Abstract
Ruminants obtain nutrients from microbial fermentation of plant material, primarily in their rumen, a multilayered forestomach. How the different layers of the rumen wall respond to diet and influence microbial fermentation, and how these process are regulated, is not well understood. Gene expression correlation networks were constructed from full thickness rumen wall transcriptomes of 24 sheep fed two different amounts and qualities of a forage and measured for methane production. The network contained two major negatively correlated gene sub-networks predominantly representing the epithelial and muscle layers of the rumen wall. Within the epithelium sub-network gene clusters representing lipid/oxo-acid metabolism, general metabolism and proliferating and differentiating cells were identified. The expression of cell cycle and metabolic genes was positively correlated with dry matter intake, ruminal short chain fatty acid concentrations and methane production. A weak correlation between lipid/oxo-acid metabolism genes and methane yield was observed. Feed consumption level explained the majority of gene expression variation, particularly for the cell cycle genes. Many known stratified epithelium transcription factors had significantly enriched targets in the epithelial gene clusters. The expression patterns of the transcription factors and their targets in proliferating and differentiating skin is mirrored in the rumen, suggesting conservation of regulatory systems.
Highlights
Extracellular matrix, lies between the muscle and the lamina propria layer, which together with the epithelium forms the mucosa
Gene expression in the epithelial layers was much more responsive to diet and the most responsive gene cluster is enriched for genes expressed in progenitor keratinocytes, including cell cycle genes, and contains the widely used cell proliferation marker MKI67 reported to be expressed in some, but not all, basal cells and some early suprabasal cells in human skin[24]
We interpret the increase in cell cycle gene expression as an increase in cell division in the transit amplifying cells in the basal layers due to increased turnover of the epithelium and/or increased epithelial volume relative to muscle volume in response to increased intake[25,26]
Summary
Extracellular matrix, lies between the muscle and the lamina propria layer, which together with the epithelium forms the mucosa. Previous studies have shown that rumen keratinsed epithelial growth[10,11] and ruminal metabolism[12] adapt to different diet conditions. Such adaptation may be associated with variation in rumen digestion efficiency and the mechanisms mediating host genetic control of rumen CH4 production via the rumen wall[13,14,15]. The exact molecular mechanisms by which the different layers of the rumen wall, including the epithelium, respond to diet and their possible relationships with CH4 production are unknown. Since the rumen shares a significant number of transcriptomic features with the skin[16], a well understood epithelial system[17], we analysed the rumen transcriptome in parallel with human skin datasets to further understand the regulatory mechanisms in the rumen epithelium
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