title: The SUVR4 histone lysine methyltransferase binds ubiquitin and converts H3K9me1 to H3K9me3 on transposon chromatin in Arabidopsis.
abstract: Chromatin structure and gene expression are regulated by posttranslational modifications (PTMs) on the N-terminal tails of histones. Mono-, di-, or trimethylation of lysine residues by histone lysine methyltransferases (HKMTases) can have activating or repressive functions depending on the position and context of the modified lysine. In Arabidopsis, trimethylation of lysine 9 on histone H3 (H3K9me3) is mainly associated with euchromatin and transcribed genes, although low levels of this mark are also detected at transposons and repeat sequences. Besides the evolutionarily conserved SET domain which is responsible for enzyme activity, most HKMTases also contain additional domains which enable them to respond to other PTMs or cellular signals. Here we show that the N-terminal WIYLD domain of the Arabidopsis SUVR4 HKMTase binds ubiquitin and that the SUVR4 product specificity shifts from di- to trimethylation in the presence of free ubiquitin, enabling conversion of H3K9me1 to H3K9me3 in vitro. Chromatin immunoprecipitation and immunocytological analysis showed that SUVR4 in vivo specifically converts H3K9me1 to H3K9me3 at transposons and pseudogenes and has a locus-specific repressive effect on the expression of such elements. Bisulfite sequencing indicates that this repression involves both DNA methylation-dependent and -independent mechanisms. Transcribed genes with high endogenous levels of H3K4me3, H3K9me3, and H2Bub1, but low H3K9me1, are generally unaffected by SUVR4 activity. Our results imply that SUVR4 is involved in the epigenetic defense mechanism by trimethylating H3K9 to suppress potentially harmful transposon activity.
authors.affiliation: Department of Molecular Biosciences, University of Oslo, Oslo, Norway.
authors.forename: Silje V
authors.initials: SV
authors.lastname: Veiseth
authors.forename: Mohummad A
authors.initials: MA
authors.lastname: Rahman
authors.forename: Kyoko L
authors.initials: KL
authors.lastname: Yap
authors.forename: Andreas
authors.initials: A
authors.lastname: Fischer
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Egge-Jacobsen
authors.forename: Gunter
authors.initials: G
authors.lastname: Reuter
authors.forename: Ming-Ming
authors.initials: MM
authors.lastname: Zhou
authors.forename: Reidunn B
authors.initials: RB
authors.lastname: Aalen
authors.forename: Tage
authors.initials: T
authors.lastname: Thorstensen
mesh_terms: D020816:Amino Acid Motifs; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002843:Chromatin / Q000378:metabolism*; D004251:DNA Transposable Elements / Q000235:genetics*; D010450:Endopeptidases / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D011495:Histone-Lysine N-Methyltransferase / Q000235:genetics / Q000378:metabolism*; D006657:Histones / Q000378:metabolism*; D008745:Methylation; D008969:Molecular Sequence Data; D016297:Mutagenesis, Site-Directed; D011485:Protein Binding; D017434:Protein Structure, Tertiary; D011994:Recombinant Proteins / Q000235:genetics / Q000378:metabolism*; D013379:Substrate Specificity; D014158:Transcription, Genetic; D020798:Two-Hybrid System Techniques; D025801:Ubiquitin / Q000378:metabolism*; D064570:Ubiquitin-Specific Proteases; D054875:Ubiquitination
chemical_list: D029681:Arabidopsis Proteins; D002843:Chromatin; D004251:DNA Transposable Elements; D006657:Histones; D011994:Recombinant Proteins; D025801:Ubiquitin; D011495:Histone-Lysine N-Methyltransferase; C515570:SUVR4 protein, Arabidopsis; D010450:Endopeptidases; D064570:Ubiquitin-Specific Proteases