Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress

Abstract

Heat-stressed Arabidopsis plants release heterochromatin-associated transposable element (TE) silencing, yet it is not accompanied by major reductions of epigenetic repressive modifications. In this study, we explored the functional role of histone H1 in repressing heterochromatic TEs in response to heat stress. We generated and analyzed RNA and bisulfite-sequencing data of wild-type and h1 mutant seedlings before and after heat stress. Loss of H1 caused activation of pericentromeric Gypsy elements upon heat treatment, despite these elements remaining highly methylated. By contrast, nonpericentromeric Copia elements became activated concomitantly with loss of DNA methylation. The same Copia elements became activated in heat-treated chromomethylase 2 (cmt2) mutants, indicating that H1 represses Copia elements through maintaining DNA methylation under heat. We discovered that H1 is required for TE repression in response to heat stress, but its functional role differs depending on TE location. Strikingly, H1-deficient plants treated with the DNA methyltransferase inhibitor zebularine were highly tolerant to heat stress, suggesting that both H1 and DNA methylation redundantly suppress the plant response to heat stress.

DNA methyltransferase CHROMOMETHYLASE3 prevents ONSEN transposon silencing under heat stress

“…This is consistent with a previous report indicating that CMT2 is required for TE body methylation on long TEs, including the Copia family [ 7 ]. Consistently, a recent study also found that DNA methylation was required for histone H1-mediated repression of ONSEN in heat stress response [ 29 ]. It has been demonstrated that a DNA methyltransferase inhibitor blocked the up-regulation of ONSEN in the heat-treated h1 mutant [ 29 ].…”

“…Consistently, a recent study also found that DNA methylation was required for histone H1-mediated repression of ONSEN in heat stress response [ 29 ]. It has been demonstrated that a DNA methyltransferase inhibitor blocked the up-regulation of ONSEN in the heat-treated h1 mutant [ 29 ]. Coinciding with our finding, the ONSEN/COPIA78 was upregulated in heat-treated cmt2 mutants [ 29 ].…”

“…It has been demonstrated that a DNA methyltransferase inhibitor blocked the up-regulation of ONSEN in the heat-treated h1 mutant [ 29 ]. Coinciding with our finding, the ONSEN/COPIA78 was upregulated in heat-treated cmt2 mutants [ 29 ]. Additionally, it has been reported that CHH methylation variation in the accessions of Arabidopsis thaliana grown at two different temperatures was associated with natural CMT2 variation [ 30 ].…”

Histone H1 protects telomeric repeats from H3K27me3 invasion inArabidopsis

“…Hence, as in mammals, incorporation of Arabidopsis H1 is thought to dampen transcription elongation, an effect that, in plants, also applies to the production of TE-derived short interfering RNAs (siRNAs) (Papareddy et al, 2020), thereby not only restricting RNA Polymerase II (Pol II) but also RNA Pol IV activity. Arabidopsis H1 further restricts accessibility of DNA methyltransferases and demethylases that target TE sequences to regulate their heterochromatinization and silencing (He et al, 2019; Liu et al, 2020; Lyons and Zilberman, 2017; Wollmann et al, 2017; Zemach et al, 2013). Interestingly, the H1 complement is massively degraded in the vegetative pollen cell nucleus (He et al, 2019; Hsieh et al, 2016) and during the formation of Arabidopsis spore mother cells (SMCs), a depletion that coincides with heterochromatin loosening and a reduction in most H3K27me3 signals in SMC nuclei (She et al, 2013; She and Baroux, 2015).…”

“…Hence, as in other eukaryotes, incorporation of Arabidopsis H1 is thought to dampen transcription elongation, an effect that also applies to the production of TE-derived short interfering RNAs (siRNAs) (Papareddy et al, 2020), thereby not only restricting RNA Polymerase II (Pol II) but also RNA Pol IV activity. Arabidopsis H1 further restricts accessibility of DNA methyltransferases and demethylases that target TE sequences to regulate their heterochromatinization and silencing (He et al, 2019; Liu et al, 2020; Lyons and Zilberman, 2017; Wollmann et al, 2017; Zemach et al, 2013). Interestingly, DNA methylation has been found to be prevalently anti-correlated with H3K27me3 along the epigenome of Arabidopsis somatic cells (Zhang et al, 2007), but there is currently little information on the role played by H1 in this antagonism and, more generally, in the dynamic equilibria modulating chromatin compaction and accessibility in plants.…”