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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, which however 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. Loss of H1 caused activation of pericentromeric GYPSY elements upon heat treatment, despite that these elements remained highly methylated. In contrast, non-pericentromeric COPIA elements became activated concomitantly with loss of DNA methylation. The same COPIA elements became activated in heat-treated chromomethylase2 (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.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE152402 | GEO | 2020/10/23

REPOSITORIES: GEO

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Project description:Silencing pathways prevent transposable element (TE) proliferation and help to maintain genome integrity through cell division. Silenced genomic regions can be classified as either euchromatic or heterochromatic, and are targeted by genetically separable epigenetic pathways. In plants, the RNA-directed DNA methylation (RdDM) pathway targets mostly euchromatic regions, while CMT methyltransferases are mainly associated with heterochromatin. However, many epigenetic features - including DNA methylation patterning - are largely indistinguishable between these regions, so how the functional separation is maintained is unclear. The linker histone H1 is preferentially localised to heterochromatin and has been proposed to restrict RdDM from encroachment. To test this hypothesis, we followed RdDM genomic localisation in an H1 mutant by performing ChIP-seq on the largest subunit, NRPE1, of the central RdDM polymerase (Pol V). Loss of H1 resulted in heterochromatic TE enrichment of NPRE1. Increased NRPE1 binding was associated with increased chromatin accessibility in h1, suggesting that H1 restricts NRPE1 occupancy by compacting chromatin. However, RdDM occupancy did not impact H1 localization, demonstrating that H1 hierarchically restricts RdDM positioning. H1 mutants experience major symmetric (CG and CHG) DNA methylation gains, and by generating an h1/nrpe1 double mutant, we demonstrate these gains are largely independent of RdDM. However, loss of NRPE1 occupancy from a subset of euchromatic regions in h1 experienced corresponding loss of methylation in all sequence contexts, while at ectopically bound heterochromatic loci, NRPE1 deposited methylation specifically in the CHH context. Additionally, we found that H1 restricts the occupancy of the methylation reader and activator complex component, SUVH1, indicating that H1’s regulatory control of methylation pathways is not limited to RdDM. Together, the results support a model whereby H1 helps maintain the exclusivity of heterochromatin by preventing encroachment from other competing pathways.

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

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