Abstract
Histone H3 lysine-4 (H3K4) methylation is associated with transcribed genes in eukaryotes. In Drosophila and mammals, both di- and tri-methylation of H3K4 are associated with gene activation. In contrast to animals, in Arabidopsis H3K4 trimethylation, but not mono- or di-methylation of H3K4, has been implicated in transcriptional activation. H3K4 methylation is catalyzed by the H3K4 methyltransferase complexes known as COMPASS or COMPASS-like in yeast and mammals. Here, we report that Arabidopsis homologs of the COMPASS and COMPASS-like complex core components known as Ash2, RbBP5, and WDR5 in humans form a nuclear subcomplex during vegetative and reproductive development, which can associate with multiple putative H3K4 methyltransferases. Loss of function of ARABIDOPSIS Ash2 RELATIVE (ASH2R) causes a great decrease in genome-wide H3K4 trimethylation, but not in di- or mono-methylation. Knockdown of ASH2R or the RbBP5 homolog suppresses the expression of a crucial Arabidopsis floral repressor, FLOWERING LOCUS C (FLC), and FLC homologs resulting in accelerated floral transition. ASH2R binds to the chromatin of FLC and FLC homologs in vivo and is required for H3K4 trimethylation, but not for H3K4 dimethylation in these loci; overexpression of ASH2R causes elevated H3K4 trimethylation, but not H3K4 dimethylation, in its target genes FLC and FLC homologs, resulting in activation of these gene expression and consequent late flowering. These results strongly suggest that H3K4 trimethylation in FLC and its homologs can activate their expression, providing concrete evidence that H3K4 trimethylation accumulation can activate eukaryotic gene expression. Furthermore, our findings suggest that there are multiple COMPASS-like complexes in Arabidopsis and that these complexes deposit trimethyl but not di- or mono-methyl H3K4 in target genes to promote their expression, providing a molecular explanation for the observed coupling of H3K4 trimethylation (but not H3K4 dimethylation) with active gene expression in Arabidopsis.
Highlights
Histone lysine methylation regulates chromatin structure and gene transcription in eukaryotes
In the flowering plant Arabidopsis only H3K4 trimethylation has been implicated in gene transcriptional activation
H3K4 methylation is catalyzed by the H3K4 methyltransferase complexes known as COMPASS-like in mammals
Summary
Histone lysine methylation regulates chromatin structure and gene transcription in eukaryotes. Various lysine residues on histones can be methylated and the e-amino group of lysines can be mono-, di- and tri-methylated. Lysine methylation is linked with transcriptional activation or repression depending on the particular residue that is methylated and the degree of methylation [1]. H3 lysine-27 trimethylation (H3K27me3) is exclusively involved in transcriptional repression, whereas H3K4 trimehtylation is associated with actively transcribed genes [2]. Recent genome-scale analyses of H3K4 methylation have revealed that different H3K4 methylation states are often associated with distinct transcription states in a gene. In the well-studied Saccharomyces cerevisiae, H3K4 trimethylation is a mark for actively transcribed genes, whereas mono- or di-methylation of H3K4 is not linked with active gene expression [3]. In the higher plant Arabidopsis thaliana, only H3K4 trimethylation, but not mono- or di-methylation of H3K4, is implicated in transcriptional activation [6]
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