The Arabidopsis histone H3K4me3-binding ALFIN-like proteins mediate histone H2A ubiquitination and coordinate diverse chromatin modifications

Abstract

The histone H3K4 trimethylation (H3K4me3) is widely distributed at numerous actively transcribed protein-coding genes throughout the genome. However, the interplay between H3K4me3 and other chromatin modifications remains poorly understood in plants. In this study, we find that the Arabidopsis thaliana H3K4me3-binding ALFIN-LIKE (AL) proteins are associated with H3K4me3-enriched genes at the whole-genome level. The AL proteins contain a C-terminal PHD finger, which has a conserved role in recognizing H3K4me3, and a PHD-associated AL (PAL) domain, which is responsible for binding to diverse chromatin-related proteins. We demonstrate that the AL proteins not only act as subunits of the Polycomb repressive complex 1 (PRC1) to mediate H2A ubiquitination at H3K4me3-enriched genes but also interact with a variety of other chromatin-related proteins. Furthermore, we elucidate the mechanisms by which AL proteins interact with other chromatin-associated proteins to integrate H3K4me3, H2A ubiquitination, H2A.Z deposition, H3K27 demethylation, and chromatin accessibility across the genome. These findings underscore the critical role of AL proteins in linking H3K4me3 with a variety of other chromatin modifications in plants.