 1941.
8. Deal, R.B., Kandasamy, M.K., McKinney, E.C. Meagher, R.B. (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell, 17, 2633 2646.
9. Deal, R.B., Topp, C.N., McKinney, E.C. Meagher, R.B. (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by histone variant H2A.Z. Plant Cell, 19, 74 83.
10. Gazzani, S., Gendall, A.R., Lister, C. Dean, C. (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107 1114.
11. Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B. Fischer, R.L. (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell, 124, 495 506.
12. Gendall, A.R., Levy, Y.Y., Wilson, A. Dean, C. (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell, 107, 525 535.
13. Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A. Gagliano, W.B. (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science, 280, 446 450.
14. Hajkova, P., Ancelin, K., Waldmann, T., Lacoste, N., Lange, U.C., Cesari, F., Lee, C., Almouzni, G., Schneider, R. Surani, M.A. (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature, 452, 877 881.
15. Han, S.K., Song, J.D., Noh, Y.S. Noh, B. (2007) Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 49, 103 114.
16. He, Y., Michaels, S.D. Amasino, R.M. (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science, 302, 1751 1754.
17. He, Y., Doyle, M.R. 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.
18. Jean Finnegan, E., Kovac, K.A., Jaligot, E., Sheldon, C.C., James Peacock, W. Dennis, E.S. (2005) The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J. 44, 420 432.
19. 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.
20. Kim, H.J., Hyun, Y., Park, J.Y., Park, M.J., Park, M.K., Kim, M.D., Lee, M.H., Moon, J., Lee, I. Kim, J. (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 36, 167 171.
21. Kim, S.Y., 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.
22. Kim, S., Choi, K., Park, C., Hwang, H.J. 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.
23. Kinoshita, T., Yadegari, R., Harada, J.J., Goldberg, R.B. Fischer, R.L. (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell, 11, 1945 1952.
24. Kiyosue, T., Ohad, N., Yadegari, R. et al. (1999) Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc. Natl Acad. Sci. USA, 96, 4186 4191.
25. Kohler, C., Hennig, L., Spillane, C., Pien, S., Gruissem, W. Grossniklaus, U. (2003) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17, 1540 1553.
26. Kohler, C., Page, D.R., Gagliardini, V. Grossniklaus, U. (2005) The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat. Genet. 37, 28 30.
27. Lee, I., Aukerman, M.J., Gore, S.L., Lohman, K.N., Michaels, S.D., Weaver, L.M., John, M.C., Feldmann, K.A. Amasino, R.M. (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell, 6, 75 83.
28. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R. Dean, C. (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science, 297, 243 246.
29. Lim, M.H., Kim, J., Kim, Y.S., Chung, K.S., Seo, Y.H., Lee, I., Kim, J., Hong, C.B., Kim, H.J. Park, C.M. (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell, 16, 731 740.
30. Macknight, R., Bancroft, I., Page, T. et al. (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell, 89, 737 745.
31. March-Diaz, R., Garcia-Dominguez, M., Florencio, F.J. Reyes, J.C. (2007) SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6. Plant Physiol. 143, 893 901.
32. March-Diaz, R., Garcia-Dominguez, M., Lozano-Juste, J., León, J., Florencio, F.J. Reyes, J.C. (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J. 53, 475 487.
33. Martin-Trillo, M., Lazaro, A., Poethig, R.S., Gomez-Mena, C., Pineiro, M.A., Martinez-Zapater, J.M. Jarillo, J.A. (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.
34. Michaels, S.D. 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.
35. Michaels, S.D. 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.
36. Michaels, S.D., He, Y., Scortecci, K.C. Amasino, R.M. (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA, 100, 10102 10107.
37. Michaels, S.D., Himelblau, E., Kim, S.Y., Schomburg, F.M. Amasino, R.M. (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149 156.
38. Noh, Y.S. Amasino, R.M. (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell, 15, 1671 1682.
39. Noh, B., Lee, S.H., Kim, H.J., Yi, G., Shin, E.A., Lee, M., Jung, K.J., Doyle, M.R., Amasino, R.M. Noh, Y.S. (2004) Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell, 16, 2601 2613.
40. 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.
41. Pien, S. Grossniklaus, U. (2007) Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769, 375 382.
42. Pien, S., Fleury, D., Mylne, J.S., 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.
43. Reik, W., Dean, W. Walter, J. (2001) Epigenetic reprogramming in mammalian development. Science, 293, 1089 1093.
44. Schomburg, F.M., Patton, D.A., Meinke, D.W. Amasino, R.M. (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell, 13, 1427 1436.
45. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J. Dennis, E.S. (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell, 11, 445 458.
46. Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J. Dennis, E.S. (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl Acad. Sci. USA, 97, 3753 3758.
47. Sheldon, C.C., Hills, M.J., Lister, C., Dean, C., Dennis, E.S. Peacock, W.J. (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl Acad. Sci. USA, 105, 2214 2219.
48. Simpson, G.G., Dijkwel, P.P., Quesada, V., Henderson, I. Dean, C. (2003) FY is an RNA 3' end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell, 113, 777 787.
49. Sung, S. Amasino, R.M. (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature, 427, 159 164.
50. Sung, S. Amasino, R.M. (2005) Remembering winter: toward a molecular understanding of vernalization. Annu. Rev. Plant Biol. 56, 491 508.
51. Wood, C.C., Robertson, M., Tanner, G., Peacock, W.J., Dennis, E.S. Helliwell, C.A. (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.
52. 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. Nat. Cell Biol. 7, 1256 1260.