Polycomb mutant partially suppresses DNA hypomethylation-associated phenotypes in Arabidopsis.

Martin Rougée,Angélique Deleris,Leandro Quadrana,Valentin Hure,Lionel Navarro,Vincent Colot,Jérôme Zervudacki

doi:10.26508/lsa.202000848

Abstract

In plants and mammals, DNA methylation and histone H3 lysine 27 trimethylation (H3K27me3), which is deposited by the polycomb repressive complex 2, are considered as two specialized systems for the epigenetic silencing of transposable element (TE) and genes, respectively. Nevertheless, many TE sequences acquire H3K27me3 when DNA methylation is lost. Here, we show in Arabidopsis thaliana that the gain of H3K27me3 observed at hundreds of TEs in the ddm1 mutant defective in the maintenance of DNA methylation, essentially depends on CURLY LEAF (CLF), one of two partially redundant H3K27 methyltransferases active in vegetative tissues. Surprisingly, the complete loss of H3K27me3 in ddm1 clf double mutant plants was not associated with further reactivation of TE expression nor with a burst of transposition. Instead, ddm1 clf plants exhibited less activated TEs, and a chromatin recompaction as well as hypermethylation of linker DNA compared with ddm1 Thus, a mutation in polycomb repressive complex 2 does not aggravate the molecular phenotypes linked to ddm1 but instead partially suppresses them, challenging our assumptions of the relationship between two conserved epigenetic silencing pathways.

Highlights

DNA methylation is an epigenetic mark involved in the stable silencing of transposable elements (TEs) as well as the regulation of gene expression in plants and mammals
We provided evidence supporting a role of polycomb group (PcG) in the transcriptional silencing of EVADE (EVD) (Zervudacki et al, 2018), an A. thaliana retroelement of the ATCOPIA93 family that is tightly controlled by DNA methylation and which transposes in plants mutated for the chromatin remodeler DDM1 (Tsukahara et al, 2009)
This argues for a major role of DNA methylation, in particular CG methylation, and rather than non-CG methylation associated with H3K9me2, in antagonizing polycomb repressive complex 2 (PRC2) as previously proposed (Mathieu et al, 2005; Deleris et al, 2012)

Summary

Introduction

DNA methylation is an epigenetic mark involved in the stable silencing of transposable elements (TEs) as well as the regulation of gene expression in plants and mammals. In contrast to DNA methylation, histone H3 lysine 27 trimethylation (H3K27me3), which is targeted by the highly conserved polycomb group (PcG) proteins, in particular polycomb repressive complex 2 (PRC2), is a hallmark of transcriptional repression of protein-coding and microRNA genes in plants as well as in animals (Prete et al, 2015; Forderer et al, 2016; Chica et al, 2017; Marasca et al, 2018); it is thought to act by promoting a local compaction of the chromatin that antagonizes the transcription machinery (Prete et al, 2015) to maintain transcriptional silencing (Holoch & Margueron, 2017). H3K27me and DNA methylation are generally considered as mutually exclusive chromatin marks

Methods

Results

Conclusion