New insights into the evolution and local adaptation of the genus Castanea in east Asia

Abstract

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.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32271929) and the National Key Research & Development Program of China (2018YFD1000605). Thanks to the Tianmu Mountain National Nature Reserve Management Bureau for their assistance in sampling.

Author contributions

Y.X. and L.Q. designed the project; X.N., S.Z., and Y.Z. worked on sequencing and data analysis; R.Z., Y.L., K.F., and B.Y. provided materials and information. X.N., W.Y., W.G., C.L, X.S., and S.C. performed experiments and drafted related methods; X.N. and Y.X. wrote and revised the main manuscript.

Data availability statement

The data supporting the findings of this work are available within the paper and its Supplementary Information files. A reporting summary for this article is available as a supplementary information file. The sequencing data in this study have been deposited in the NGDC Sequence Read Archive under accession number PRJCA017848 (https://ngdc.cncb.ac.cn/gsub/submit/bioproject/PRJCA017848). The datasets of 19 bioclimatic variables of the 2.5 arc-minute scale (CCSM4) data for 1970-2000 and Last Glacial Maximum (LGM) were obtained from WorldClim 2 [75] (http://www.worldclim.org/). The code for bioinformatics analysis is publicly available in the GitHub repository (https://github.com/niexinghua/Saner).

Conflict of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Supplementary information

Supplementary data are available at Horticulture Research online.

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