Arabidopsis Trithorax histone methyltransferases are redundant in regulating development and DNA methylation

Abstract

Although the Trithorax histone methyltransferases ATX1–5 are known to regulate development and stress responses by catalyzing histone H3K4 methylation in Arabidopsis thaliana, it is unknown whether and how these histone methyltransferases affect DNA methylation. Here, we found that the redundant ATX1–5 proteins are not only required for plant development and viability but also for the regulation of DNA methylation. The expression and H3K4me3 levels of both RNA‐directed DNA methylation (RdDM) genes (NRPE1, DCL3, IDN2, and IDP2) and active DNA demethylation genes (ROS1, DML2, and DML3) were downregulated in the atx1/2/4/5 mutant. Consistent with the facts that the active DNA demethylation pathway mediates DNA demethylation mainly at CG and CHG sites, and that the RdDM pathway mediates DNA methylation mainly at CHH sites, whole‐genome DNA methylation analyses showed that hyper‐CG and CHG DMRs in atx1/2/4/5 significantly overlapped with those in the DNA demethylation pathway mutant ros1 dml2 dml3 (rdd), and that hypo‐CHH DMRs in atx1/2/4/5 significantly overlapped with those in the RdDM mutant nrpe1, suggesting that the ATX paralogues function redundantly to regulate DNA methylation by promoting H3K4me3 levels and expression levels of both RdDM genes and active DNA demethylation genes. Given that the ATX proteins function as catalytic subunits of COMPASS histone methyltransferase complexes, we also demonstrated that the COMPASS complex components function as a whole to regulate DNA methylation. This study reveals a previously uncharacterized mechanism underlying the regulation of DNA methylation.

Dynamic DNA methylation turnover in gene bodies is associated with enhanced gene expression plasticity in plants

“…To further explore if a functional relationship exists between the presence of regulatory chromatin and Dynamic GbM, we re-analyzed publicly available DNA methylation data from histone methyltransferase mutants sdg2 [33], and quadruple atx1;2;4;5 mutants [45], which are both associated with the methylation of H3K4 and exhibit reduced H3K4me2 and H3K4me3 genome-wide. In both sdg2 and atx1;2;4;5 mutants, DNA methylation was increased at Dynamic GbM genes (Fig.…”

COMPASS core subunits MpSet1 and MpSwd3 regulate Monascus pigments synthesis in Monascus purpureus

“…These COMPASS complexes influence the development, lifespan, and life activities of D. melanogaster [6,12]. In Arabidopsis thaliana, there are three types of COMPASS complexes, composed of five AtAtx1 to AtAtx5 proteins, and are named AtAtx1/2-, AtAtx3-, and AtAtx4/5containing COMPASS complexes [13,14]. In this species, the COMPASS complexes affect growth, flowering time, and biotic stress response [12,15].…”

Celebrating the discovery of DNA demethylase

“…For example, a breakthrough report by (Liu, Chen, et al, 2022) details how a histone chaperone, nuclear autoantigenic sperm protein (NASP), recognizes histone H3. (Shang et al, 2022) reveal a mechanistic link between DNA methylation and histone methylation by Arabidopsis TRITHORAX histone methyltransferases, which are components of the COMPASS complex. In addition, ROS1 recruitment to specific loci remains an interesting question, and (Zhou et al, 2022) reveal a mechanism by which the gene silencing mark H3K9me2 regulates demethylation.…”