Chestnut plants (Castanea) are important nut fruit trees worldwide. However, little is known regarding the genetic relationship and evolutionary history of different species within the genus. How modern chestnut plants have developed local adaptation to various climates remains a mystery. The genomic data showed that Castanea henryi first diverged in the Oligocene ~31.56 million years ago, followed by Castanea mollissima, and the divergence between Castanea seguinii and Castanea crenata occurred in the mid-Miocene. Over the last 5 million years, the population of chestnut plants has continued to decline. A combination of selective sweep and environmental association studies was applied to investigate the genomic basis of chestnut adaptation to different climates. Twenty-two candidate genes were associated with temperature and precipitation. We also revealed the molecular mechanism by which CmTOE1 interacts with CmZFP8 and CmGIS3 to promote the formation of non-glandular trichomes for adaptation to low temperature and high altitudes. We found a significant expansion of CER1 genes in Chinese chestnut (C. mollissima) and verified the CmERF48 regulation of CmCER1.6 adaptation to drought environments. These results shed light on the East Asian chestnut plants as a monophyletic group that had completed interspecific differentiation in the Miocene, and provided candidate genes for future studies on adaptation to climate change in nut trees.

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