Transcriptomic analysis reveals the molecular mechanisms of rumen wall morphological and functional development induced by different solid diet introduction in a lamb model

BACKGROUND: This study aimed to elucidate the molecular mechanisms of solid diet introduction initiating the cellular growth and maturation of rumen tissues and characterize the shared and unique biological processes upon different solid diet regimes. METHODS: Twenty-four Hu lambs were randomly allocated to three groups fed following diets: goat milk powder only (M, n = 8), goat milk powder + alfalfa hay (MH, n = 8), and goat milk powder + concentrate starter (MC, n = 8). At 42 days of age, the lambs were slaughtered. Ruminal fluid sample was collected for analysis of concentration of volatile fatty acid (VFA) and microbial crude protein (MCP). The sample of the rumen wall from the ventral sac was collected for analysis of rumen papilla morphology and transcriptomics. RESULTS: Compared with the M group, MH and MC group had a higher concentration of VFA, MCP, rumen weight, and rumen papilla area. The transcriptomic results of rumen wall showed that there were 312 shared differentially expressed genes (DEGs) between in “MH vs. M” and “MC vs. M”, and 232 or 796 unique DEGs observed in “MH vs. M” or “MC vs. M”, respectively. The shared DEGs were most enriched in VFA absorption and metabolism, such as peroxisome proliferator-activated receptor (PPAR) signaling pathway, butanoate metabolism, and synthesis and degradation of ketone bodies. Additionally, a weighted gene co-expression network analysis identified M16 (2,052 genes) and M18 (579 genes) modules were positively correlated with VFA and rumen wall morphology. The M16 module was mainly related to metabolism pathway, while the M18 module was mainly associated with signaling transport. Moreover, hay specifically depressed expression of genes involved in cytokine production, immune response, and immunocyte activation, and concentrate starter mainly altered nutrient transport and metabolism, especially ion transport, amino acid, and fatty acid metabolism. CONCLUSIONS: The energy production during VFA metabolism may drive the rumen wall development directly. The hay introduction facilitated establishment of immune function, while the concentrate starter enhanced nutrient transport and metabolism, which are important biological processes required for rumen development. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-021-00556-4.