DNA methylation either antagonizes or promotes Polycomb recruitment at transposable elements in Arabidopsis

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 we observe this competition at one newly inserted transgenic TE, we remarkably find that H3K27me3 deposition at another neo-inserted TE requires the de novo methyltransferase DRM2, revealing that DNA methylation can also promote Polycomb recruitment. Accordingly, genome-wide H3K27me3 profiling in different DNA methylation mutants shows that DNA methylation either antagonizes or promotes H3K27me3 in a locus-specific manner. Targeted DNA methylation experiments as well as the use of a drm2 catalytic mutant further demonstrate that DNA methylation directly influences Polycomb recruitment. Overall, our work reveals a previously unappreciated interplay between DNA methylation and Polycomb pathways that maintains genome and epigenome integrity in eukaryotes.