Subspecies-specific epigenetic remodeling drives differential cold adaptation in geng/xian rice

Cold stress is a major constraint on rice productivity, with the geng/japonica and xian/indica subspecies exhibiting markedly different cold tolerance. To uncover the epigenetic basis of this divergence, we conducted an integrated multi‑omics analysis of cold‑sensitive xian variety 9311 and cold‑tolerant geng variety Nipponbare. We identified fundamentally distinct epigenetic response strategies, Nipponbare actively remodels its epigenome through dynamic redistribution of H3K27me3 (21,043 differential peaks) and DNA methylation (12,031 differentially methylated regions) under cold stress, whereas 9311 undergoes passive epigenetic erosion that restricts its adaptive plasticity. This active remodeling in Nipponbare involves coordinated regulation of epigenetic writers and erasers, enabling precise control of chromatin states. Mechanistically, enhanced cold tolerance is achieved through dual epigenetic repression, H3K27me3 deposition and DNA hypermethylation, of negative regulators (e.g., OsGSK1 and 86 other cold‑stress‑related genes). Concurrently, positive regulators within the stress‑response network are activated via removal of these repressive marks or modulation of cis‑regulatory elements. The functional necessity of these epigenetic mechanisms was confirmed by pharmacological inhibition, which severely compromised the cold‑stress survival of Nipponbare. Evolutionary analysis suggests that geng rice has exploited epigenetic regulation to fine‑tune stress responses, while xian rice is subject to stronger epigenetic constraints. Collectively, our study establishes a genome-wide antagonistic interplay between H3K27me3 and DNA methylation and illustrates how their coordinated actions contribute to transcriptional diversity and adaptive evolution in rice.