Gene expression in bovine rumen epithelium during weaning identifies molecular regulators of rumen development and growth

Abstract

During weaning, epithelial cell function in the rumen transitions in response to conversion from a pre-ruminant to a true ruminant environment to ensure efficient nutrient absorption and metabolism. To identify gene networks affected by weaning in bovine rumen, Holstein bull calves were fed commercial milk replacer only (MRO) until 42 days of age, then were provided diets of either milk + orchardgrass hay (MH) or milk + grain-based calf starter (MG). Rumen epithelial RNA was extracted from calves sacrificed at four time points: day 14 (n = 3) and day 42 (n = 3) of age while fed the MRO diet and day 56 (n = 3/diet) and day 70 (n = 3/diet) while fed the MH and MG diets for transcript profiling by microarray hybridization. Five two-group comparisons were made using Permutation Analysis of Differential Expression® to identify differentially expressed genes over time and developmental stage between days 14 and 42 within the MRO diet, between day 42 on the MRO diet and day 56 on the MG or MH diets, and between the MG and MH diets at days 56 and 70. Ingenuity Pathway Analysis (IPA) of differentially expressed genes during weaning indicated the top 5 gene networks involving molecules participating in lipid metabolism, cell morphology and death, cellular growth and proliferation, molecular transport, and the cell cycle. Putative genes functioning in the establishment of the rumen microbial population and associated rumen epithelial inflammation during weaning were identified. Activation of transcription factor PPAR-α was identified by IPA software as an important regulator of molecular changes in rumen epithelium that function in papillary development and fatty acid oxidation during the transition from pre-rumination to rumination. Thus, molecular markers of rumen development and gene networks regulating differentiation and growth of rumen epithelium were identified for selecting targets and methods for improving and assessing rumen development and function, particularly in the growing calf.

Effects of early feeding on the host rumen transcriptome and bacterial diversity in lambs

“…It has been reported that solid feed consumption can increase total VFA concentrations and the molar proportion of acetate and butyrate in the rumen of starter + milk replacer-fed lambs when compared with lambs fed only milk replacement during 1 to 84 days of life9. Indeed, administering grain-based feed and orchard grass hay to neonatal ruminants significantly increase the length and density of the rumen papillae, whereas feeding milk alone resulted in little development of these structures and poor animal growth10. Therefore, this feeding strategy provides biologically appropriate fuels, and is thought to enhance early rumen development.…”

Invited Review: Nutritional regulation of gut function in dairy calves: From colostrum to weaning

“…During the weaning process, the GIT undergoes significant changes, with the total volume of the rumen increasing from 30 to 70% of the entire forestomach (Warner et al, 1956), enhanced expression of metabolic genes (Connor et al, 2013), and altered microbial populations (Meale et al, 2017). The physical growth of rumen tissue accommodates absorption of the end products of ruminal fermentation to meet the demands for growth ( Figure 2; Baldwin et al, 2004).…”

Utilization of digital differential display to identify differentially expressed genes related to rumen development

“…HMGCS2 plays an important role in ketogenesis in the rumen epithelium of sheep during development, and is upregulated in the rumen epithelium of weaned Holstein calves compared with that in nonweaned calves (Lane et al 2002;Connor et al 2013). HMGCS2 gene expression was significantly increased in the rumen at post-weaning than at pre-weaning.…”

“…After weaning, the development of the rumen papillae increases the efficiency in VFA production and absorption. Indeed, giving grain-based feed and orchard grass hay to neonatal calves significantly increases the length and density of the rumen papillae, whereas feeding only milk resulted in little development of these structures and poor growth of the animals (Connor et al 2013). In addition, high-concentrate diets induce significant increases in density and length of the rumen papillae (Stobo et al 1966).…”

“…In addition, high-concentrate diets induce significant increases in density and length of the rumen papillae (Stobo et al 1966). Indeed, giving grain-based feed and orchard grass hay to neonatal calves significantly increases the length and density of the rumen papillae, whereas feeding only milk resulted in little development of these structures and poor growth of the animals (Connor et al 2013). TGFβ1 (transforming growth factor beta 1) and ESRRα (estrogen-related receptor alpha) can be capable of contributing to the development of rumen epithelium and energy metabolism, respectively, as transcriptional regulators and provide the targets for mediation of rumen development and function in growing Correspondence: Sang-gun Roh, Lab of Animal Physiology, Graduate School of Agricultural Science, Tohoku University, Sendai,Japan.…”