Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment

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

doi:10.1186/s13059-023-03052-2

Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment

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

Northwest Normal University
Guangxi Academy of Agricultural Sciences
Animal Breeding and Genomics Centre
Inner Mongolia University
International Livestock Research Institute (ILRI)
School of Veterinary Medicine, City University of Hong Kong, Hong Kong, Hong Kong SAR.
Chinese Academy of Tropical Agricultural Sciences
Hainan Academy of Agricultural Sciences
Qinghai University
Ningxia University

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Article number	211
Number of pages	22
Journal	Genome Biology
Volume	24
Issue number	1
DOIs	https://doi.org/10.1186/s13059-023-03052-2
Publication status	Published - Dec 2023

Bibliographical 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.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 13 Climate Action

Keywords

East Asian cattle
Genome assembly
Long-read sequencing
Structural variation

Access to Document

10.1186/s13059-023-03052-2Licence: CC BY

s13059-023-03052-2Final published version, 3.44 MBLicence: CC BY

Cite this

Xia, X., Zhang, F., Li, S., Luo, X., Peng, L., Dong, Z., Pausch, H., Leonard, A. S., Crysnanto, D., Wang, S., Tong, B., Lenstra, J. A., Han, J., Li, F., Xu, T., Gu, L., Jin, L., Dang, R., Huang, Y., ... Chen, N. (2023). Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment. Genome Biology, 24(1), Article 211. https://doi.org/10.1186/s13059-023-03052-2

@article{e74aa0abbab74844abbda0a0e831ec19,

title = "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 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.",

keywords = "East Asian cattle, Genome assembly, Long-read sequencing, Structural variation",

author = "Xiaoting Xia and Fengwei Zhang and Shuang Li and Xiaoyu Luo and Lixin Peng and Zheng Dong and Hubert Pausch and Leonard, \{Alexander S\} and Danang Crysnanto and Shikang Wang and Bin Tong and Lenstra, \{Johannes A\} and Jianlin Han and Fuyong Li and Tieshan Xu and Lihong Gu and Liangliang Jin and Ruihua Dang and Yongzhen Huang and Xianyong Lan and Gang Ren and Yu Wang and Yuanpeng Gao and Zhijie Ma and Haijian Cheng and Yun Ma and Hong Chen and Weijun Pang and Chuzhao Lei and Ningbo Chen",

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{\textquoteright}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: {\textcopyright} 2023, BioMed Central Ltd., part of Springer Nature.",

year = "2023",

month = dec,

doi = "10.1186/s13059-023-03052-2",

language = "English",

volume = "24",

journal = "Genome Biology",

issn = "1465-6906",

publisher = "BioMed Central",

number = "1",

}

Xia, X, Zhang, F, Li, S, Luo, X, Peng, L, Dong, Z, Pausch, H, Leonard, AS, Crysnanto, D, Wang, S, Tong, B, Lenstra, JA, Han, J, Li, F, Xu, T, Gu, L, Jin, L, Dang, R, Huang, Y, Lan, X, Ren, G, Wang, Y, Gao, Y, Ma, Z, Cheng, H, Ma, Y, Chen, H, Pang, W, Lei, C & Chen, N 2023, 'Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment', Genome Biology, vol. 24, no. 1, 211. https://doi.org/10.1186/s13059-023-03052-2

TY - JOUR

T1 - Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment

AU - Xia, Xiaoting

AU - Zhang, Fengwei

AU - Li, Shuang

AU - Luo, Xiaoyu

AU - Peng, Lixin

AU - Dong, Zheng

AU - Pausch, Hubert

AU - Leonard, Alexander S

AU - Crysnanto, Danang

AU - Wang, Shikang

AU - Tong, Bin

AU - Lenstra, Johannes A

AU - Han, Jianlin

AU - Li, Fuyong

AU - Xu, Tieshan

AU - Gu, Lihong

AU - Jin, Liangliang

AU - Dang, Ruihua

AU - Huang, Yongzhen

AU - Lan, Xianyong

AU - Ren, Gang

AU - Wang, Yu

AU - Gao, Yuanpeng

AU - Ma, Zhijie

AU - Cheng, Haijian

AU - Ma, Yun

AU - Chen, Hong

AU - Pang, Weijun

AU - Lei, Chuzhao

AU - Chen, Ningbo

N1 - 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.

PY - 2023/12

Y1 - 2023/12

N2 - 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.

AB - 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.

KW - East Asian cattle

KW - Genome assembly

KW - Long-read sequencing

KW - Structural variation

UR - https://www.scopus.com/pages/publications/85171573449

U2 - 10.1186/s13059-023-03052-2

DO - 10.1186/s13059-023-03052-2

M3 - Article

C2 - 37723525

SN - 1465-6906

VL - 24

JO - Genome Biology

JF - Genome Biology

IS - 1

M1 - 211

ER -

Structural variation and introgression from wild populations in East Asian cattle genomes confer adaptation to local environment

Abstract

Bibliographical note

UN SDGs

Keywords

Access to Document

Other files and links

Fingerprint

Cite this