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DNA methylation-linked chromatin accessibility affects genomic architecture in Arabidopsis

ABSTRACT: DNA methylation is one of the most widely distributed epigenetic marks that has a profound impact on developmental regulation, yet its influence on chromatin accessibility and 3D genome architecture is not well explored in plants. Here, we present genome-wide chromatin accessibility profiles of 18 Arabidopsis mutants that are deficient in CG, CHG or CHH DNA methylation. We find that chromatin inaccessibility at heterochromatin regions are maintained by DNA methylation in all three contexts. Many regions maintain their chromatin inaccessibility when DNA methylation is lost in only one or two contexts but we found the most increase in accessibility at sites that shown DNA methylation reduction in all contexts, suggesting an interplay between CG and non-CG methylation and chromatin accessibility. In addition, we observed that an increase in chromatin accessibility is accompanied with chromatin decompaction of many transposable elements, which leads to heterochromatin decompaction and an enhancement of long-range chromosomal interactions in the 3D genome architecture. Together, these results provide a valuable resource for chromatin compaction analyses and uncover a pivotal role for DNA methylation in the maintenance of heterochromatin inaccessibility in Arabidopsis.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE155503 | GEO | 2021/01/25

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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DNA methylation-linked chromatin accessibility affects genomic architecture in Arabidopsis

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