Replication-independent eviction of the histone variant H2B.8 reveals chromatin reprogramming during seed imbibition

Abstract

Abstract The transition from seed to seedling involves major changes in nuclear organization and gene expression, yet the extent to which this developmental transition requires chromatin reprogramming remains largely unexplored. Here, we report that Arabidopsis dry seed embryos accumulate the histone variant H2B.8, which contributes to higher-order chromatin organization by forming spatial clusters that structure the 3D nuclear space. H2B.8 predominantly assembles into heterotypic nucleosomes, is enriched at euchromatic transposons and lowly expressed genes and, during imbibition, modulates the transcriptional activation of a subset of these genes. Water uptake triggers a decrease in H2B.8 transcripts and the eviction of the H2B.8 variant from chromatin, in a process that operates independently of DNA replication but requires de novo transcription. Histone eviction is not restricted to H2B.8, as imbibition also induces turnover of the H3.3 histone variant and therefore initiates a replication-independent chromatin reprogramming process. These findings highlight a fundamental mechanism of epigenetic regulation during early plant development.