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

Zool Res. 2022 Jul 18;43(4):634-647. doi: 10.24272/j.issn.2095-8137.2022.086.

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.

瘤胃是反刍动物最重要的进化创新和独特器官,它在反刍动物适应复杂的生态环境中发挥着重要作用。然而,瘤胃复杂的形态结构和创新功能的细胞基础仍不清楚。为此,该研究采集了妊娠期、胚胎期和出生后等7个阶段的瘤胃组织,基于5 6000个单细胞转录组数据,共鉴定出8种主要细胞类型,揭示了瘤胃上皮乳头和角质化发生发育细胞和分子特征及其动态变化规律和异质性。基底细胞、角质细胞、分化角质细胞、终末分化角质细胞和特殊棘状层细胞是瘤胃上皮的细胞基础。更为重要的是,该研究发现了两个重要的角质化过程,分别是发生在早期瘤胃乳头发生和乳头角质化阶段, TBX3是乳头发生的潜在标记基因。棘层细胞在挥发性脂肪酸(VFA)代谢和免疫反应中发挥了关键作用。总而言之,该研究在单细胞分辨率水平揭示了瘤胃上皮发生发育的转录图谱,对于研究日粮代谢和瘤胃的互作机制的提供了重要依据。.

Keywords: Keratinization; Rumen; Ruminal epithelium; scRNA-seq.

MeSH terms

  • Animals
  • Diet / veterinary
  • Epithelium / metabolism
  • Fatty Acids, Volatile / metabolism
  • Rumen* / metabolism
  • Sheep / genetics
  • Transcriptome*

Substances

  • Fatty Acids, Volatile

Associated data

  • BioProject/PRJNA857336

Grants and funding

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.