Background <p>The rumen epithelium, liver, and muscle tissues are key metabolic organs in ruminants, each performing distinct yet interconnected roles in energy metabolism and growth. However, how these tissues coordinate their gene expression to meet metabolic demands in Hu sheep remains poorly understood.</p> Results <p>RNA sequencing of 48 tissue samples (rumen epithelium, liver, and muscle tissues from 16 male Hu sheep) identified 30,171 transcripts, including 7,403 commonly expressed and 3,414 uniquely expressed genes. The rumen epithelium displayed the highest number of uniquely expressed genes but lower functional enrichment compared to the liver and muscle, emphasizing its specialized yet limited metabolic pathways. Functional enrichment analysis showed that the rumen epithelium was enriched in pathways related to epithelial renewal. Differential gene expression analysis of commonly expressed genes further distinguished these tissues, reinforcing the metabolic specialization of the rumen epithelium. Weighted Gene Co-expression Network Analysis (WGCNA) revealed distinct tissue-specific modules associated with tissues. Key hub genes from different co-expression modules included histone deacetylase 1 (<i>HDAC1</i>, MEblue module, rumen epithelium), alpha-1-microglobulin/bikunin precursor (<i>AMBP</i>, MEdarkslateblue module, liver), and SWI/SNF related, matrix associated, actin dependent regulator of chromatin subfamily d member 3 (<i>SMARCD3</i>, MEbrown module, muscle), which regulate epithelial renewal, metabolic detoxification, and growth, respectively. Modules correlated with dry matter intake (DMI) were mainly found in the rumen epithelium and liver, while average daily gain (ADG)-related modules were enriched in the liver and muscle, indicating tissue-dependent regulatory mechanisms linking metabolic networks to performance.</p> Conclusions <p>This study reveals transcriptional specialization and inter-tissue coordination in Hu sheep metabolic organs, identifies tissue-specific gene modules associated with DMI and ADG, and highlights hub genes as potential targets for precision breeding and feeding strategies to improve feed efficiency and growth in Hu sheep.</p>

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Transcriptomic profiling of rumen epithelium, liver, and muscle reveals tissue-specific gene expression patterns in Hu sheep

  • Xiaowei Jia,
  • Jiaxiao Li,
  • Yuanxin Zhang,
  • Boya Tian,
  • Shengyong Mao,
  • Junhua Liu,
  • Wenxi Qian

摘要

Background

The rumen epithelium, liver, and muscle tissues are key metabolic organs in ruminants, each performing distinct yet interconnected roles in energy metabolism and growth. However, how these tissues coordinate their gene expression to meet metabolic demands in Hu sheep remains poorly understood.

Results

RNA sequencing of 48 tissue samples (rumen epithelium, liver, and muscle tissues from 16 male Hu sheep) identified 30,171 transcripts, including 7,403 commonly expressed and 3,414 uniquely expressed genes. The rumen epithelium displayed the highest number of uniquely expressed genes but lower functional enrichment compared to the liver and muscle, emphasizing its specialized yet limited metabolic pathways. Functional enrichment analysis showed that the rumen epithelium was enriched in pathways related to epithelial renewal. Differential gene expression analysis of commonly expressed genes further distinguished these tissues, reinforcing the metabolic specialization of the rumen epithelium. Weighted Gene Co-expression Network Analysis (WGCNA) revealed distinct tissue-specific modules associated with tissues. Key hub genes from different co-expression modules included histone deacetylase 1 (HDAC1, MEblue module, rumen epithelium), alpha-1-microglobulin/bikunin precursor (AMBP, MEdarkslateblue module, liver), and SWI/SNF related, matrix associated, actin dependent regulator of chromatin subfamily d member 3 (SMARCD3, MEbrown module, muscle), which regulate epithelial renewal, metabolic detoxification, and growth, respectively. Modules correlated with dry matter intake (DMI) were mainly found in the rumen epithelium and liver, while average daily gain (ADG)-related modules were enriched in the liver and muscle, indicating tissue-dependent regulatory mechanisms linking metabolic networks to performance.

Conclusions

This study reveals transcriptional specialization and inter-tissue coordination in Hu sheep metabolic organs, identifies tissue-specific gene modules associated with DMI and ADG, and highlights hub genes as potential targets for precision breeding and feeding strategies to improve feed efficiency and growth in Hu sheep.