Arabidopsis SDG proteins mediate Polycomb removal and transcription-coupled H3K36 methylation for gene activation

Abstract Polycomb Repressive Complex 2 (PRC2) recognizes Polycomb response elements (PREs) and catalyzes trimethylation of histone H3 on lysine 27 (H3K27me3) for gene silencing. This silencing is counteracted by H3K36 methylation for epigenetic activation of gene expression. Here, we show that the Arabidopsis thaliana H3K36 methyltransferases SET DOMAIN-CONTAINING PROTEIN 7 (SDG7) and SDG8 antagonize PRC2-mediated silencing and establish H3K36 methylation patterns with the general transcription machinery. The sdg7 sdg8 double mutant shows developmental defects and lower H3K36me2 and H3K36me3 levels. SDG7 preferentially binds near PREs, but SDG8 is recruited to H3K36 methylation peaks. The sdg7 sdg8 phenotypes are partially rescued by loss of Polycomb function. SDG7 overlaps with PRC2 and its recruiters on chromatin and evicts them from shared target genes when conditionally induced. SDG8 and RNA Polymerase II associate at SDG- and RNA POLYMERASE II ASSOCIATED FACTOR 1 complex-regulated targets for H3K36 methylation and transcription. These results suggest that SDG proteins evict PRC2 from PREs to prevent H3K27me3 deposition and activate target genes via transcription-coupled H3K36 methylation.