Population epigenomics reveals epigenetic drivers of replicated evolution and missing heritability in soybean

Heritable epimutations can lead to transmissible phenotypic variation. However, the contribution of epigenetic variations to phenotypic diversity in plant evolution and crop domestication remains elusive. In this study, we constructed a comprehensive DNA methylation atlas of 1102 soybean accessions, including wild soybeans, landraces, and improved cultivars. Integrated analysis of the methylome, variome, and transcriptome revealed that de novo epimutations contributed to increased epigenetic diversity following the domestication bottleneck and modulated gene expression during soybean evolution. An epigenome-wide association study and targeted DNA methylation editing validated an epiallele governing the expression of GmFT5a, which contributed to the replicated evolution of earlier flowering during high-latitude adaptation in both wild and cultivated soybeans. Notably, integrating genetic and epigenetic variants substantially increased the proportion of phenotypic variance explained, capturing a larger fraction of the heritability of these agronomic traits. This study emphasizes the considerable potential of epialleles for crop improvement and may pave the way for epigenetics-driven breeding.