Altering Polycomb Repressive Complex 2 activity partially suppressesddm1mutant phenotypes in Arabidopsis

Abstract

14In plants and mammals, DNA methylation is a hallmark of transposable element (TE) 15 sequences that contributes to their epigenetic silencing. In contrast, histone H3 lysine 27 16 trimethylation (H3K27me3), which is deposited by the Polycomb Repressive Complex 2 17 (PRC2), is a hallmark of repressed genes. Nevertheless, there is a growing body of evidence for 18 a functional interplay between these pathways. In particular, many TE sequences acquire 19H3K27me3 when they lose DNA methylation and it has been proposed that PRC2 can serve as 20 a back-up silencing system for hypomethylated TEs. Here, we show in the flowering plant 21Arabidopsis thaliana that hundreds of TEs gain H3K27m3 in the mutant ddm1, which is 22 defective in the maintenance of DNA methylation specifically over TE and other repeat 23 sequences. Moreover, this gain depends solely on CURLY LEAF (CLF), which is one of two 24 otherwise partially redundant H3K27 methyltransferases active in vegetative tissues. Finally, 25 our results challenge the notion that PRC2 can be a compensatory silencing system for 26 hypomethylated TEs, as the complete loss of H3K27me3 in ddm1 clf double mutant plants was 27 not associated with further reactivation of TE expression nor with a burst of transposition. 28Instead, ddm1 clf plants exhibited a partial suppression of ddm1 molecular phenotypes with 29 with TE silencing, chromatin recompaction and hypermethylation of linker DNA compared to 30 ddm1. Thus, we have uncovered a novel role for PcG in antagonizing both chromatin 31 compaction and linker DNA methylation at pericentromeric TEs, which could be particularly 32 important during the reproductive stage, when TE become hypomethylated in the pollen and 33 the endosperm. 34

A new role for histone demethylases in the maintenance of plant genome integrity

“…Additionally, analysis of the Arabidopsis met1 mutant has shown that a large number of TEs that lose DNA methylation gain H3K27me3 ( Deleris et al, 2012 ). Similarly, TEs in Arabidopsis gain H3K27me3 in response to ddm1 -induced loss of DNA methylation ( Rougée et al, 2020 ). Collectively, our data together with these reports suggest that DNA methylation and H3K27me3 act antagonistically to mediate the transcriptional silencing of transposons.…”

The epigenetic origin of life history transitions in plants and algae

“…Changes to heterochromatin are known to occur in the angiosperm female gametophyte, where the reduction in DNA and H3K9 methylation coincides with a redistribution of H3K27me3 to a large proportion of TEs (Weinhofer et al 2010). Accumulation of H3K27me3 at TEs also occurs in mutants affecting constitutive heterochromatin in fungi, animals and even plants (Reddington et al 2013;Jamieson et al 2016;Rougée et al 2019). We have already highlighted how transposons and repeats are marked by H3K27me3 in unicellular red algae and green algae (Fig.…”

The contribution of transposable elements to transcriptional novelty in plants: theFLCaffair

“…However, a recent deep repeat annotation revealed traces of uncharacterized TEs within FLC [37]. Interestingly, numerous TEs that lose DNA methylation in mutants deficient in MET1 or the chromatin remodeler DDM1, as well as in the endosperm of wild-type seeds, gain ectopic H3K27me3 [38][39][40][41], indicating that unmethylated TEs can be targeted by PCR2. Therefore, it is reasonable to speculate that the accumulation of old, highly degenerated and unmethylated TE sequences within FLC may have contributed to the evolution of this notable intron and its epigenetic regulation.…”