Abstract
Dimethylation of histone H3 lysine 9 (H3K9m2) and trimethylation of histone H3 lysine 27 (H3K27m3) are two hallmarks of transcriptional repression in many organisms. In Arabidopsis thaliana, H3K27m3 is targeted by Polycomb Group (PcG) proteins and is associated with silent protein-coding genes, while H3K9m2 is correlated with DNA methylation and is associated with transposons and repetitive sequences. Recently, ectopic genic DNA methylation in the CHG context (where H is any base except G) has been observed in globally DNA hypomethylated mutants such as met1, but neither the nature of the hypermethylated loci nor the biological significance of this epigenetic phenomenon have been investigated. Here, we generated high-resolution, genome-wide maps of both H3K9m2 and H3K27m3 in wild-type and met1 plants, which we integrated with transcriptional data, to explore the relationships between these two marks. We found that ectopic H3K9m2 observed in met1 can be due to defects in IBM1-mediated H3K9m2 demethylation at some sites, but most importantly targets H3K27m3-marked genes, suggesting an interplay between these two silencing marks. Furthermore, H3K9m2/DNA-hypermethylation at these PcG targets in met1 is coupled with a decrease in H3K27m3 marks, whereas CG/H3K9m2 hypomethylated transposons become ectopically H3K27m3 hypermethylated. Our results bear interesting similarities with cancer cells, which show global losses of DNA methylation but ectopic hypermethylation of genes previously marked by H3K27m3.
Highlights
Post-transcriptional modifications of histone tails—and combinations thereof—are thought to define specific chromatin structures and transcriptional states across eukaryotes [1,2]
While significant H3K9 hypermethylation was observed in the first generation of ibm1 mutants, this phenomenon only become clearly apparent in the second generation of met1 mutant
We found that the set of genes that are H3K9 hypermethylated in met1 in our experiment displayed increased levels of non-CG methylation, in the CHG context, at individual loci and in a genome-wide manner (Figure 1A, Figure 1B, Figure S1)
Summary
Post-transcriptional modifications of histone tails—and combinations thereof—are thought to define specific chromatin structures and transcriptional states across eukaryotes [1,2]. In both animals and plants, trimethylation of histone 3 lysine 27 (H3K27) and dimethylation of histone 3 lysine 9 (H3K9) (and/or trimethylation in metazoa) are two, generally alternative, hallmarks of transcriptional repression. H3K27m3 was found to mark selected transposons and repeated sequences in some particular contexts when they are DNA hypomethylated such as in the met mutants [6] or in endosperms [7]. Establishment of cytosine methylation in all sequence contexts is catalyzed by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2), the plant homolog of mammalian DNMT3a and DNMT3b.
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