Molecules and Cells

, Volume 32, Issue 3, pp 227–234 | Cite as

FVE, an Arabidopsis homologue of the retinoblastoma-associated protein that regulates flowering time and cold response, binds to chromatin as a large multiprotein complex



Some genetic studies indicate that plant homologues of proteins involved in chromatin modification and remodeling in other organisms may regulate plant development. Previously, we described an Arabidopsis mutant with altered cold-responsive gene expression (acg1) displaying a late flowering phenotype, a null allele of fve. FVE is a homologue of the mammalian retinoblastoma-associated protein (RbAp), one component of a histone deacetylase (HDAC) complex involved in transcriptional repression, and has been shown to be involved in the deacetylation of the FLOWERING LOCUS C (FLC) chromatin encoding for a repressor of flowering. In an effort to gain insight into the biochemical functions of FVE, we overexpressed FVE tagged with the hemagglutinin (HA) and FLAG epitope at the N-terminus in acg1 mutants. The results of physiological and molecular analyses demonstrated that FVE overexpression in acg1 rescued the mutant phenotypes, including late flowering and alterations in floral pathway gene expression such as FLC, SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), and FLOWERING LOCUS T (FT), and also super-induced cold-responsive reporter gene expression. The chromatin immunoprecipitation experiments revealed the amplification of specific DNA regions of FLC and COLD-REGULATED 15A (COR15A), indicating that FVE may bind to the FLC and COR15A chromatin. Gel-filtration chromatography and the immunoprecipitation of putative FVE complexes showed that FVE forms a protein complex of approximately 1.0 MDa. These results demonstrate that FVE may exist as a multiprotein complex, similar to the mammalian HDAC complex harboring RbAp, to regulate flowering time and cold response by associating with the FLC and COR chromatin.


chromatin flowering FVE histone deacetylase retinoblastoma-associated protein 


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  1. Alland, L., Muhle, R., Hou, H., Jr., Potes, J., Chin, L., Schreiber-Agus, N., and DePinho, R.A. (1997). Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 387, 49–55.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  3. Ausin, I., Alonso-Blanco, C., and Martinez-Zapater, J.M. (2005). Environmental regulation of flowering. Int. J. Dev. Biol. 49, 689–705.PubMedCrossRefGoogle Scholar
  4. Boss, P.K., Bastow, R.M., Mylne, J.S., and Dean, C. (2004). Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16, S18–S31.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. Gusmaroli, G., Feng, S., and Deng, X.W. (2004). The Arabidopsis CSN5A and CSN5B subunits are present in distinct COP9 signalosome complexes, and mutations in their JAMM domains exhibit differential dominant negative effects on development. Plant Cell 16, 2984–3001.PubMedCrossRefGoogle Scholar
  7. Hassig, C.A., Fleischer, T.C., Billin, A.N., Schreiber, S.L., and Ayer, D.E. (1997). Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 89, 341–347.PubMedCrossRefGoogle Scholar
  8. He, Y., Michaels, S.D., and Amasino, R.M. (2003). Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751–1754.PubMedCrossRefGoogle Scholar
  9. Heinzel, T., Lavinsky, R.M., Mullen, T.M., Soderstrom, M., Laherty, C.D., Torchia, J., Yang, W.M., Brard, G., Ngo, S.D., Davie, J.R., et al. (1997). A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387, 43–48.PubMedCrossRefGoogle Scholar
  10. Hennig, L., Bouveret, R., and Gruissem, W. (2005). MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol. 15, 295–302.PubMedCrossRefGoogle Scholar
  11. Jefferson, R.A., and Wilson, K.J. (1991). The GUS gene fusion system. Plant Mol. Biol. Manual, (Dordrecht: Kluwer Academic Publishers). B14, 1–33.Google Scholar
  12. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907.PubMedGoogle Scholar
  13. Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novák, O., Ku, S.J., Cho, C., Lee, D.J., Lee, E.J., Strnad, M., et al. (2010). A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 285, 23371–23386.PubMedCrossRefGoogle Scholar
  14. Kasten, M.M., Dorland, S., and Stillman, D.J. (1997). A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators. Mol. Cell. Biol. 17, 4852–4858.PubMedGoogle Scholar
  15. Kim, H.J., Kim, Y.K., Park, J.Y., and Kim, J. (2002). Light signalling mediated by phytochrome plays an important role in coldinduced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J. 29, 693–704.PubMedCrossRefGoogle Scholar
  16. Kim, H.J., Hyun, Y., Park, J.Y., Park, M.J., Park, M.K., Kim, M.D., Lee, M.H., Moon, J., Lee, I., and Kim, J. (2004). A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 36, 167–171.PubMedCrossRefGoogle Scholar
  17. Kim, S., Choi, K., Park, C., Hwang, H.J., and 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.PubMedCrossRefGoogle Scholar
  18. Laherty, C.D., Yang, W.M., Sun, J.M., Davie, J.R., Seto, E., and Eisenman, R.N. (1997). Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89, 349–356.PubMedCrossRefGoogle Scholar
  19. Lee, I., Aukerman, M.J., Gore, S.L., Lohman, K.N., Michaels, S.D., Weaver, L.M., John, M.C., Feldmann, K.A., and Amasino, R.M. (1994). Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6, 75–83.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. Luo, R.X., Postigo, A.A., and Dean, D.C. (1998). Rb interacts with histone deacetylase to repress transcription. Cell 92, 463–473.PubMedCrossRefGoogle Scholar
  22. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., et al. (1997). FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737–745.PubMedCrossRefGoogle Scholar
  23. Magnaghi-Jaulin, L., Groisman, R., Naguibneva, I., Robin, P., Lorain, S., Le Villain, J.P., Troalen, F., Trouche, D., and Harel-Bellan, A. (1998). Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391, 601–605.PubMedCrossRefGoogle Scholar
  24. Michels, 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.CrossRefGoogle Scholar
  25. Nagy, L., Kao, H.Y., Chakravarti, D., Lin, R.J., Hassig, C.A., Ayer, D.E., Schreiber, S.L., and Evans, R.M. (1997). Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89, 373–380.PubMedCrossRefGoogle Scholar
  26. Nicolas, E., Morales, V., Magnaghi-Jaulin, L., Harel-Bellan, A., Richard-Foy, H., and Trouche, D. (2000). RbAp48 belongs to the histone deacetylase complex that associates with the retinoblastoma protein. J. Biol. Chem. 275, 9797–9804.PubMedCrossRefGoogle Scholar
  27. Pazhouhandeh, M., Molinier, J., Berr, A., and Genschik, P. (2011). MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc. Natl. Acad. Sci. USA 108, 3430–3435.PubMedCrossRefGoogle Scholar
  28. Putterill, J., Laurie, R., and Macknight, R. (2004). It’s time to flower: the genetic control of flowering time. Bioessays 26, 363–373.PubMedCrossRefGoogle Scholar
  29. Qian, Y.W., and Lee, E.Y. (1995). Dual retinoblastoma-binding proteins with properties related to a negative regulator of ras in yeast. J. Biol. Chem. 270, 25507–25513.PubMedCrossRefGoogle Scholar
  30. Rossi, V., Locatelli, S., Lanzanova, C., Boniotti, M.B., Varotto, S., Pipal, A., Goralik-Schramel, M., Lusser, A., Gatz, C., Gutierrez, C., et al. (2003). A maize histone deacetylase and retinoblastoma-related protein physically interact and cooperate in repressing gene transcription. Plant Mol. Biol. 51, 401–413.PubMedCrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858.PubMedCrossRefGoogle Scholar
  33. Simpson, G.G. (2004). The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol. 7, 570–574.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. Stockinger, E.J., Gilmour, S.J., and Thomashow, M.F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA 94, 1035–1040.PubMedCrossRefGoogle Scholar
  36. Taunton, J., Hassig, C.A., and Schreiber, S.L. (1996). A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272, 408–411.PubMedCrossRefGoogle Scholar
  37. Wade, P.A., Jones, P.L., Vermaak, D., and Wolffe, A.P. (1998). A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr. Biol. 8, 843–846.PubMedCrossRefGoogle Scholar
  38. Zhang, Y., Iratni, R., Erdjument-Bromage, H., Tempst, P., and Reinberg, D. (1997). Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89, 357–364.PubMedCrossRefGoogle Scholar
  39. Zhang, Y., Sun, Z.W., Iratni, R., Erdjument-Bromage, H., Tempst, P., Hampsey, M., and Reinberg, D. (1998). SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex. Mol. Cell 1, 1021–1031.PubMedCrossRefGoogle Scholar

Copyright information

© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2011

Authors and Affiliations

  1. 1.Department of Plant BiotechnologyChonnam National UniversityGwangjuKorea
  2. 2.Department of Bioenergy Science and TechnologyChonnam National UniversityGwangjuKorea

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