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

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

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.

OriginalsprogEngelsk
TidsskriftZoological research
Vol/bind43
Udgave nummer4
Sider (fra-til)634-647
Antal sider14
ISSN2095-8137
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
Received: 27 May 2022; Accepted: 27 June 2022; Online: 04 July 2022 Foundation items: 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. #Authors contributed equally to this work *Corresponding authors, E-mail: zhplicaas@163.com; liujunhua@ njau.edu.cn; qiuqiang@lzu.edu.cn

Funding Information:
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.

Publisher Copyright:
Copyright ©2022 Editorial Office of Zoological Research, Kunming Institute of Zoology, Chinese Academy of Sciences.

ID: 318803739