Continuous climatic change threatens rice production globally and could be mitigated by enhancing crop adaptability to diverse environments. Epigenetic factors such as DNA methylation are known to facilitate adaptation in one-year transplant experiments. However, such short-term adaptation is likely confounded with acclimation response. To delineate the epigenetic influences in rice adaptation versus acclimation, we designed an 8-year transplantation experiment where Japanese rice cultivar Koshihikari was grown in Thai soil. While the plants are weak in the initial years, approximately we observed a stable 200% yield increment after year 5, potentially attributed to long-term adaptation. Between years 0-7 and 7-8, about 17K and 7K epialleles display clear changes of methylation, respectively, yet only 4K are shared. This suggests that methylation is tightly regulated to target different loci during early and late stages of adaptation. Using year 8 methylation data to track early-stage epialleles, we found that 60% reverted to near-initial-planting level (i.e., reversed), likely reflecting stress resolution, while 40% continued to deviate from year 0 (i.e., reinforced), likely due to ongoing adaptation. About 23% of these epialleles are accompanied by expression changes. The reinforced epialleles we identified from early stages are found to be enriched in yield and vigour traits (adaptation), while those reversed alleles are enriched in stress response traits (acclimation). Altogether, our analysis captures epigenetic regulation of phenotypically-observable adaptation, and distinguishes it from transient response to stress. Our results address the critical issue of differentiating between acclimation and true adaptation, leading to more adapted traits and healthier rice.

rice, epigenome