Integrated Comparative Transcriptome and circRNA-lncRNA-miRNA-mRNA ceRNA Regulatory Network Analyses Identify Molecular Mechanisms Associated with Intramuscular Fat Content in Beef Cattle
by
, , and
Vahid Dehghanian Reyhan
1,†,
Farzad Ghafouri
1,†
,
Mostafa Sadeghi
1,*,
Seyed Reza Miraei-Ashtiani
1, 
John P. Kastelic
2,
Herman W. Barkema
2 and
Masoud Shirali
3,4,*
1
Department of Animal Science, University College of Agriculture and Natural Resources, University of Tehran, Karaj 77871-31587, Iran
2
Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada
3
Agri-Food and Biosciences Institute, Hillsborough BT26 6DR, UK
4
School of Biological Sciences, Queen’s University Belfast, Belfast BT9 5AJ, UK
*
Authors to whom correspondence should be addressed.
†
These authors have contributed equally to this work.
Animals 2023, 13(16), 2598; https://doi.org/10.3390/ani13162598
Submission received: 16 June 2023
/
Revised: 5 August 2023
/
Accepted: 8 August 2023
/
Published: 11 August 2023
(This article belongs to the Collection Advances in Cattle Breeding, Genetics and Genomics)
Simple Summary
Meat quality and human-health-related indexes are important traits in beef cattle breeding. Intramuscular fat content (IMF) is a major meat quality trait that influences aroma, tenderness, and juiciness. Our objective was to integrate comparative transcriptomic and competing endogenous RNA (ceRNA) network analyses to identify candidate messenger RNAs (mRNAs) and regulatory RNAs involved in molecular regulation of longissimus dorsi muscle (LDM) tissue for IMF and fat metabolism of five beef cattle breeds (Angus, Chinese Simmental, Luxi, Nanyang, and Shandong Black). This study identified the primary metabolic-signaling pathways associated with IMF and fat metabolism, including calcium, cGMP-PKG, thyroid hormone, oxytocin signaling, and other metabolic pathways. In addition, genes MCU, CYB5R1, and BAG3 were common among the 10 comparative groups that were involved in most of the terms related to fat storage and metabolic process. Perhaps differences in expression levels of lipid-metabolism-related RNAs demonstrated molecular factors underlying beef cattle breed differences in IMF and fat metabolism. The results of this study could inform marker-assisted selection and identify regulatory molecular mechanisms associated with IMF in beef cattle.
Abstract
Intramuscular fat content (IMF), one of the most important carcass traits in beef cattle, is controlled by complex regulatory factors. At present, molecular mechanisms involved in regulating IMF and fat metabolism in beef cattle are not well understood. Our objective was to integrate comparative transcriptomic and competing endogenous RNA (ceRNA) network analyses to identify candidate messenger RNAs (mRNAs) and regulatory RNAs involved in molecular regulation of longissimus dorsi muscle (LDM) tissue for IMF and fat metabolism of 5 beef cattle breeds (Angus, Chinese Simmental, Luxi, Nanyang, and Shandong Black). In total, 34 circRNAs, 57 lncRNAs, 15 miRNAs, and 374 mRNAs were identified by integrating gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses. Furthermore, 7 key subnets with 16 circRNAs, 43 lncRNAs, 7 miRNAs, and 237 mRNAs were detected through clustering analyses, whereas GO enrichment analysis of identified RNAs revealed 48, 13, and 28 significantly enriched GO terms related to IMF in biological process, molecular function, and cellular component categories, respectively. The main metabolic-signaling pathways associated with IMF and fat metabolism that were enriched included metabolic, calcium, cGMP-PKG, thyroid hormone, and oxytocin signaling pathways. Moreover, MCU, CYB5R1, and BAG3 genes were common among the 10 comparative groups defined as important candidate marker genes for fat metabolism in beef cattle. Contributions of transcriptome profiles from various beef breeds and a competing endogenous RNA (ceRNA) regulatory network underlying phenotypic differences in IMF provided novel insights into molecular mechanisms associated with meat quality.
