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

Abstract

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.

Longitudinal investigations of anatomical and morphological development of the gastrointestinal tract in goats from colostrum to postweaning

“…The improvement of body size indices was slow in the milk phase, whereas it was remarkable in the MMSD phase. In addition, the weaning transition is an essential phase for the manipulation of rumen development using nutritional strategies, which can affect ruminant growth performance and health (Sun et al, 2021). The current study results confirmed the beneficial effects of solid feed to enhance the preweaning growth and overcome the weaning stress.…”

“…Moreover, Cui et al (2020) showed the increased rumen papillae height and width, and muscle layer thickness of rumen by starter intake. The rumen epithelial thickness and rumen papillary were improved in solid feed (Sun et al, 2021).…”

“…As the goats increased in age and the liquid diet changed to solid, the rumen development increased. The solid feed is the main diet for rumen epithelium development (Sun et al, 2021). The solid meal is the source of readily fermentable carbohydrates.…”

“…It provides more carbon and nitrogen to produce microbial CP and VFA (Yang, 2002;Jiao et al, 2015b;Cui et al, 2020). In addition, the AA and fatty acid metabolism function in the rumen epithelia increases with the introduction of concentrate starters (Sun et al, 2021). The VFA provide an energy source for rumen development during early life (Baldwin, 1999;Jiao et al, 2015b;Lv et al, 2019).…”

Transcriptome Analysis of Bovine Rumen Tissue in Three Developmental Stages

“…In this progress, PPAR α promoted papillary development by activating HMGCS2 ( Connor et al, 2013 ). ACAT1 , BDH1 , HMGCL , and HMGCS2 were found involved in the pathways of synthesis and degradation of ketone bodies and butanoate metabolism, which were found as features of rumen wall development ( Sun et al, 2021 ). Microbial fermentation of dietary carbohydrates in the rumen produces large amount of short-chain fatty acids (SCFAs) ( Poulsen et al, 2012 ), such as butyrate, which are known to affect rumen development and stimulate rumen epithelial cells proliferation in vivo ( Sakata and Tamate 1978 ).…”