Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL

Rui Liu,Xuehua Zhong,Ray N Scheid,Shuiming Qian,Li Lu,Xinchen Lv,Zhenlin Yang,Jiamu Du,Melissa D Boersma,John M Denu,Wei Chen

doi:10.1038/s41467-018-04836-y

Abstract

The ability of a cell to dynamically switch its chromatin between different functional states constitutes a key mechanism regulating gene expression. Histone mark “readers” display distinct binding specificity to different histone modifications and play critical roles in regulating chromatin states. Here, we show a plant-specific histone reader SHORT LIFE (SHL) capable of recognizing both H3K27me3 and H3K4me3 via its bromo-adjacent homology (BAH) and plant homeodomain (PHD) domains, respectively. Detailed biochemical and structural studies suggest a binding mechanism that is mutually exclusive for either H3K4me3 or H3K27me3. Furthermore, we show a genome-wide co-localization of SHL with H3K27me3 and H3K4me3, and that BAH-H3K27me3 and PHD-H3K4me3 interactions are important for SHL-mediated floral repression. Together, our study establishes BAH-PHD cassette as a dual histone methyl-lysine binding module that is distinct from others in recognizing both active and repressive histone marks.

Highlights

The ability of a cell to dynamically switch its chromatin between different functional states constitutes a key mechanism regulating gene expression
We show a genome-wide co-localization of SHORT LIFE (SHL) with H3K27me[3] and H3K4me[3], and that bromo-adjacent homology (BAH)-H3K27me[3] and plant homeodomain (PHD)-H3K4me[3] interactions are important for SHL-mediated floral repression
While EARLY BOLTING IN SHORT DAYS (EBS) regulates the expression of a floral integrator FLOWERING LOCUS T (FT), SHL has been shown to repress another floral integrator SUPPRESSION OF OVEREXPRESSION OF CO1 (SOC1) to inhibit flowering[33, 35]

Summary

Introduction

The ability of a cell to dynamically switch its chromatin between different functional states constitutes a key mechanism regulating gene expression. We show a plant-specific histone reader SHORT LIFE (SHL) capable of recognizing both H3K27me[3] and H3K4me[3] via its bromo-adjacent homology (BAH) and plant homeodomain (PHD) domains, respectively. Our study establishes BAH-PHD cassette as a dual histone methyl-lysine binding module that is distinct from others in recognizing both active and repressive histone marks. In Arabidopsis, the BAH and PHD dual domain-containing proteins SHORT LIFE (SHL) and EARLY BOLTING IN SHORT DAYS (EBS) function in chromatin-mediated floral repression and seed dormancy[33,34,35,36,37]. Our biochemical and X-ray structural studies show that SHL is capable of recognizing an active histone mark H3K4me[3] and a repressive mark H3K27me[3] independently via its PHD and BAH domain, respectively. We establish a single protein-mediated dual histone mark recognition and provide insights into establishing and maintaining proper chromatin landscapes

Methods

Results

Conclusion