Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies

Yuan Yuan; Da-Ming Sun; Tao Qin; Sheng-Yong Mao; Wei-Yun Zhu; Yu-Yang Yin; Jie Huang; Rasmus Heller; Zhi-Peng Li; Jun-Hua Liu; Qiang Qiu

doi:10.24272/j.issn.2095-8137.2022.086

Volume 43 Issue 4

Jul. 2022

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Article Navigation > Zoological Research > 2022 > 43(4): 634-647

Yuan Yuan, Da-Ming Sun, Tao Qin, Sheng-Yong Mao, Wei-Yun Zhu, Yu-Yang Yin, Jie Huang, Rasmus Heller, Zhi-Peng Li, Jun-Hua Liu, Qiang Qiu. Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies. Zoological Research, 2022, 43(4): 634-647. doi: 10.24272/j.issn.2095-8137.2022.086

Citation:

Yuan Yuan, Da-Ming Sun, Tao Qin, Sheng-Yong Mao, Wei-Yun Zhu, Yu-Yang Yin, Jie Huang, Rasmus Heller, Zhi-Peng Li, Jun-Hua Liu, Qiang Qiu. Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies. Zoological Research, 2022, 43(4): 634-647. doi: 10.24272/j.issn.2095-8137.2022.086

Citation:

Yuan Yuan, Da-Ming Sun, Tao Qin, Sheng-Yong Mao, Wei-Yun Zhu, Yu-Yang Yin, Jie Huang, Rasmus Heller, Zhi-Peng Li, Jun-Hua Liu, Qiang Qiu. Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies. Zoological Research, 2022, 43(4): 634-647. doi: 10.24272/j.issn.2095-8137.2022.086

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Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies

doi: 10.24272/j.issn.2095-8137.2022.086

Yuan Yuan^{1, #},
Da-Ming Sun^{2, 3, #},
Tao Qin^{1, #},
Sheng-Yong Mao^{2, 3},
Wei-Yun Zhu^{2, 3},
Yu-Yang Yin⁴,
Jie Huang⁴,
Rasmus Heller⁵,
Zhi-Peng Li^{6
,
,},
Jun-Hua Liu^{2, 3
,
,},
Qiang Qiu^{1
,
,}

1.
School of Ecology and Environment, Northwestern Polytechnical University, Xi’an, Shaanxi 710072, China
2.
Ruminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
3.
Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research on Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
4.
Huzhou Academy of Agricultural Sciences, Huzhou, Zhejiang 313000, China
5.
Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, Copenhagen DK-2200, Denmark
6.
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin 130118, China

#Authors contributed equally to this work

Funds: This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA26040301-02), National Natural Science Foundation of China (31970392, 32172752, 32122083), Research Funds for Interdisciplinary Subject of NWPU (19SH030408), Funds Awarded by the 1000 Talent Project of Shaanxi Province, Project for Top Young Talents Program of College of Animal Science and Technology of Nanjing Agricultural University (DKQB201904), and Talents Team Construction Fund of Jilin Agricultural University.

More Information

Corresponding author: E-mail: zhplicaas@163.com; liujunhua@njau.edu.cn; qiuqiang@lzu.edu.cn
Received Date: 2022-05-27
Accepted Date: 2022-06-27

Published Online: 2022-07-04

Publish Date: 2022-07-18

Abstract

Abstract

As an important evolutionary innovation and unique organ, the rumen has played a crucial role in ruminant adaptation to complex ecological environments. However, the cellular basis of its complex morphology and function remains largely unknown. In this study, we identified eight major cell types from seven representative prenatal and postnatal rumen samples using ~56 600 single-cell transcriptomes. We captured the dynamic changes and high heterogeneity in cellular and molecular profiles before, during, and after the appearance of keratinized stratified squamous epithelium with neatly arranged papillae and functional maturity. Basal cells, keratinocytes, differentiating keratinocytes, terminally differentiated keratinocytes, and special spinous cells provided the cellular basis for rumen epithelium formation. Notably, we obtained clear evidence of two keratinization processes involved in early papillogenesis and papillae keratinization and identified TBX3 as a potential marker gene. Importantly, enriched stratum spinosum cells played crucial roles in volatile fatty acid (VFA) metabolism and immune response. Our results provide a comprehensive transcriptional landscape of rumen development at single-cell resolution, as well as valuable insight into the interactions between dietary metabolism and the rumen.
- Rumen,
- scRNA-seq,
- Ruminal epithelium,
- Keratinization

#Authors contributed equally to this work

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References(58)

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