Transcriptome profiling of the rumen epithelium of beef cattle differing in residual feed intake

Abstract

Background: Feed efficient cattle consume less feed and produce less environmental waste than inefficient cattle. Many factors are known to contribute to differences in feed efficiency, however the underlying molecular mechanisms are largely unknown. Our study aimed to understand how host gene expression in the rumen epithelium contributes to differences in residual feed intake (RFI), a measure of feed efficiency, using a transcriptome profiling based approach.

Results: The rumen epithelial transcriptome from highly efficient (low (L-) RFI, n = 9) and inefficient (high (H-) RFI, n = 9) Hereford x Angus steers was obtained using RNA-sequencing. There were 122 genes differentially expressed between the rumen epithelial tissues of L- and H- RFI steers (p < 0.05) with 85 up-regulated and 37 down-regulated in L-RFI steers. Functional analysis of up-regulated genes revealed their involvement in acetylation, remodeling of adherens junctions, cytoskeletal dynamics, cell migration, and cell turnover. Additionally, a weighted gene co-expression network analysis (WGCNA) identified a significant gene module containing 764 genes that was negatively correlated with RFI (r = -0.5, p = 0.03). Functional analysis revealed significant enrichment of genes involved in modulation of intercellular adhesion through adherens junctions, protein and cell turnover, and cytoskeletal organization that suggest possible increased tissue morphogenesis in the L-RFI steers. Additionally, the L-RFI epithelium had increased expression of genes involved with the mitochondrion, acetylation, and energy generating pathways such as glycolysis, tricarboxylic acid cycle, and oxidative phosphorylation. Further qPCR analysis of steers with different RFI (L-RFI, n = 35; M-RFI, n = 34; H-RFI, n = 35) revealed that the relative mitochondrial genome copy number per cell of the epithelium was positively correlated with RFI (r = 0.21, p = 0.03).

Conclusions: Our results suggest that the rumen epithelium of L-RFI (efficient) steers may have increased tissue morphogenesis that possibly increases paracellular permeability for the absorption of nutrients and increased energy production to support the energetic demands of increased tissue morphogenesis compared to those of H-RFI (inefficient) animals. Greater expression of mitochondrial genes and lower relative mitochondrial genome copy numbers suggest a greater rate of transcription in the rumen epithelial mitochondria of L-RFI steers. Understanding how host gene expression profiles are associated with RFI could potentially lead to identification of mechanisms behind this trait, which are vital to develop strategies for the improvement of cattle feed efficiency.

Keywords: Beef cattle; Feed efficiency; RNA-sequencing; Residual feed intake; Rumen epithelium; Transcriptome.

Fig. 1

Biological functions of the core rumen epithelial genes as identified by PANTHER. The percentage of 9700 core rumen epithelial genes involved in various (a) Molecular functions and (b) Biological processes

Fig. 2

PCA plot of the rumen epithelial transcriptomes from cattle with L- and H- RFI. The L-RFI (Blue, n = 9) and H-RFI (Red, n = 9) samples are plotted along the first two principal components axis (PC1 and PC2)

Fig. 3

Hierarchical clustering dendrogram of rumen epithelial transcriptomes (9 L-RFI, 9 H-RFI) and trait heat map. The gradient from white to dark red in the trait heat map represents low to high levels of the trait while grey represents unavailable data. Traits examined were residual feed intake (RFI), dry matter intake (DMI), metabolizable energy intake (MEI), birth weight (BirthWT), weaning weight (WeanWT), metabolic mid-weight (MWT), end weight (EndWT), carcass weight (CWT), and average daily gain (ADG)

Fig. 4

WGCNA identification of rumen epithelial gene modules correlated with the RFI trait. Module names and sizes are shown along with the module-trait relationships indicating the correlation coefficients and p-values. The strength of the correlation is colored by different intensities of red (positive correlation) and blue (negative correlation). Asterisks indicate modules that are significantly (p < 0.05) correlated with RFI

Fig. 5

KEGG pathway for adherens junction. Genes within the turquoise module that have increased expression in the L-RFI rumen epithelium are shown in orange

Fig. 6

Correlation scatterplot of RFI and relative mtDNA copy number per cell of rumen epithelium (mtDNA/nDNA). Correlation coefficient (r) = 0.21, p-value = 0.03