Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya

doi:10.1016/j.pld.2025.04.002

Plant Diversity ›› 2025, Vol. 47 ›› Issue (03): 365-381.DOI: 10.1016/j.pld.2025.04.002

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Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya

Fangdong Geng (耿方东)^a, Miaoqing Liu (刘苗青)^a, Luzhen Wang (王璐珍)^a, Xuedong Zhang (张雪栋)^a, Jiayu Ma (马佳雨)^a, Hang Ye (叶航)^a, Keith Woeste^b, Peng Zhao (赵鹏)^a

a. Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi'an, Shaanxi 710069, China;
b. USDA Forest Service, Sustainable Forest Management Research, 201 14th Street SW, Washington, DC 20250, USA

Received:2024-12-09 Revised:2025-04-03 Online:2025-05-21 Published:2025-05-25
Contact: Peng Zhao (赵鹏),E-mail:pengzhao@nwu.edu.cn
Supported by:
This work was supported by the National Natural Science Foundation of China (32370386, 32070372, and 32200295), Science Foundation for Distinguished Young Scholars of Shaanxi Province (2023-JC-JQ-22), Basic Research Project of Shaanxi Academy of Fundamental Science (22JHZ005), Shaanxi Key Research and Development Program (2024NC-YBXM-064), Science and Technology Program of Shaanxi Academy of Science (2023K-49, 2023K-26, and 2019K-06), Shaanxi Forestry Science and Technology Innovation Key Project (SXLK2023-02-20), Qinling Hundred Talents Project of Shaanxi Academy of Science (Y23Z619F17).

Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya

Fangdong Geng (耿方东)^a, Miaoqing Liu (刘苗青)^a, Luzhen Wang (王璐珍)^a, Xuedong Zhang (张雪栋)^a, Jiayu Ma (马佳雨)^a, Hang Ye (叶航)^a, Keith Woeste^b, Peng Zhao (赵鹏)^a

a. Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi'an, Shaanxi 710069, China;
b. USDA Forest Service, Sustainable Forest Management Research, 201 14th Street SW, Washington, DC 20250, USA

通讯作者: Peng Zhao (赵鹏),E-mail:pengzhao@nwu.edu.cn
基金资助:
This work was supported by the National Natural Science Foundation of China (32370386, 32070372, and 32200295), Science Foundation for Distinguished Young Scholars of Shaanxi Province (2023-JC-JQ-22), Basic Research Project of Shaanxi Academy of Fundamental Science (22JHZ005), Shaanxi Key Research and Development Program (2024NC-YBXM-064), Science and Technology Program of Shaanxi Academy of Science (2023K-49, 2023K-26, and 2019K-06), Shaanxi Forestry Science and Technology Innovation Key Project (SXLK2023-02-20), Qinling Hundred Talents Project of Shaanxi Academy of Science (Y23Z619F17).

Abstract

Abstract: Intraspecific genetic variance and gene flow can support the adaptive evolution of species challenged by climate shifts or novel environmental conditions. Less well understood is how genome organization and gene flow interact in closely related species during evolutionary divergence and differentiation. Here we conducted genomic footprint analyses to determine how three species of Pterocarya (P. stenoptera, P. hupehensis, and P. macroptera), which are sympatric but occupy different elevational niches, adapted to the heterogeneous environment of the Qinling-Daba Mountains, China. We identified candidate genes for environmental adaptation (i.e., PIEZO1, WRKY39, VDAC3, CBL1, and RAF), and also identified regions of gene introgression between P. hupehensis and P. macroptera that show lower genetic load and higher genetic diversity than the rest of their genomes. The same introgressed regions are notably situated in areas of minimal genetic divergence yet they are characterized by elevated recombination rates. We also identified candidate genes within these introgressed regions related to environmental adaptation (TPLC2, CYCH;1, LUH, bHLH112, GLX1, TLP-3, and ABC1). Our findings have thus clarified the important role of gene flow in ecological adaptation and revealed genomic signatures of past introgression. Together, these findings provide a stronger theoretical basis for understanding the ecological adaptation and conservation of Quaternary relict woody plants in East Asia.

Key words: East Asian woody relict, Environmental adaptation, Gene introgression, Speciation, Genetic load, Genome evolution

摘要： Intraspecific genetic variance and gene flow can support the adaptive evolution of species challenged by climate shifts or novel environmental conditions. Less well understood is how genome organization and gene flow interact in closely related species during evolutionary divergence and differentiation. Here we conducted genomic footprint analyses to determine how three species of Pterocarya (P. stenoptera, P. hupehensis, and P. macroptera), which are sympatric but occupy different elevational niches, adapted to the heterogeneous environment of the Qinling-Daba Mountains, China. We identified candidate genes for environmental adaptation (i.e., PIEZO1, WRKY39, VDAC3, CBL1, and RAF), and also identified regions of gene introgression between P. hupehensis and P. macroptera that show lower genetic load and higher genetic diversity than the rest of their genomes. The same introgressed regions are notably situated in areas of minimal genetic divergence yet they are characterized by elevated recombination rates. We also identified candidate genes within these introgressed regions related to environmental adaptation (TPLC2, CYCH;1, LUH, bHLH112, GLX1, TLP-3, and ABC1). Our findings have thus clarified the important role of gene flow in ecological adaptation and revealed genomic signatures of past introgression. Together, these findings provide a stronger theoretical basis for understanding the ecological adaptation and conservation of Quaternary relict woody plants in East Asia.

关键词: East Asian woody relict, Environmental adaptation, Gene introgression, Speciation, Genetic load, Genome evolution

Fangdong Geng (耿方东), Miaoqing Liu (刘苗青), Luzhen Wang (王璐珍), Xuedong Zhang (张雪栋), Jiayu Ma (马佳雨), Hang Ye (叶航), Keith Woeste, Peng Zhao (赵鹏). Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya[J]. Plant Diversity, 2025, 47(03): 365-381.

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Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya

Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya

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