Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment
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 enviro...
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| Language: | English |
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BMC
2023-09-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-023-03052-2 |
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| author | Xiaoting Xia Fengwei Zhang Shuang Li Xiaoyu Luo Lixin Peng Zheng Dong Hubert Pausch Alexander S. Leonard Danang Crysnanto Shikang Wang Bin Tong Johannes A. Lenstra Jianlin Han Fuyong Li Tieshan Xu Lihong Gu Liangliang Jin Ruihua Dang Yongzhen Huang Xianyong Lan Gang Ren Yu Wang Yuanpeng Gao Zhijie Ma Haijian Cheng Yun Ma Hong Chen Weijun Pang Chuzhao Lei Ningbo Chen |
| author_facet | Xiaoting Xia Fengwei Zhang Shuang Li Xiaoyu Luo Lixin Peng Zheng Dong Hubert Pausch Alexander S. Leonard Danang Crysnanto Shikang Wang Bin Tong Johannes A. Lenstra Jianlin Han Fuyong Li Tieshan Xu Lihong Gu Liangliang Jin Ruihua Dang Yongzhen Huang Xianyong Lan Gang Ren Yu Wang Yuanpeng Gao Zhijie Ma Haijian Cheng Yun Ma Hong Chen Weijun Pang Chuzhao Lei Ningbo Chen |
| author_sort | Xiaoting Xia |
| collection | DOAJ |
| description | 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 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. |
| first_indexed | 2024-03-09T15:08:47Z |
| format | Article |
| id | doaj.art-58caa3921a344e52a6c318514f981a68 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-03-09T15:08:47Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-58caa3921a344e52a6c318514f981a682023-11-26T13:29:11ZengBMCGenome Biology1474-760X2023-09-0124112210.1186/s13059-023-03052-2Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environmentXiaoting Xia0Fengwei Zhang1Shuang Li2Xiaoyu Luo3Lixin Peng4Zheng Dong5Hubert Pausch6Alexander S. Leonard7Danang Crysnanto8Shikang Wang9Bin Tong10Johannes A. Lenstra11Jianlin Han12Fuyong Li13Tieshan Xu14Lihong Gu15Liangliang Jin16Ruihua Dang17Yongzhen Huang18Xianyong Lan19Gang Ren20Yu Wang21Yuanpeng Gao22Zhijie Ma23Haijian Cheng24Yun Ma25Hong Chen26Weijun Pang27Chuzhao Lei28Ningbo Chen29Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityNational Engineering Research Center for Non-Food Biorefinery, Guangxi Academy of SciencesKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAnimal Genomics, ETH Zurich, Universitaetstrasse 2Animal Genomics, ETH Zurich, Universitaetstrasse 2Animal Genomics, ETH Zurich, Universitaetstrasse 2Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityThe State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, School of Life Sciences, Inner Mongolia UniversityFaculty of Veterinary Medicine, Utrecht UniversityLivestock Genetics Program, International Livestock Research Institute (ILRI)Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong KongTropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural SciencesInstitute of Animal Science & Veterinary Medicine, Hainan Academy of Agricultural SciencesKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityCollege of Veterinary Medicine, Northwest A&F UniversityQinghai Academy of Animal Science and Veterinary Medicine, Qinghai UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Ruminant Molecular and Cellular Breeding of Ningxia Hui Autonomous Region, School of Agriculture, Ningxia UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F UniversityAbstract 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 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.https://doi.org/10.1186/s13059-023-03052-2Structural variationGenome assemblyLong-read sequencingEast Asian cattle |
| spellingShingle | Xiaoting Xia Fengwei Zhang Shuang Li Xiaoyu Luo Lixin Peng Zheng Dong Hubert Pausch Alexander S. Leonard Danang Crysnanto Shikang Wang Bin Tong Johannes A. Lenstra Jianlin Han Fuyong Li Tieshan Xu Lihong Gu Liangliang Jin Ruihua Dang Yongzhen Huang Xianyong Lan Gang Ren Yu Wang Yuanpeng Gao Zhijie Ma Haijian Cheng Yun Ma Hong Chen Weijun Pang Chuzhao Lei Ningbo Chen Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment Genome Biology Structural variation Genome assembly Long-read sequencing East Asian cattle |
| title | Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment |
| title_full | Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment |
| title_fullStr | Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment |
| title_full_unstemmed | Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment |
| title_short | Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment |
| title_sort | structural variation and introgression from wild populations in east asian cattle genomes confer adaptation to local environment |
| topic | Structural variation Genome assembly Long-read sequencing East Asian cattle |
| url | https://doi.org/10.1186/s13059-023-03052-2 |
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