Plant mobile domain protein-DNA motif modules counteract Polycomb silencing to stabilize gene expression

Abstract

In plants and animals, Polycomb group proteins are crucial for development, regulating gene expression through the trimethylation of lysine 27 on histone H3 and subsequent gene silencing. While the specification of Polycomb silencing targets is increasingly understood, it remains unclear how certain genes with apparent silencing-attracting features escape this process. Here we show that the plant-mobile-domain-C-containing proteins MAINTENANCE OF MERISTEMS (MAIN), MAIN-LIKE 1 (MAIL1) and MAIL2 oppose Polycomb silencing at numerous actively transcribed genes in Arabidopsis. Mutations in MAIN, MAIL1 or MAIL2 result in Polycomb-group-dependent ectopic H3 K27 trimethylation, often associated with transcriptional repression. We show that MAIL1 (which functions in concert with MAIN) and MAIL2 target distinct gene sets and associate with chromatin at specific DNA sequence motifs. We demonstrate that the integrity of these motif sequences is essential for promoting expression and antagonizing H3 K27 trimethylation. Our results unveil a system opposing Polycomb silencing that involves plant mobile domain C protein-DNA motif modules, expanding our understanding of eukaryotic gene regulation mechanisms.