A Chinese indicine pan-genome reveals a wealth of novel structural variants introgressed from other Bos species

Authors: DAI, XUELEI - Northwest A&f University; BIAN, PEIPEI - Northwest A&f University; HU, DEXIANG - Northwest A&f University; LUO, FUNONG - Northwest A&f University; HUANG, YONGZHEN - Northwest A&f University; JIAO, SHAOHUA - Northwest A&f University; WANG, XIHONG - Northwest A&f University; GONG, MIAN - Northwest A&f University; LI, RAN - Northwest A&f University; CAI, YUDONG - Northwest A&f University; WEN, JIAYUE - Northwest A&f University; YANG, QIMENG - Northwest A&f University; DENG, WEIDONG - Yunnan Agricultural University; NANAEI, HOJJAT - Northwest A&f University; WANG, YU - Northwest A&f University; WANG, FEI - Northwest A&f University; ZHANG, ZIJING - Henan Academy Of Agricultural Science; Rosen, Benjamin - Ben; HELLER, RASMUS - University Of Copenhagen; JIANG, YU - Northwest A&f University

Submitted to: Genome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/30/2023
Publication Date: 9/15/2023
Citation: Dai, X., Bian, P., Hu, D., Luo, F., Huang, Y., Jiao, S., Wang, X., Gong, M., Li, R., Cai, Y., Wen, J., Yang, Q., Deng, W., Nanaei, H.A., Wang, Y., Wang, F., Zhang, Z., Rosen, B.D., Heller, R., Jiang, Y. 2023. A Chinese indicine pan-genome reveals a wealth of novel structural variants introgressed from other Bos species. Genome Research. 33(8):1284–1298. https://doi.org/10.1101/gr.277481.122.
DOI: https://doi.org/10.1101/gr.277481.122

Interpretive Summary: Chinese indicine cattle have been found to have a greater variety of genetic traits compared to other domestic cattle. However, researchers have not yet explored the detailed structure of their genetic makeup. In this study, 20 high quality genomes of 10 Chinese indicine cattle from different regions in southern China were created. By analyzing the genomes, we discovered distinct and reliable variations in the DNA sequence that are not found in other cattle breeds. Additionally, we identified specific regions in the genomes, called hotspots, where a large number of these variations are clustered together. The study also revealed the presence of DNA in Chinese indicine cattle that originated from other related species of wild cattle. These fragments were incorporated into the genetic makeup of Chinese indicine cattle through a process called introgression, which is the transfer of genetic material between different species. These introgressed fragments are found over nearly the entire genome. We were able to trace the origin of these introgressed fragments and found that they came from various related species of wild cattle, including banteng-like, kouprey-like, gayal-like, and gaur-like Bos species. Overall, this study demonstrates that the high genetic diversity observed in Chinese indicine cattle is the result of significant genetic exchange with multiple related species. It emphasizes the role of interspecies introgression in shaping the genetic composition of these important livestock populations. Furthermore, the findings illustrate how the incorporation of genetic material from different species can contribute to the overall genetic variation available for selection in breeding programs.

Technical Abstract: Chinese indicine cattle harbor a much higher genetic diversity compared to other domestic cattle, but their genome architecture remains uninvestigated. Using PacBio HiFi sequencing data from 10 Chinese indicine cattle across southern China, we assembled 20 reference-quality haplotype-resolved genomes, and integrated them into a multiassembly graph containing 148.5 Mb (5.6%) of novel sequence. We identified 156,009 high-confidence non-redundant structural variants (SVs) and 206 SV hotspots spanning ~195 megabases of gene-rich sequence. We detected 34,249 archaic introgressed fragments in Chinese indicine cattle covering 1.93 Gb (73.3% ) of the genome. We inferred an average of 3.8%, 3.2%, 1.4%, 0.5%, of introgressed sequence originating respectively from banteng-like, kouprey-like, gayal-like, gaur-like Bos species, and 0.6% of unknown origin. We therefore show that the high genetic diversity of Chinese indicine cattle is due to substantial introgression from multiple donors. Altogether, this study highlights the contribution of interspecies introgression to the genomic architecture of an important livestock population, and demonstrates how exotic genomic elements can contribute to the genetic variation available for selection.