Integrated histone modification and transcriptome analyses reveal the regulatory mechanism for sustained agronomic performance of rice under terminal drought stress

ABSTRACT Histone methylation is a key epigenetic mechanism that modulates gene expression, particularly during developmental processes and in response to environmental stresses. In this study, we investigated genome-wide patterns of histone H3 lysine 4 trimethylation (H3K4me3) and histone H3 lysine 27 trimethylation (H3K27me3) in two contrasting rice ( Oryza sativa L.) cultivars: IR-64, which is sensitive to terminal drought stress, and Nagina-22 (N-22), a drought-tolerant genotype. Under terminal drought stress, a pronounced enrichment of H3K4me3 mark was observed in the panicles of N-22, whereas IR-64 exhibited a marked increase in H3K27me3 levels. H3K4me3 was predominantly localized to promoter regions, while H3K27me3 displayed a broader distribution across exons, introns, transcription termination sites, and intergenic regions. In N-22, H3K27me3 peaks were associated with 3,052 genes, including 799 genes uniquely expressed in this cultivar. In contrast, IR-64 showed H3K27me3 enrichment across 7,521 genes, of which 5,268 were uniquely expressed in the sensitive cultivar. Notably, N-22 exhibited a substantially higher number of H3K4me3-marked genes under drought stress, reflecting enhanced transcriptional activity in the tolerant cultivar. Of the 19,430 genes carrying H3K4me3 modifications, 18,785 were exclusive to N-22, whereas only 283 genes were uniquely marked in IR-64. In N-22, H3K27me3 enrichment was detected in nine genes associated with drought tolerance, and these epigenetic changes were consistent with their transcript abundance. A positive correlation between H3K4me3 enrichment and gene expression was observed for 646 genes in N-22, compared with only five genes in IR-64 under terminal drought stress. Differential enrichment of histone modification peak was prominent in genes involved in regulatory and stress-related functions, including transcription factors, detoxification pathways, and redox signaling. Coordinated changes in histone modifications and gene expression were observed in only a small subset of genes, which included key stress-responsive families such as AP2/ERF and MYB transcription factors, chloroplast precursor proteins, cytochrome P450s, oxidoreductases, and glutathione S-transferases. Together, these findings highlight distinct epigenetic landscapes associated with drought tolerance and sensitivity in rice and provide a valuable resource for understanding the epigenetic regulation of gene expression under terminal drought stress.