Transcriptional Reprogramming in Rumen Epithelium during the Developmental Transition of Pre-Ruminant to the Ruminant in Cattle

SIMPLE SUMMARY: The rumen is the critical organ mediating nutrient uptake and use in cattle. Health development is essential to ensure animal feed efficiency. In this report, we present an analysis of gene expression dynamic in rumen epithelium during the transition from pre-ruminant to ruminant in cattle fed with hay or concentrated diets at weaning. The global shifts in gene expression and correlated transcription factors activities indicate transcriptional reprogramming during weaning. Transcriptional reprogramming in rumen epithelial tissue reflects critical nutrient-gene interactions occurring during the developmental progression. The results unveiled that nutrient-gene interactions compel transcriptional reprogramming. Our findings also suggest that this transcriptional reprogramming is the molecular basis of the transitional development of pre-ruminant to the ruminant in cattle. ABSTRACT: We present an analysis of transcriptomic dynamics in rumen epithelium of 18 Holstein calves during the transition from pre-rumination to rumination in cattle-fed hay or concentrated diets at weaning. Three calves each were euthanized at 14 and 42 d of age to exemplify preweaning, and six calves each were provided diets of either milk replacer and grass hay or calf starter to introduce weaning. The two distinct phases of rumen development and function in cattle are tightly regulated by a series of signaling events and clusters of effectors on critical pathways. The dietary shift from liquid to solid feeds prompted the shifting of gene activity. The number of differentially expressed genes increased significantly after weaning. Bioinformatic analysis revealed gene activity shifts underline the functional transitions in the ruminal epithelium and signify the transcriptomic reprogramming. Gene ontogeny (GO) term enrichment shows extensively activated biological functions of differentially expressed genes in the ruminal epithelium after weaning were predominant metabolic functions. The transcriptomic reprogramming signifies a correlation between gene activity and changes in metabolism and energy production in the rumen epithelium, which occur at weaning when transitioning from glucose use to VFA use by epithelium during the weaning.