Nuclear envelope dysfunction drives premature aging and modulates heterochromatic methylome drift in Arabidopsis

Aging involves progressive functional decline accompanied by molecular and epigenomic drift. Although nuclear-envelope (NE) defects cause premature aging in animals, the contribution of nuclear architecture to aging in plants remains unclear. Here we show that NE integrity is essential for maintaining epigenetic stability in Arabidopsis thaliana . Under short-day conditions, loss of KAKU4 or CRWN proteins uncovers a photoperiod-sensitive, progeroid-like trajectory with premature senescence, transcriptional drift, and disruption of heterochromatin maintenance. Multi-omics analyses reveal that KAKU4 occupancy is confined to euchromatin and contracts with age, while CHH and CHG methylation erosion occurs within H3K9me2-enriched, transposon-dense heterochromatin. Wild-type plants normally exhibit age-associated CHH hypermethylation at transposable elements, a process abolished in NE mutants. Thus, nuclear-envelope integrity couples chromatin organization to the direction and rate of epigenomic drift, positioning perinuclear architecture as a conserved determinant of heterochromatin stability and aging trajectory across eukaryotes.