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. 2024 Dec 4;25(1):1178.
doi: 10.1186/s12864-024-11066-8.

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

Irene Alexandre Reis  1 , Welder Angelo Baldassini  1   2 , Germán Darío Ramírez-Zamudio  3 , Iasmin Myrele Santos Calaça de Farias  1 , Marcos Roberto Chiaratti  4 , Sérgio Pereira Junior  4 , Ricardo Perecin Nociti  3 , Pedro Henrique Vilela Carvalho  5 , Rogério Abdallah Curi  1   2 , Guilherme Luis Pereira  1   2 , Luis Artur Loyola Chardulo  1   2 , Otávio Rodrigues Machado Neto  6   7
Affiliations

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

Irene Alexandre Reis et al. BMC Genomics. .

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.

Keywords: Longissimus thoracis; Marbling; RNA sequencing; Sex class.

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Conflict of interest statement

Declarations. Ethics approval and consent to participate: The procedures followed the ethical guidelines of the Júlio de Mesquita Filho Paulista State University (UNESP), and the protocol was approved by the Animal Use Ethics Committee of the institution (CEUA 07594/2019). Consent for publication: Not applicable. Competing interests: The authors declare no competing interests. Moreover, informed consent has been obtained from the authority of feedlot facilities of Fazenda Turbilhão, Estrela D’Oeste, São Paulo, Brazil to carry out the study.

Figures

Fig. 1
Fig. 1
(A) Intramuscular fat content (B) Ribeye area in Longissimus thoracis muscle of feedlot-finished F1 Angus-Nellore bulls (n = 60) and steers (n = 60). * Significant difference (P < 0.05)
Fig. 2
Fig. 2
Principal component (PC) analysis of transcripts detected in the groups of animals (bulls versus steers)
Fig. 3
Fig. 3
MD plot showing the log2 fold change versus log2 mean of differentially expressed RNAs. Green dots indicate genes that are up-regulated, and grey dots indicate genes that are down-regulated in bovine muscle (Bulls versus Steers)
Fig. 4
Fig. 4
Top 50 genes identified as differentially expressed between F1 Angus-Nellore bulls and steers
Fig. 5
Fig. 5
Gene ontology (GO) enrichment analysis of genes that are differentially expressed in F1 Angus-Nellore bulls versus steers. (A) GO terms for all genes differentially expressed (B) GO terms for up-regulated genes differentially expressed (C) GO terms down-regulated genes differentially expressed
Fig. 6
Fig. 6
Analysis of related KEGG pathways in F1 Angus-Nellore bulls and steers
Fig. 7
Fig. 7
Regulatory mechanisms of signaling pathways and genes associated with fat metabolism and deposition in F1 Angus-Nellore bulls and steers
Fig. 8
Fig. 8
Correlation analysis. (A) Heatmap of the correlation between DEG and hub genes with phenotype (Ribeye area – REA and Intramuscular fat - IMF) in Bulls and Steers, previously reported in Santiago et al. [3, 25]. (B) Heatmap of the correlation between hub genes with DEG. The plotted points represent significant correlations between variables
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