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RESEARCH PAPER
1 Institute of Genetics, Biologicum, Martin Luther University Halle, D-06120 Halle, Germany; 2 Research Institute of Molecular Pathology (IMP), The Vienna Biocenter, A-1030, Austria; 3 Department of Genetics, University of Leipzig, D-04103 Leipzig, Germany
Histone lysine methylation is an epigenetic mark to index chromosomal subdomains. In Drosophila, H3-K9 di- and trimethylation is mainly controlled by the heterochromatic SU(VAR)3-9 HMTase, a major regulator of position-effect variegation (PEV). In contrast, H3-K27 methylation states are independently mediated by the Pc-group enzyme E(Z). Isolation of 19 point mutants demonstrates that the silencing potential of Su(var)3-9 increases with its associated HMTase activity. A hyperactive Su(var)3-9 mutant, pitkinD, displays extensive H3-K9 di- and trimethylation within but also outside pericentric heterochromatin. Notably, mutations in a novel Su(var) gene, Su(var)3-1, severely restrict Su(var)3-9-mediated gene silencing. Su(var)3-1 was identified as "antimorphic" mutants of the euchromatic H3-S10 kinase JIL-1. JIL-1Su(var)3-1 mutants maintain kinase activity and do not detectably impair repressive histone lysine methylation marks. However, analyses with seven different PEV rearrangements demonstrate a general role of JIL-1Su(var)3-1 in controlling heterochromatin compaction and expansion. Our data provide evidence for a dynamic balance between heterochromatin and euchromatin, and define two distinct mechanisms for Su(var) gene function. Whereas the majority of Su(var)s encode inherent components of heterochromatin that can establish repressive chromatin structures [intrinsic Su(var)s], Su(var)3-1 reflects gain-of-function mutants of a euchromatic component that antagonize the expansion of heterochromatic subdomains [acquired Su(var)s].
[Keywords: Su(var) genes; Su(var)3-9; JIL-1; heterochromatin; position-effect variegation; histone lysine methylation]
Received April 30, 2004; revised version accepted September 21, 2004.
Article and publication are at http://www.genesdev.org/cgi/doi/10.1101/gad.323004.
4 These authors contributed equally to this work.
5 Corresponding author.
E-MAIL reuter{at}genetik.uni-halle.de; FAX 49-0-345-55-27294.
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