DNA methylation either antagonizes or promotes Polycomb recruitment at transposable elements
Transposable elements (TEs) are usually silenced by DNA methylation and H3K9me2, but in the absence of DNA methylation they can instead acquire the Polycomb-associated mark H3K27me3. Here, we initially set out to test whether DNA methylation and H3K27me3 compete during TE silencing establishment in Arabidopsis. Although this competition was confirmed at one newly inserted transgenic TE, we unexpectedly found that H3K27me3 deposition at another neo-inserted TE required the de novo methyltransferase DRM2, revealing that DNA methylation can also promote Polycomb recruitment. Genome-wide H3K27me3 profiling in drm2, met1, and rdd mutants showed that DNA methylation either antagonizes or promotes H3K27me3 in a locus-specific manner, and that DNA demethylation also shapes H3K27me3 levels in vegetative tissues. Targeted methylation experiments demonstrated that DNA methylation directly influences PcG recruitment, while analyses using a DRM2 catalytic mutant confirmed that this effect depends on DNA methylation itself. Overall, our work reveals an unexpected, cooperative crosstalk between DNA methylation and Polycomb pathways to maintain genome and epigenome integrity in eukaryotes.