Dimethylation of Histone H3 Lysine 9 is a Critical Mark for DNA Methylation and Gene Silencing in Arabidopsis Thaliana

Overview

Journal Chromosoma

Specialty Molecular Biology

Date 2004 Mar 12

PMID 15014946

Citations 140

Authors

James P Jackson

Lianna Johnson

Zuzana Jasencakova

Xing Zhang

Laura PerezBurgos

Prim B Singh

Xiaodong Cheng

Ingo Schubert

Thomas Jenuwein

Steven E Jacobsen

Affiliations

Soon will be listed here.

Abstract

The Arabidopsis KRYPTONITE gene encodes a member of the Su(var)3-9 family of histone methyltransferases. Mutations of kryptonite cause a reduction of methylated histone H3 lysine 9, a loss of DNA methylation, and reduced gene silencing. Lysine residues of histones can be either monomethylated, dimethylated or trimethylated and recent evidence suggests that different methylation states are found in different chromatin domains. Here we show that bulk Arabidopsis histones contain high levels of monomethylated and dimethylated, but not trimethylated histone H3 lysine 9. Using both immunostaining of nuclei and chromatin immunoprecipitation assays, we show that monomethyl and dimethyl histone H3 lysine 9 are concentrated in heterochromatin. In kryptonite mutants, dimethyl histone H3 lysine 9 is nearly completely lost, but monomethyl histone H3 lysine 9 levels are only slightly reduced. Recombinant KRYPTONITE can add one or two, but not three, methyl groups to the lysine 9 position of histone H3. Further, we identify a KRYPTONITE-related protein, SUVH6, which displays histone H3 lysine 9 methylation activity with a spectrum similar to that of KRYPTONITE. Our results suggest that multiple Su(var)3-9 family members are active in Arabidopsis and that dimethylation of histone H3 lysine 9 is the critical mark for gene silencing and DNA methylation.

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References

Peters A, Kubicek S, Mechtler K, OSullivan R, Derijck A, Perez-Burgos L . Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell. 2003; 12(6):1577-89. DOI: 10.1016/s1097-2765(03)00477-5. View

Ng H, Robert F, Young R, Struhl K . Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell. 2003; 11(3):709-19. DOI: 10.1016/s1097-2765(03)00092-3. View

Waterborg J . Sequence analysis of acetylation and methylation in two histone H3 variants of alfalfa. J Biol Chem. 1990; 265(28):17157-61. View

Nakayama J, Rice J, Strahl B, Allis C, Grewal S . Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science. 2001; 292(5514):110-3. DOI: 10.1126/science.1060118. View

Richards E, Elgin S . Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell. 2002; 108(4):489-500. DOI: 10.1016/s0092-8674(02)00644-x. View

Martienssen R, Colot V . DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science. 2001; 293(5532):1070-4. DOI: 10.1126/science.293.5532.1070. View

Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M . G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 2002; 16(14):1779-91. PMC: 186403. DOI: 10.1101/gad.989402. View

Wang H, An W, Cao R, Xia L, Erdjument-Bromage H, Chatton B . mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Mol Cell. 2003; 12(2):475-87. DOI: 10.1016/j.molcel.2003.08.007. View

Johnson L, Cao X, Jacobsen S . Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol. 2002; 12(16):1360-7. DOI: 10.1016/s0960-9822(02)00976-4. View

10.

Rea S, Eisenhaber F, OCarroll D, Strahl B, Sun Z, Schmid M . Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000; 406(6796):593-9. DOI: 10.1038/35020506. View

11.

Strahl B, Allis C . The language of covalent histone modifications. Nature. 2000; 403(6765):41-5. DOI: 10.1038/47412. View

12.

Malagnac F, Bartee L, Bender J . An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 2002; 21(24):6842-52. PMC: 139107. DOI: 10.1093/emboj/cdf687. View

13.

Baumbusch L, Thorstensen T, Krauss V, Fischer A, NAUMANN K, Assalkhou R . The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 2001; 29(21):4319-33. PMC: 60187. DOI: 10.1093/nar/29.21.4319. View

14.

Turner B . Histone acetylation and an epigenetic code. Bioessays. 2000; 22(9):836-45. DOI: 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X. View

15.

Cowell I, Aucott R, Mahadevaiah S, Burgoyne P, Huskisson N, Bongiorni S . Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma. 2002; 111(1):22-36. DOI: 10.1007/s00412-002-0182-8. View

16.

Tamaru H, Zhang X, McMillen D, Singh P, Nakayama J, Grewal S . Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet. 2003; 34(1):75-9. DOI: 10.1038/ng1143. View

17.

TSCHIERSCH B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G . The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994; 13(16):3822-31. PMC: 395295. DOI: 10.1002/j.1460-2075.1994.tb06693.x. View

18.

Tachibana M, Sugimoto K, Fukushima T, Shinkai Y . Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem. 2001; 276(27):25309-17. DOI: 10.1074/jbc.M101914200. View

19.

Jasencakova Z, Soppe W, Meister A, Gernand D, Turner B, Schubert I . Histone modifications in Arabidopsis- high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J. 2003; 33(3):471-80. DOI: 10.1046/j.1365-313x.2003.01638.x. View

20.

Rice J, Briggs S, Ueberheide B, Barber C, Shabanowitz J, Hunt D . Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell. 2003; 12(6):1591-8. DOI: 10.1016/s1097-2765(03)00479-9. View