Specifications of Targeting Heterochromatin Modifications in Plants

Abstract

Plants encode a diverse repertoire of DNA methyltransferases that have specialized to target cytosines for methylation in specific sequence contexts. These include the de novo methyltransferase, DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2), which methylates cytosines in all sequence contexts through an RNA-guided process, the CHROMOMETHYLASES (CMTs), which methylate CHH and CHG cytosines (where H is A, T, or C), and METHYLTRANSFERASE 1 (MET1), which maintains methylation of symmetrical CG contexts. In this review, we discuss the sequence specificities and targeting of each of these pathways. In particular, we highlight recent studies that indicate CMTs preferentially target CWG or CWA/CAW motifs (where W is A or T), and discuss how self-reinforcing feedback loops between DNA methyltransferases and histone modifications characteristic of heterochromatin specify targeting. Finally, the initiating events that lead to gene body methylation are discussed as a model illustrating how interdependent targeting of different silencing pathways can potentiate the establishment of off-target epialleles.

Crosstalk between epigenetic silencing and infection by tobacco rattle virus in Arabidopsis

“…Our analysis identified a preponderance of hypomethylated DMRs that was consistent with the induction of the demethylase ROS1. In addition, repression of MET1 and DRM2‐associated AGO4 or AGO6 may contribute to hypomethylation by negatively impacting maintenance of CG and CHH methylation, respectively, in infected inflorescences (Panda et al ., ; Wendte and Schmitz, ).…”

“…In plants, DNA methylation targets mainly transposable elements (TEs) and repetitive DNA sequences, and plays essential roles in maintaining genome stability and regulating gene expression (Matzke and Mosher, ; Matzke et al ., ). RNA‐directed DNA methylation (RdDM) initiates and re‐establishes silencing of TEs through de novo methylation of cytosines (Panda et al ., ; Wendte and Pikaard, ; Wendte and Schmitz, ). The ‘non‐canonical’ RdDM pathway entails Pol II transcription at DNA loci without epigenetic marks, synthesis of double‐stranded RNA (dsRNA) by RNA‐DEPENDENT RNA POLYMERASE 6 (RDR6), production of 21‐ to 24‐nt siRNAs by RNase III‐like DICER‐LIKE 2 (DCL2), DCL3 or DCL4, and recruitment by ARGONAUTE 4 (AGO4) (Duan et al ., ; Gao et al ., ; Mari‐Ordonez et al ., ; McCue et al ., ; Nuthikattu et al ., ; Panda and Slotkin, ; Panda et al ., ; Stroud et al ., ).…”

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

“…Furthermore, histone modifications, including histone H3 Lys9 methylation (H3K9me), are tightly linked to non-CG methylation, and are associated with repressive chromatin states [16]. Chromatin with these modifications results in the formation of a condensed repressive chromatin structure called heterochromatin [16][17][18], commonly associated with most TE sequences. The chromatin remodeler Decrease in DNA Methylation 1 (DDM1) is required for the maintenance of heterochromatin [19][20][21].…”

Neuronal non-CG methylation is an essential target for MeCP2 function

“…Recent studies have explored the abundance of methylation at CH sites. Unlike plants, which have specific DNA methyltransferases that target CHG and CHH sites (Wendte and Schmitz, 2018), mCH in mammals relies on 'off-target' activity by DNMT3A and DNMT3B (Gabel et al, 2015;Guo et al, 2014;Lister et al, 2013;Ramsahoye et al, 2000;Stroud et al, 2017). There appears to be no mechanism to maintain asymmetrical CH methylation, however, which means that CH methylation is lost in replicating cells (He and Ecker, 2015).…”