Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A.Z deposition

Magdalena E Potok,Shima Rayatpisheh,Wanlu Liu,Linhao Xu,Israel Ausin,Zhenhui Zhong,Bilguudei Naranbaatar,James A Wohlschlegel,Steven E Jacobsen,Suhua Feng,Zonghua Wang,Yafei Wang

doi:10.1038/s41467-019-11291-w

Abstract

Deposition of the histone variant H2A.Z by the SWI2/SNF2-Related 1 chromatin remodeling complex (SWR1-C) is important for gene regulation in eukaryotes, but the composition of the Arabidopsis SWR1-C has not been thoroughly characterized. Here, we aim to identify interacting partners of a conserved Arabidopsis SWR1 subunit ACTIN-RELATED PROTEIN 6 (ARP6). We isolate nine predicted components and identify additional interactors implicated in histone acetylation and chromatin biology. One of the interacting partners, methyl-CpG-binding domain 9 (MBD9), also strongly interacts with the Imitation SWItch (ISWI) chromatin remodeling complex. MBD9 is required for deposition of H2A.Z at a distinct subset of ARP6-dependent loci. MBD9 is preferentially bound to nucleosome-depleted regions at the 5’ ends of genes containing high levels of activating histone marks. These data suggest that MBD9 is a SWR1-C interacting protein required for H2A.Z deposition at a subset of actively transcribing genes.

Highlights

Deposition of the histone variant H2A.Z by the SWI2/SNF2-Related 1 chromatin remodeling complex (SWR1-C) is important for gene regulation in eukaryotes, but the composition of the Arabidopsis SWR1-C has not been thoroughly characterized
We focus on characterizing methyl-CpGbinding domain 9 (MBD9), a protein implicated in flowering time regulation[55]
We identified nine Arabidopsis proteins that are homologous to subunits common to the yeast (SWR1) and mammalian (SRCAP)

Summary

Introduction

Deposition of the histone variant H2A.Z by the SWI2/SNF2-Related 1 chromatin remodeling complex (SWR1-C) is important for gene regulation in eukaryotes, but the composition of the Arabidopsis SWR1-C has not been thoroughly characterized. MBD9 is a SWR1-C interacting protein required for H2A.Z deposition at a subset of actively transcribing genes. When present in the active genes of some organisms, the levels of H2A.Z at the TSS positively correlate with gene expression, typically when found together with H3/H4 acetylation, marks of active transcription[10,11,12,13]. In Arabidopsis, genes bearing high levels of gene body DNA methylation tend to be long and highly expressed, and show H2A.Z enrichment at their 5′-ends overlapping with activating histone modifications[17,22,23,24].

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