Muscle tissue transcriptome of F1 Angus-Nellore bulls and steers feedlot finished: impacts on intramuscular fat deposition

Abstract

Background: Castration is a common practice in beef cattle production systems to manage breeding and enhance meat quality by promoting intramuscular fat (IMF) deposition, known as marbling. However, the molecular mechanisms that are influenced by castration in beef cattle are poorly understood. The aim of this study was to identify differentially expressed genes (DEGs) and metabolic pathways that regulate IMF deposition in crossbred cattle by RNA sequencing (RNA-Seq) of skeletal muscle tissue. Six hundred and forty F1 Angus-Nellore bulls and steers (n = 320/group) were submitted to feedlot finishing for 180 days. Sixty Longissimus thoracis muscle samples were collected randomly from each group in the hot carcass (at slaughter) and 48 h post-mortem (at deboning), at between 12th and 13th thoracic vertebrae. Three muscle samples of each group were randomly selected for RNA-Seq analysis, while the post-deboning meat samples were submitted to determination of IMF content. Results: Steers had a 2.7-fold greater IMF content than bulls (5.59 vs. 2.07%; P < 0.01). A total of 921 DEGs (FDR < 0.05) were identified in contrast between Bulls versus Steers; of these, 371 were up-regulated, and 550 were down-regulated. Functional transcriptome enrichment analysis revealed differences in biological processes and metabolic pathways related to adipogenesis and lipogenesis, such as insulin resistance, AMPK, cAMP, regulation of lipolysis in adipocytes, and PI3K-Akt signaling pathways. Candidate genes such as FOXO1, PPARG, PCK2, CALM1, LEP, ADIPOQ, FASN, FABP4, PLIN1, PIK3R3, ROCK2, ADCY5, and ADORA1 were regulated in steers, which explains the expressive difference in IMF content when compared to bulls. Conclusions: The current findings suggest the importance of these pathways and genes for lipid metabolism in steers with greater IMF. Notably, this study reveals for the first time the involvement of the PI3K-Akt pathway and associated genes in regulating IMF deposition in F1 Angus-Nellore cattle. Castration influenced DEGs linked to energy metabolism and lipid biosynthesis, highlighting key molecular players responsible for IMF accumulation post-castration in beef cattle. Graphical Abstract: (Figure presented.)