Abstract
The rumen is the hallmark organ of ruminants and hosts a diverse ecosystem of microorganisms that facilitates efficient digestion of plant fibers. We analyzed 897 transcriptomes from three Cetartiodactyla lineages: ruminants, camels and cetaceans, as well as data from ruminant comparative genomics and functional assays to explore the genetic basis of rumen functional innovations. We identified genes with relatively high expression in the rumen, of which many appeared to be recruited from other tissues. These genes show functional enrichment in ketone body metabolism, regulation of microbial community, and epithelium absorption, which are the most prominent biological processes involved in rumen innovations. Several modes of genetic change underlying rumen functional innovations were uncovered, including coding mutations, genes newly evolved, and changes of regulatory elements. We validated that the key ketogenesis rate-limiting gene (HMGCS2) with five ruminant-specific mutations was under positive selection and exhibits higher synthesis activity than those of other mammals. Two newly evolved genes (LYZ1 and DEFB1) are resistant to Gram-positive bacteria and thereby may regulate microbial community equilibrium. Furthermore, we confirmed that the changes of regulatory elements accounted for the majority of rumen gene recruitment. These results greatly improve our understanding of rumen evolution and organ evo-devo in general.
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Acknowledgements
This project was supported by the National Natural Science Foundation of China (31822052, 31572381), the National Thousand Youth Talents Plan to Y.J., National Natural Science Foundation of China (31660644) to S.H., National Natural Science Foundation of China (41422604) to S.L. The Villum Foundation (VKR 023447) and the Independent Research Fund Denmark (8049-00098B) are thanked for supporting R.H. We thank the members of the FANNG project for sharing their transcriptome data. We thank Yongchuan Li, Zhengzhi Wei, Zixin Yang, and Haiyu Gao from Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, for helping to collect samples from the porpoise and whale. We thank High-Performance Computing (HPC) of Northwest A&F University (NWAFU) for providing computing resources.
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Compliance and ethics Two provisional Chinese patent applications on potential application in the antimicrobial and antibiotic substitute by way of the DEFB1 gene and LYZ1 gene have been filed by Northwest A&F University (application number 202010100677.8 and 202010097562.8), where Y.J., X.P., X.C, and W.W. are listed as inventors. The author(s) declare that they have no conflict of interest.
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Pan, X., Cai, Y., Li, Z. et al. Modes of genetic adaptations underlying functional innovations in the rumen. Sci. China Life Sci. 64, 1–21 (2021). https://doi.org/10.1007/s11427-020-1828-8
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DOI: https://doi.org/10.1007/s11427-020-1828-8