Background Chromatin provides a tunable platform for gene expression control. Besides the well-studied core nucleosome, H1 linker histones are abundant chromatin components with intrinsic potential to influence chromatin function. Well studied in animals, little is known about the evolution of H1 function in other eukaryotic lineages for instance plants. Notably, in the model plant Arabidopsis , while H1 is known to influence heterochromatin and DNA methylation, its contribution to transcription, molecular, and cytological chromatin organization remains elusive. Results We provide a multi-scale functional study of Arabidopsis linker histones. We show that H1-deficient plants are viable yet show phenotypes in seed dormancy, flowering time, lateral root, and stomata formation—complemented by either or both of the major variants. H1 depletion also impairs pluripotent callus formation. Fine-scale chromatin analyses combined with transcriptome and nucleosome profiling reveal distinct roles of H1 on hetero- and euchromatin: H1 is necessary to form heterochromatic domains yet dispensable for silencing of most transposable elements; H1 depletion affects nucleosome density distribution and mobility in euchromatin, spatial arrangement of nanodomains, histone acetylation, and methylation. These drastic changes affect moderately the transcription but reveal a subset of H1-sensitive genes. Conclusions H1 variants have a profound impact on the molecular and spatial (nuclear) chromatin organization in Arabidopsis with distinct roles in euchromatin and heterochromatin and a dual causality on gene expression. Phenotypical analyses further suggest the novel possibility that H1-mediated chromatin organization may contribute to the epigenetic control of developmental and cellular transitions. Electronic supplementary material The online version of this article (10.1186/s13059-019-1767-3) contains supplementary material, which is available to authorized users.

Linker histones play a pivotal role in shaping chromatin architecture, notably through their globular H1 (GH1) domain that contacts the nucleosome and linker DNA. Yet, the interplay of H1 with chromatin factors along the epigenome landscape is poorly understood. Here, we report that Arabidopsis H1 favors chromatin compaction and H3K27me3 marking on a majority of Polycomb-targeted protein-coding genes while preventing H3K27me3 accumulation on telomeres and pericentromeric interstitial telomeric repeats (ITRs). These contrasting effects of H1 on H3K27me3 enrichment are associated with long-distance effects on the 3D organization of telomeres and ITRs. Mechanistically, H1 prevents ITRs from being invaded by Telomere Repeat Binding 1 (TRB1), a GH1-containing telomere component with an extra-telomeric function in targeting Polycomb to genes bearing telomeric motifs. We propose that reciprocal DNA binding of H1 and TRB1 to clustered telobox motifs prevents H3K27me3 accumulation on large chromosomal blocks, conferring a sequence-specific role to H1 in epigenome homeostasis.