Grain-maturing temperature induces seed epi-memory via DNA methylation for subsequent development in rice ( Oryza sativa L.)

High temperature during grain filling diminishes the yield and quality of rice (Oryza sativa L.), but whether and how it affects development and agronomic traits in the subsequent plants remain unclear. In this study, we dissected the DNA methylome of seeds that developed under heat stress (heat-treated during development seeds, HDS) or control seeds (CS), and the transcriptomes of the plants derived from these seeds. Our methylome analysis identified 457 differentially methylated regions in HDS, mostly at the promoter regions of protein-coding genes and transposons. Transcriptome analysis detected 2,824 differentially expressed genes (DEGs) between plants grown from HDS or CS. HDS-derived subsequent plants were shorter, produced more tillers, had greater stomatal density, flowered earlier, and exhibited earlier diurnal floret opening than CS-derived plants. We linked DEGs to these phenotypic changes: OsSLB1 and OsYODA1 were downregulated, promoting abundant tillering and high stomatal density, respectively; OsHd1 and OsAOC1 were upregulated, leading to early flowering and early diurnal floret opening, respectively. In HDS, the OsSLB1 and OsYODA1 promoters were hypermethylated, but the OsHd1 and OsAOC1 promoters were hypomethylated, relative to CS. Notably, these seed methylation differences remained in their derived subsequent plants. Finally, yield was 9.5% higher for HDS-derived plants than for CS-derived plants when cultivated in the field. Our findings suggest the importance of seed epigenetic memory, mediated by DNA methylation, for the development of preferred agronomic traits.