SUPPRESSOR of FRIGIDA4, encoding a C2H2-type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C

Plant Cell

Volumn 18, Issue 11, 2006, Pages 2985-2998

  Kim, Sanghee ^a   Choi, Kyuha ^a   Park, Chulmin ^a   Hwang, Hyun Ju ^a   Lee, Ilha ^a,b  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; PLANT CELL CULTURE; PLANTS (BOTANY);

FINGER PROTEINS; IMMUNOPRECIPITATION ASSAYS; VERNALIZATION;

PROTEINS;

ACTIVATION; MUTATION; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33845763347     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.045179     Document Type: Article

References (66)

1. Aukerman, M.J., Lee, I., Weigel, D., and Amasino, R.M. (1999). The Arabidopsis flowering-time gene LUMINIDEPENDENS is expressed primarily in regions of cell proliferation and encodes a nuclear protein that regulates LEAFY expression. Plant J. 18, 195-203.
2. Ausin, I., Alonso-Blanco, C., Jarillo, J.A., Ruiz-Garcia, L., and Martinez-Zapater, J.M. (2004). Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36, 162-166.
3. Bastow, R., Mylne, J.S., Lister, C., Lippman, Z., Martienssen, R.A., and Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164-167.
4. Bergqvist, M., Brattstrom, D., Brodin, D., Lindkvist, A., Dahlman-Wright, K., Dreilich, M., Wagenius, G., and Paulsson-Karlsson, Y. (2006). Genes associated with telomerase activity levels in esophageal carcinoma cell lines. Dis. Esophagus 19, 20-23.
5. Blazquez, M., Soowal, L., Lee, I., and Weigel, D. (1997). LEAFY expression and flower initiation in Arabidopsis. Development 124, 3835-3844.
6. Blázquez, M.A., and Weigel, D. (2000). Integration of floral inductive signals in Arabidopsis. Nature 404, 889-892.
7. Chanvivattana, Y., Bishop, A., Schubert, D., Stock, C., Moon, Y.H., Sung, Z.R., and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263-5276.
8. Choi, K., Kim, S., Kim, S.Y., Kim, M., Hyun, Y., Lee, H., Choe, S., Kim, S.G., Michaels, S., and Lee, I. (2005). SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17, 2647-2660.
9. Deal, R.B., Kandasamy, M.K., McKinney, E.C., and 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.
10. Englbrecht, C.C., Schoof, H., and Bohm, S. (2004). Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5, 39.
11. Finnegan, E.J., Sheldon, C.C., Jardinaud, F., Peacock, W.J., and Dennis, E.S. (2004). A cluster of Arabidopsis genes with a coordinate response to an environmental stimulus. Curr. Biol. 14, 911-916.
12. Fischer, R., Vaquero-Martin, C., Sack, M., Drossard, J., Emans, N., and Commandeur, U. (1999). Towards molecular farming in the future: Transient protein expression in plants. Biotechnol. Appl. Biochem. 30, 113-116.
13. Gaudin, V., Libault, M., Pouteau, S., Juul, T., Zhao, G., Lefebvre, G., and Grandjean, O. (2001). Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128, 4847-4858.
14. Gazzani, S., Gendall, A.R., Lister, C., and Dean, C. (2003). Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107-1114.
15. Gendall, A.R., Levy, Y.Y., Wilson, A., and Dean, C. (2001). The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525-535.
16. 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.
17. He, Y., Michaels, S.D., and Amasino, R.M. (2003). Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751-1754.
18. Jack, T., Fox, G.L., and Meyerowitz, E.M. (1994). Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and post-transcriptional regulation determine floral organ identity. Cell 76, 703-716.
19. 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.
20. Johnson, K.D., and Bresnick, E.H. (2002). Dissecting long-range transcriptional mechanisms by chromatin immunoprecipitation. Methods 26, 27-36.
21. 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.
22. Klug, A., and Schwabe, J.W. (1995). Protein motifs 5. Zinc fingers. FASEB J. 9, 597-604.
23. Koornneef, M., Blankestijn-de Wies, H., Hanhart, C., Soppe, W., and 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 wild-type. Plant J. 6, 911-919.
24. Kotake, T., Takada, S., Nakahigashi, K., Ohto, M., and Goto, K. (2003). Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44, 555-564.
25. Kuzmichev, A., Nishioka, K., Erdjument-Bromage, H., Tempst, P., and Reinberg, D. (2002). Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16, 2893-2905.
26. Lee, H., Sun, S.S., Park, E., Cho, E., Ahn, J.H., Kim, S.G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376.
27. 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.
28. Lee, I., Michaels, S.D., Masshardt, A.S., and Amasino, R.M. (1994). The late-flowering phenotype of FRIGIDA and LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903-909.
29. Leibfried, A., To, J.P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J.J., and Lohmann, J.U. (2005). WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172-1175.
30. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R., and Dean, C. (2002). Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243-246.
31. Lim, M.H., Kim, J., Kim, Y.S., Chung, K.S., Seo, Y.H., Lee, I., Kim, J., Hong, C.B., Kim, H.J., and 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.
32. Liu, J., He, Y., Amasino, R., and Chen, X. (2004). siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev. 18, 2873-2878.
33. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25, 402-408.
34. Llave, C., Kasschau, K.D., and Carrington, J.C. (2000). Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc. Natl. Acad. Sci. USA 97, 13401-13406.
35. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in Arabidopsis. Plant Physiol. 123, 795-805.
36. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., and Dean, C. (1997). FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737-745.
37. Martin-Trillo, M., Lazaro, A., Poethig, R.S., Gomez-Mena, C., Pineiro, MA., Martinez-Zapater, J.M., and Jarillo, J.A. (2006). EARLY IN SHORT DAYS 1 (ESDI) 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.
40. Michaels, S.D., Bezerra, I.C., and Amasino, R.M. (2004). FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc. Natl. Acad. Sci. USA 101, 3281-3285.
41. Michaels, S.D., He, Y., Scortecci, K.C., and 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.
42. Napp-Zinn, K. (1985). Arabidopsis thaliana. In CRC Handbook of Flowering, H.A. Halevy, ed (Boca Raton, FL: CRC Press), pp. 492-503.
43. Noh, Y.S., and Amasino, R.M. (2003). PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15, 1671-1682.
44. Oh, S., Zhang, H., Ludwig, P., and 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.
45. Pahl, P.M., Hodges, Y.K., Meltesen, L, Perryman, M.B., Horwitz, K.B., and Horwitz, L.D. (1998). ZNF207, a ubiquitously expressed zinc finger gene on chromosome 6p21.3. Genomics 53, 410-412.
46. 2 zinc finger domain of the GATA protein flanked by basic residues is sufficient for high-affinity specific DNA binding. Proc. Natl. Acad. Sci. USA 93, 2822-2826.
47. 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.
48. 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.
49. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1618.
50. Schmitz, R.J., Hong, L., Michaels, S., and Amasino, R.M. (2005). FRIGIDA-ESSENTIAL1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132, 5471-5478.
51. Schomburg, F.M., Patton, D.A., Meinke, D.W., and 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.
52. 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.
53. Sheen, J. (2002). A transient expression assay using Arabidopsis mesophyll protoplasts. http://genetics.mgh.harvard.edu/sheenweb/.
54. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and 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.
55. Sheldon, C.C., Conn, A.B., Dennis, E.S., and Peacock, W.J. (2002). Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527-2537.
56. Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J., and 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.
57. Simpson, G.G., and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time? Science 296, 285-289.
58. Simpson, G.G., Dijkwel, P.P., Quesada, V., Henderson, I., and 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.
59. Soppe, W.J., Bentsink, L., and Koornneef, M. (1999). The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development 126, 4763-4770.
60. Sung, S., and Amasino, P.M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164.
61. Taguchi, E., Muramatsu, H., Fan, Q.W., Kurosawa, N., Sobue, G., and Muramatsu, T. (1998). Zep: A novel zinc finger protein containing a large proline-rich domain. J. Biochem. (Tokyo) 124, 1220-1228.
62. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.
63. Williams, T., and Tjian, R. (1991). Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev. 5, 670-682.
64. Williamson, M.P. (1994). The structure and function of proline-rich regions in proteins. Biochem. J. 297, 249-260.
65. Zhang, H., and van Nocker, S. (2002). The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C. Plant J. 31, 663-667.
66. 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.