Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis

Plant Journal

Volumn 62, Issue 5, 2010, Pages 796-806

  Perrella, Giorgio ^a   Consiglio, M Federica ^a   Aiese Cigliano, Riccardo ^a   Cremona, Gaetana ^a   Sanchez Moran, Eugenio ^b   Barra, Lucia ^a   Errico, Angela ^a   Bressan, Ray A ^c   Franklin, F Christopher H ^b   Conicella, Clara ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Arabidopsis; Chiasma; Chromatin organization; Histone acetylation; Meiosis

Indexed keywords

ACETYLATION; ACTIVATION ANALYSIS;

ARABIDOPSIS; CHIASMA; CHROMATIN ORGANIZATION; HISTONE ACETYLATION; MEIOSIS;

CHROMOSOMES;

ARABIDOPSIS;

EID: 77952837863     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04191.x     Document Type: Article

References (69)

1. Akiyama, T., Nagata, M. Aoki, F. (2006) Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc. Natl Acad. Sci. USA, 103, 7339 7344.
2. Alexander, M.P. (1969) Differential staining of aborted and nonaborted pollen. Stain Technol. 44, 117 122.
3. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
4. Armstrong, S.J. Jones, G.H. (2001) Female meiosis in wild type Arabidopsis thaliana and in two meiotic mutants. Sex. Plant Reprod. 13, 177 183.
5. Armstrong, S.J., Caryl, A.P., Jones, G.H. Franklin, F.C.H. (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645 3655.
6. Armstrong, S.J., Franklin, F.C.H. Jones, G.H. (2003) A meiotic time-course for Arabidopsis thaliana. Sex. Plant Reprod. 16, 141 149.
7. Aufsatz, W., Mette, M.F., Van Der Winden, J., Matzke, M. Matzke, A.J. (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21, 6832 6841.
8. Bertrand, C., Bergounioux, C., Domenichini, S., Delarue, M. Zhou, D.X. (2003) Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J. Biol. Chem. 278, 28246 28251.
9. Boateng, K.A., Yang, X., Dong, F., Owen, H.A. Makaroff, C.A. (2008) SWI1 is required for meiotic chromosome remodeling events. Mol. Plant, 1, 620 633.
10. Borde, V., Robine, N., Lin, W., Bonfils, S., Géli, B. Nicolas, A. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28, 99 111.
11. Boyes, D.C., Zaved, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. Görlach, J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell, 13, 1499 1510.
12. Buard, J., Barthès, P., Grey, C. de Massy, B. (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J. 28, 2616 2624.
13. Bui, H.T., Van Thuan, N., Kishigami, S., Wakayama, S., Hikichi, T., Ohta, H., Mizutani, E., Yamaoka, E., Wakayama, T. Miyano, T. (2007) Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes. Reproduction, 133, 371 382.
14. Burgess, S.M., Ajimura, M. Kleckner, N. (1999) GCN5-dependent histone H3 acetylation and RPD3-dependent histone H4 deacetylation have distinct, opposing effects on IME2 transcription, during meiosis and during vegetative growth, in budding yeast. Proc. Natl Acad. Sci. USA, 96, 6835 6840.
15. Choy, J.S., Tobe, B.T., Huh, J.H. Kron, S.J. (2001) Yng2p-dependent NuA4 histone H4 acetylation activity is required for mitotic and meiotic progression. J. Biol. Chem. 276, 43653 43662.
16. Cimini, D., Mattiuzzo, M., Torosantucci, L. Degrassi, F. (2003) Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol. Biol. Cell, 14, 3821 3833.
17. Copenhaver, G.P. Pikaard, C.S. (1996) RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J. 9, 259 272.
18. De La Fuente, R. (2006) Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 292, 1 12.
19. De La Fuente, R., Viveiros, M.M., Burns, K.H., Adashi, E.Y., Matzuk, M.M. Eppig, J.J. (2004) Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev. Biol. 275, 447 458.
20. Drouaud, J., Camilleri, C., Bourguignon, P.Y. et al. (2006) Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination 'hot spots.' Genome Res. 16, 106 114.
21. Ekwall, K., Olsson, T., Turner, B.M., Cranston, G. Allshire, R.C. (1997) Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell, 91, 1021 1032.
22. Eot-Houllier, G., Fulcrand, G., Watanabe, Y., Magnaghi-Jaulin, L. Jaulin, C. (2008) Histone deacetylase 3 is required for centromeric H3K4 deacetylation and sister chromatid cohesion. Genes Dev. 22, 2693 2744.
23. Fenic, I., Sonnack, V., Failing, K., Bergmann, M. Steger, K. (2004) In vivo effects of histone-deacetylase inhibitor trichostatin-A on murine spermatogenesis. J. Androl. 25, 811 818.
24. Gottlieb, S. Esposito, R.E. (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell, 56, 771 776.
25. Higgins, J.D., Armstrong, S.J., Franklin, F.C. Jones, G.H. (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18, 2557 2570.
26. Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Jones, G.H. Franklin, F.C. (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 15, 2488 2500.
27. Hirota, K., Mizuno, K., Shibata, T. Ohta, K. (2008) Distinct chromatin modulators regulate the formation of accessible and repressive chromatin at the fission yeast recombination hotspot ade6-M26. Mol. Biol. Cell, 19, 1162 1173.
28. Ishii, S., Kurasawa, Y., Wong, J. Yu-Lee, L.Y. (2008) Histone deacetylase 3 localizes to the mitotic spindle and is required for kinetochore-microtubule attachment. Proc. Natl Acad. Sci. USA, 105, 4179 4184.
29. Ishitani, M., Xiong, L., Stevenson, B. Zhu, J.K. (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell, 9, 1935 1949.
30. Jenuwein, T. Allis, C.D. (2001) Translating the histone code. Science, 293, 1074 1080.
31. Koiwa, H., Barb, A.W., Xiong, L. et al. (2002) C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc. Natl Acad. Sci. USA, 99, 10893 10898.
32. Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693 705.
33. Lam, S.Y., Horn, S.R., Radford, S.J., Housworth, E.A., Stahl, F.W. Copenhaver, G.P. (2005) Crossover interference on nucleolus organizing region-bearing chromosomes in Arabidopsis. Genetics, 170, 807 812.
34. Latrasse, D., Benhamed, M., Henry, Y., Domenichini, S., Kim, W., Zhou, D.X. Delarue, M. (2008) The MYST histone acetyltransferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol. 8, 121.
35. Li, Y., Butenko, Y. Grafi, G. (2005) Histone deacetylation is required for progression through mitosis in tobacco cells. Plant J. 41, 346 352.
36. Liu, Y., Mitsukawa, N., Oosumi, T. Whitter, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457 463.
37. Lohr, D., Kovacic, R.T. Van Holde, K.E. (1977) Quantitative analysis of the digestion of yeast chromatin by staphylococcal nuclease. Biochemistry, 16, 463 471.
38. Magnaghi-Jaulin, L. Jaulin, C. (2006) Histone deacetylase activity is necessary for chromosome condensation during meiotic maturation in Xenopus laevis. Chromosome Res. 14, 319 332.
39. Merker, J.D., Dominska, M., Greewell, P.W., Rinella, E., Bouck, D.C., Shibata, Y., Strahl, B.D., Mieczkowski, P. Petes, T.D. (2008) The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae. DNA Repair, 7, 1298 1308.
40. Mieczkowski, P.A., Dominska, M., Buck, M.J., Lieb, J.D. Petes, T.D. (2007) Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 104, 3955 3960.
41. Millar, C.B. Grunstein, M. (2006) Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 7, 657 666.
42. Murphy, J.P., McAleer, J.P., Uglialoro, A., Papile, J., Weniger, J., Bethelmie, F. Tramontano, W.A. (2000) Histone deacetylase inhibitors and cell proliferation in pea root meristems. Phytochemistry, 55, 11 18.
43. Pandey, R., Muller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W. Jorgensen, R.A. (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30, 5036 5055.
44. Perrella, G., Cremona, G., Consiglio, F., Errico, A., Bressan, R.A. Conicella, C. (2006) Screening for mutations affecting sexual reproduction after activation tagging in Arabidopsis thaliana. J. Appl. Genet. 47, 109 111.
45. Probst, A.V., Fagard, M., Proux, F. et al. (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell, 16, 1021 1034.
46. Ross, K.J., Fransz, P. Jones, G.H. (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507 516.
47. Sanchez-Moran, E., Armstrong, S.J., Santos, J.L., Franklin, C.H. Jones, G.H. (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9, 121 128.
48. Sanchez-Moran, E., Jones, G.H., Franklin, C.H. Santos, J.L. (2004) A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. Plant Cell, 16, 2895 2909.
49. Sanchez-Moran, E., Santos, J.L., Jones, G.H. Franklin, C.H. (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21, 2220 2233.
50. Santos, J.L., Alfaro, D., Sanchez-Moran, E., Armstrong, S.J., Franklin, F.C.H. Jones, G.H. (2003) Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics, 165, 1533 1540.
51. Schardl, C.L., Bvrd, A.D., Benzion, G., Altschuler, M.A., Hildebrand, D.F. Hunt, A.G. (1987) Design and construction of a versatile system for the expression of foreign genes in plants. Gene, 61, 1 11.
52. Schneitz, K., Hülskamp, M. Pruitt, R.E. (1995) Wild type ovule development in Arabidopsis thaliana- a light microscope study of cleared whole-mount tissue. Plant J. 7, 731 749.
53. Seo, H., Masuoka, M., Murofushi, H., Takeda, S., Shibata, T. Ohta, K. (2005) Rapid generation of specific antibodies by enhanced homologous recombination. Nat. Biotechnol. 23, 731 735.
54. Sharma, A.K. Sharma, A. (1980) Processing. In Chromosome Techniques.
55. Shogren-Knaak, M., Ishii, H., Sun, J.M., Pazin, M.J., Davie, J.R. Peterson, C.L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 311, 844 847.
56. Smith, C.M., Gafken, P.R., Zhang, Z., Gottschling, D.E., Smith, J.B. Smith, D.L. (2003) Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal. Biochem. 316, 23 33.
57. Smyth, D.R., Bowman, J.L. Meyerowitz, E.M. (1990) Early flower development in Arabidopsis. Plant Cell, 8, 755 767.
58. Strahl, B.D. Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41 45.
59. Taddei, A., Maison, C., Roche, D. Almouzni, G. (2001) Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol. 3, 114 120.
60. Tian, L., Wang, J., Fong, M.P., Chen, M., Cao, H., Gelvin, S.B. Chen, Z.J. (2003) Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. Genetics, 165, 399 409.
61. Verdel, A., Seigneurin-Berny, D., Faure, A.K., Eddahbi, M., Khochbin, S. Nonchev, S. (2003) HDAC6-induced premature chromatin compaction in mouse oocytes and fertilised eggs. Zygote, 11, 323 328.
62. Vlachonasios, K.E., Thomashow, M.F. 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.
63. Wang, Q., Yin, S., Ai, J.S., Liang, C.G., Hou, Y., Chen, D.Y., Schatten, H. Sun, Q.Y. (2006) Histone deacetylation is required for orderly meiosis. Cell Cycle, 5, 766 774.
64. Weigel, D., Ahn, J.H., Blázquez, M.A. et al. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003 1113.
65. Wu, K., Tian, L., Malik, K., Brown, D. Miki, B. (2000) Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant J. 22, 19 27.
66. Wu, K., Zhang, L., Zhou, C., Yu, C.W. Chaikam, V. (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 59, 225 234.
67. Yamada, T., Mizuno, K.I., Hirota, K., Kon, N., Wahls, W.P., Hartsuiker, E., Murofushi, H., Shibata, T. Ohta, K. (2004) Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J. 23, 1792 1803.
68. Yang, X., Timofejeva, L., Ma, H. Makaroff, C.A. (2006) The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J. Cell Sci. 119, 3754 3763.
69. Zickler, D. Kleckner, N. (1998) The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619 697.