Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment
Xia, Xiaoting; Zhang, Fengwei; Li, Shuang; Luo, Xiaoyu; Peng, Lixin; Dong, Zheng; Pausch, Hubert; Leonard, Alexander S; Crysnanto, Danang; Wang, Shikang; Tong, Bin; Lenstra, Johannes A; Han, Jianlin; Li, Fuyong; Xu, Tieshan; Gu, Lihong; Jin, Liangliang; Dang, Ruihua; Huang, Yongzhen; Lan, Xianyong; Ren, Gang; Wang, Yu; Gao, Yuanpeng; Ma, Zhijie; Cheng, Haijian; Ma, Yun; Chen, Hong; Pang, Weijun; Lei, Chuzhao; Chen, Ningbo
(2023) Genome Biology, volume 24, issue 1
(Article)
Abstract
BACKGROUND: Structural variations (SVs) in individual genomes are major determinants of complex traits, including adaptability to environmental variables. The Mongolian and Hainan cattle breeds in East Asia are of taurine and indicine origins that have evolved to adapt to cold and hot environments, respectively. However, few studies have investigated SVs
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in East Asian cattle genomes and their roles in environmental adaptation, and little is known about adaptively introgressed SVs in East Asian cattle. RESULTS: In this study, we examine the roles of SVs in the climate adaptation of these two cattle lineages by generating highly contiguous chromosome-scale genome assemblies. Comparison of the two assemblies along with 18 Mongolian and Hainan cattle genomes obtained by long-read sequencing data provides a catalog of 123,898 nonredundant SVs. Several SVs detected from long reads are in exons of genes associated with epidermal differentiation, skin barrier, and bovine tuberculosis resistance. Functional investigations show that a 108-bp exonic insertion in SPN may affect the uptake of Mycobacterium tuberculosis by macrophages, which might contribute to the low susceptibility of Hainan cattle to bovine tuberculosis. Genotyping of 373 whole genomes from 39 breeds identifies 2610 SVs that are differentiated along a "north-south" gradient in China and overlap with 862 related genes that are enriched in pathways related to environmental adaptation. We identify 1457 Chinese indicine-stratified SVs that possibly originate from banteng and are frequent in Chinese indicine cattle. CONCLUSIONS: Our findings highlight the unique contribution of SVs in East Asian cattle to environmental adaptation and disease resistance.
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Keywords: East Asian cattle, Genome assembly, Long-read sequencing, Structural variation, Genetics, Ecology, Evolution, Behavior and Systematics, Cell Biology
ISSN: 1465-6906
Publisher: BioMed Central
Note: Funding Information: The project was supported by the earmarked fund for China Agriculture Research System-the National Beef Cattle and Yak Industrial Technology System (CARS-37), the Yunnan Academician Workstations (202305AF150156), and the National Natural Science Foundation of China (32372854) to C.L.; the National Key Research and Development Program of China (SQ2021YFF1000041), the fellowship of China Postdoctoral Science Foundation (2021T140564 and 2020M683587), the Shaanxi Youth Science and Technology New Star (2022KJXX-77), the Natural Science Basic Research Program of Shaanxi (2021JQ-137), the National Natural Science Foundation of China (32102523), the High-end Foreign Experts Recruitment Plan (G2022172032L), and the Fundamental Research Funds for the Central Universities to N.C.; the Inner Mongolia Science & Technology Plan (No. 2021ZZ0204) to B.T.; the National Natural Science Foundation of China (32072720) to Y.M.; and the National Natural Science Foundation of China (31872979) and the Key Research and Development Program of Shaanxi Province (2022ZDLNY01-04) to W.P. The Chinese government’s contribution to the CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources in Beijing (2023-YWF-ZX-02) is appreciated. Funding Information: We acknowledge the strong support from Professor Yu Jiang for this study. We thank the High-Performance Computing (HPC) of Northwest A&F University (NWAFU) and Heifei Advanced Computing Center for providing computing resources. The review history is available as Additional file 3. Tim Sands was the primary editor of this article and managed its editorial process and peer review in collaboration with the rest of the editorial team. Publisher Copyright: © 2023, BioMed Central Ltd., part of Springer Nature.
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