ALFIN-like proteins link histone H3K4me3 to H2A ubiquitination and coordinate diverse chromatin modifications in Arabidopsis.

Abstract

Trimethylation of histone H3K4 (H3K4me3) is widely distributed at numerous actively transcribed protein-coding genes throughout the genome. However, the interplay between H3K4me3 and other chromatin modifications in plants remains poorly understood. In this study, we show that the Arabidopsis thaliana ALFIN-LIKE (AL) proteins contain a C-terminal PHD finger capable of binding to H3K4me3 and a PHD-associated AL (PAL) domain that interacts with components of the Polycomb repressive complex 1, thereby facilitating H2A ubiquitination (H2Aub) at H3K4me3-enriched genes throughout the genome. Furthermore, we demonstrate that loss of function of SDG2, encoding a key histone H3K4 methyltransferase, leads to a reduction in H3K4me3 level, which subsequently causes a genome-wide decrease in H2Aub, revealing a strong association between H3K4me3 and H2Aub. Finally, we discover that the PAL domain of AL proteins interacts with various other chromatin-related proteins or complexes, including those involved in regulating H2A.Z deposition, H3K27me3 demethylation, histone deacetylation, and chromatin accessibility. Our genome-wide analysis suggests that the AL proteins play a crucial role in coordinating H3K4me3 with multiple other chromatin modifications across the genome.