Modes of genetic adaptations underlying functional innovations in the rumen

doi:10.1007/s11427-020-1828-8

. 2021 Jan;64(1):1-21.

doi: 10.1007/s11427-020-1828-8. Epub 2020 Nov 5.

Modes of genetic adaptations underlying functional innovations in the rumen

Xiangyu Pan^#¹, Yudong Cai^#¹, Zongjun Li^#¹, Xianqing Chen^#², Rasmus Heller^#³, Nini Wang^#¹, Yu Wang¹, Chen Zhao¹, Yong Wang^{4

5

6}, Han Xu¹, Songhai Li⁷, Ming Li¹, Cunyuan Li⁸, Shengwei Hu⁸, Hui Li^{1

9}, Kun Wang², Lei Chen², Bin Wei¹, Zhuqing Zheng¹, Weiwei Fu¹, Yue Yang², Tingting Zhang¹, Zhuoting Hou², Yueyang Yan¹, Xiaoyang Lv¹⁰, Wei Sun^{10

11}, Xinyu Li¹², Shisheng Huang¹³, Lixiang Liu¹⁴, Shengyong Mao¹⁴, Wenqing Liu¹⁵, Jinlian Hua¹⁵, Zhipeng Li¹⁶, Guojie Zhang^{5

17

18

19}, Yulin Chen¹, Xihong Wang¹, Qiang Qiu^{2

20}, Brian P Dalrymple²¹, Wen Wang^{22

23

24}, Yu Jiang²⁵

Affiliations

¹ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.
² School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, 710072, China.
³ Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, Copenhagen, DK-2100, Denmark.
⁴ University of Chinese Academy of Sciences, Beijing, 100049, China.
⁵ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China.
⁶ CEMS, NCMIS, MDIS, Academy of Mathematics and Systems Science, Chinese Academy of Sciences, Beijing, 100080, China.
⁷ Marine Mammal and Marine Bioacoustics Laboratory, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China.
⁸ College of Life Sciences, Shihezi University, Shihezi, 832003, China.
⁹ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, 530005, China.
¹⁰ College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China.
¹¹ Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
¹² Key Laboratory for Major Obstetric Diseases of Guangdong Province, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510150, China.
¹³ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China.
¹⁴ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China.
¹⁵ College of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest A&F University, Yangling, 712100, China.
¹⁶ Department of Special Economic Animal Nutrition and Feed Science, Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, Changchun, 130112, China.
¹⁷ Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DK-2100, Denmark.
¹⁸ China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
¹⁹ State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China.
²⁰ State Key Laboratory of Grassland Agro-Ecosystem, College of Life Sciences, Lanzhou University, Lanzhou, 730000, China.
²¹ School of Animal Biology and Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009, Australia.
²² School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, 710072, China. wwang@mail.kiz.ac.cn.
²³ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China. wwang@mail.kiz.ac.cn.
²⁴ State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China. wwang@mail.kiz.ac.cn.
²⁵ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China. yu.jiang@nwafu.edu.cn.

^# Contributed equally.

PMID: 33165812
DOI: 10.1007/s11427-020-1828-8

Modes of genetic adaptations underlying functional innovations in the rumen

Xiangyu Pan et al. Sci China Life Sci. 2021 Jan.

. 2021 Jan;64(1):1-21.

doi: 10.1007/s11427-020-1828-8. Epub 2020 Nov 5.

Authors

Affiliations

¹ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China.
² School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, 710072, China.
³ Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, Copenhagen, DK-2100, Denmark.
⁴ University of Chinese Academy of Sciences, Beijing, 100049, China.
⁵ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China.
⁶ CEMS, NCMIS, MDIS, Academy of Mathematics and Systems Science, Chinese Academy of Sciences, Beijing, 100080, China.
⁷ Marine Mammal and Marine Bioacoustics Laboratory, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China.
⁸ College of Life Sciences, Shihezi University, Shihezi, 832003, China.
⁹ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Animal Science and Technology, Guangxi University, Nanning, 530005, China.
¹⁰ College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China.
¹¹ Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
¹² Key Laboratory for Major Obstetric Diseases of Guangdong Province, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510150, China.
¹³ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China.
¹⁴ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China.
¹⁵ College of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest A&F University, Yangling, 712100, China.
¹⁶ Department of Special Economic Animal Nutrition and Feed Science, Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, Changchun, 130112, China.
¹⁷ Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DK-2100, Denmark.
¹⁸ China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
¹⁹ State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China.
²⁰ State Key Laboratory of Grassland Agro-Ecosystem, College of Life Sciences, Lanzhou University, Lanzhou, 730000, China.
²¹ School of Animal Biology and Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009, Australia.
²² School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, 710072, China. wwang@mail.kiz.ac.cn.
²³ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China. wwang@mail.kiz.ac.cn.
²⁴ State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China. wwang@mail.kiz.ac.cn.
²⁵ Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China. yu.jiang@nwafu.edu.cn.

^# Contributed equally.

PMID: 33165812
DOI: 10.1007/s11427-020-1828-8

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.

Keywords: comparative genomics; comparative transcriptomics; evo-devo; evolution of organs; rumen innovations.

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References

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1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402. - PubMed - PMC
1. Andrews S. (2016). FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Cambridge, UK.
1. Baldwin VI, R.L., McLeod, K.R., Klotz, J.L., and Heitmann, R.N. (2004). Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. J Dairy Sci 87, E55–E65.
1. Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. - PubMed - PMC

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[1] Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J.D. (1983). Molecular Biology Of The Cell (Garland Publishing).

[2] Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J.D. (1983). Molecular Biology Of The Cell (Garland Publishing).

[3] Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402. - PubMed - PMC

[4] Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402. - PubMed - PMC

[5] Andrews S. (2016). FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Cambridge, UK.

[6] Andrews S. (2016). FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics, Cambridge, UK.

[7] Baldwin VI, R.L., McLeod, K.R., Klotz, J.L., and Heitmann, R.N. (2004). Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. J Dairy Sci 87, E55–E65.

[8] Baldwin VI, R.L., McLeod, K.R., Klotz, J.L., and Heitmann, R.N. (2004). Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. J Dairy Sci 87, E55–E65.

[9] Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. - PubMed - PMC

[10] Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. - PubMed - PMC

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Modes of genetic adaptations underlying functional innovations in the rumen

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Modes of genetic adaptations underlying functional innovations in the rumen

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