Histone acetylation, vernalization insensitive 3, flowering locus C, and the vernalization response

Molecular Plant

Volumn 2, Issue 4, 2009, Pages 724-737

  Bond, Donna M ^a,b   Dennis, Elizabeth S ^a   Pogson, Barry J ^b   Finnegan, E Jean ^a  

^a CSIRO   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Cold acclimation; Histone acetyltransferase; Histone deacetylase; Nicotinamide; SIR2

Indexed keywords

ARABIDOPSIS;

EID: 68449104035     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssp021     Document Type: Article

References (62)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657.
2. Ausin, I., Alonso-Blanco, C., Jarillo, J.A., Ruiz-Garcia, L., and Martinez-Zapater, J.M. (2004). Regulation offloweringtimebyFVE,aretino- blastoma-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. Benhamed, M., Bertrand, C., Servet, C., and Zhou, D.X. (2006). Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate his-tone acetylation required for light-responsive gene expression. Plant Cell. 18, 2893-2903.
5. Bertrand, C., Benhamed, M., Li, Y.F., Ayadi, M., Lemonnier, G., Renou, J.P., Delarue, M., and Zhou, D.X. (2005). Arabidopsis HAF2 gene encoding TATA-binding protein (TBP)-associated factor TAF1, is required to integrate light signals to regulate gene expression and growth. J. Biol. Chem. 280, 1465-1473.
6. Bertrand, C., Bergounioux, C., Domenichini, S., Delarue, M., and Zhou, D.X. (2003). Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/ AGAMOUS pathway. J. Biol. Chem. 278, 28246-28251.
7. Bitterman, K.J., Anderson, R.M., Cohen, H.Y., Latorre-Esteves, M., and Sinclair, D.A. (2002). Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J. Biol. Chem. 277, 45099-45107.
8. Bordoli, L., Netsch, M., Luthi, U., Lutz, W., and Eckner, R. (2001). Plant orthologs of p300/CBP: conservation of a core domain in metazoan p300/CBP acetyltransferase-related proteins. Nucleic Acids Res. 29, 589-597.
9. Cao, R., and Zhang, Y. (2004). The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14, 155-164.
10. Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B.H., Hong, X., Agarwal, M., and Zhu, J.K. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17, 1043-1054.
11. Chua, Y.L., Mott, E., Brown, A.P., MacLean, D., and Gray, J.C. (2004). Microarray analysis of chromatin-immunoprecipitated DNA identifies specific regions of tobacco genes associated with acet-ylated histones. Plant J. 37, 789-800.
12. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Davie, J.R. (2003). Inhibition of histone deacetylase activity by bu-tyrate. J. Nutr. 133, 2485S-2493S.
14. De Lucia, F., Crevillen, P., Jones, A.M.E., Greb, T., and Dean, C. (2008). A PHD-Polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl Acad. Sci. U S A. 105, 16831-16836.
15. Deng, W., Liu, C., Pei, Y., Deng, X., Niu, L., and Cao, X. (2007). Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol. 143, 1660-1668.
16. Earley, K.W., Shook, M.S., Brower-Toland, B., Hicks, L., and Pikaard, C.S. (2007). In vitro specificities of Arabidopsis coactivator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J. 52, 615-626.
17. Edwards, K., Johnstone, C., and Thompson, C. (1991). A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
18. Finnegan, E.J., and Dennis, E.S. (2007). Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978-1983.
19. Finnegan, E.J., Kovac, K.A., Jaligot, E., Sheldon, C.C., James Peacock, W., and 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.
20. 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.
21. Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., and Thomashow, M.F. (1998). Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16, 433-442.
22. Greb, T., Mylne, J.S., Crevillen, P., Geraldo, N., An, H., Gendall, A.R., and Dean, C. (2007). The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73-78.
23. Han, S.K., Song, J.D., Noh, Y.S., and Noh, B. (2006). Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 49, 103-114.
24. Hark, A.T., Vlachonasios, K.E., Pavangadkar, K.A., Rao, S., Gordon, H., Adamakis, I.D., Kaldis, A., Thomashow, M.F., and Triezenberg, S.J. (2009). Two Arabidopsis orthologs of the transcriptional coactivator ADA2 have distinct biological functions. Biochim. Biophys. Acta. 1789, 117-124.
25. Hebbes, T.R., Thorne, A.W., and Crane-Robinson, C. (1988). A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7, 1395-1402.
26. Helliwell, C.A., Wood, C.C., Robertson, M., James Peacock, W., and Dennis, E.S. (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 J. 46, 183-192.
27. Hollender, C., and Liu, Z. (2008). Histone deacetylase genes in Arabidopsis development. J. Integr. Plant Biol. 50, 875-885.
28. Jackson, T.M., Rawling, J.M., Roebuck, B.D., and Kirkland, J.B. (1995). Large supplements of nicotinic acid and nicotinamide increase tissue NAD+ and poly(ADP-ribose) levels but do not affect diethylnitrosamine-induced altered hepatic foci in Fischer-344 rats. J. Nutr. 125, 1455-1461.
29. Johnson, L., Cao, X., and Jacobsen,S. (2002). Interplay between two epigenetic marks: DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360-1367.
30. Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., Peacock, W.J., Dolferus, R., and Dennis, E.S. (2002). Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell. 14, 2481-2494.
31. Landry, J., Slama, J.T., and Sternglanz, R. (2000). Role of NAD(+) in the deacetylase activity of the SIR2-like proteins. Biochem. Biophys. Res. Commun. 278, 685-690.
32. Latrasse, D., Benhamed, M., Henry, Y., Domenichini, S., Kim, W., Zhou, D.-X., and Delarue, M. (2008). The MYST histone acetyl-transferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol. 8, 121.
33. Lee, I., Michaels, S.D., Masshardt, A.S., and Amasino, R.M. (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.
34. 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.
35. Long, J.A., Ohno, C., Smith, Z.R., and Meyerowitz, E.M. (2006). TOPLESS regulates apical embryonic fate in Arabidopsis. Science. 312, 1520-1523.
36. Luo, J., Nikolaev, A.Y., Imai, S., Chen, D., Su, F., Shiloh, A., Guarente, L., and Gu, W. (2001). Negative control of p53 by Sir2-alpha promotes cell survival under stress. Cell. 107, 137-148.
37. Maciejewska, U., and Kacperska, A. (1987). Changes in the level of oxidized and reduced pyridine nucleotides during cold acclimation of winter rape plants. Physiol. Plant. 69, 687-691.
38. Mao, Y., Pavangadkar, K.A., Thomashow, M.F., and Triezenberg, S.J. (2006). Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim. Biophys. Acta. 1759, 69-79.
39. 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.
40. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assay with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
41. Mylne, J.S., Barrett, L., Tessadori, F., Mesnage, S., Johnson, L., Bernatavichute, Y.V., Jacobsen, S.E., Fransz, P., and Dean, C. (2006). LHP1, the Arabidopsis homologue of HETEROCHROMA-TIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl Acad. Sci. U S A. 103, 5012-5017.
42. Nelissen, H., et al. (2005). The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc. Natl Acad. Sci. U S A. 102, 7754-7759.
43. Pandey, R., Muller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W., and Jorgensen, R.A. (2002). Analysis of histone acetyltransferase and histone deace-tylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30, 5036-5055.
44. Rybtsova, N., Leimgruber, E., Seguin-Estevez, Q., Dunand-Sauthier, I., Krawczyk, M., and Reith, W. (2007). Transcription-coupled deposition of histone modifications during MHC class II gene activation. Nucleic Acids Res. 35, 3431-3441.
45. Schonrock, N., Bouveret, R., Leroy, O., Borghi, L., Kohler, C., Gruissem, W., and Hennig, L. (2006). Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev. 20, 1667-1678.
46. Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T., and Goodrich, J. (2006). Silencing by plant Poly-comb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638-4649.
47. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R.A., and Coupland, G. (2006). The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898-912.
48. Shahbazian, M.D., and Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75-100.
49. 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.
50. Sheldon, C.C., Hills, M.J., Lister, C., Dean, C., Dennis, E.S., and Peacock, W.J. (2008). Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl Acad. Sci. U S A. 105, 2214-2219.
51. 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.U S A. 97, 3753-3758.
52. 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.
53. Sterner, D.E., and Berger, S.L. (2000). Acetylationofhistones andtran-scription-related factors. Microbiol. Mol. Biol. Rev. 64, 435-459.
54. Stockinger, E.J., Mao, Y., Regier, M.K., Triezenberg, S.J., and Thomashow, M.F. (2001). Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res. 29, 1524-1533.
55. Sung, S., and Amasino, R.M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature. 427, 159-164.
56. Sung, S., He, Y., Eshoo, T.W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S.E., and Amasino, R.M. (2006a). Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706-710.
57. Sung, S., Schmitz, R.J., and Amasino, R.M. (2006b). A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev. 20, 3244-3248.
58. Tsuji, H., Saika, H., Tsutsumi, N., Hirai, A., and Nakazono, M. (2006). Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol. 47, 995-1003.
59. Vlachonasios, K.E., Thomashow, M.F., and Triezenberg, S.J. (2003). Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell. 15, 626-638.
60. Wood, C.C., Robertson, M., Tanner, G., Peacock, W.J., Dennis, E.S., and Helliwell, C.A. (2006). The Arabidopsis thaliana vernalization response requiresapolycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl Acad. Sci. U S A. 103, 14631-14636.
61. Wu, K., Zhang, L., Zhou, C., Yu, C.W., and Chaikam, V. (2008). HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 59, 225-234.
62. Xu, C.R., Liu, C., Wang, Y.L., Li, L.C., Chen, W.Q., Xu, Z.H., and Bai, S.N. (2005). Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc. Natl Acad. Sci. U S A. 102, 14469-14474.