Abstract
Intramuscular fat content (IMF) is a complex trait influencing the technological and sensorial features of meat products and determining pork quality. Thus, we aimed at analyzing through RNA-sequencing the Semimembranosus muscle transcriptome of Italian Large White pigs to study the gene networks associated with IMF deposition. Two groups of samples were used; each one was composed of six unrelated pigs with extreme and divergent IMF content (0.67 ± 0.09% in low IMF vs. 6.81 ± 1.17% in high IMF groups) that were chosen from 950 purebred individuals. Paired-end RNA sequences were aligned to Sus scrofa genome assembly 11.1 and gene counts were analyzed using WGCNA and DeSeq2 packages in R environment. Interestingly, among the 58 differentially expressed genes (DEGs), several were related to primary cilia organelles (such as Lebercilin 5 gene), in addition to the genes involved in the regulation of cell differentiation, in the control of RNA-processing, and G-protein and ERK signaling pathways. Together with cilia-related genes, we also found in high IMF pigs an over-expression of the Fibroblast Growth Factor 2 (FGF2) gene, which in other animal species was found to be a regulator of ciliogenesis. Four WGCNA gene modules resulted significantly associated with IMF deposition: grey60 (P = 0.003), darkturquoise (P = 0.022), skyblue1 (P = 0.022), and lavenderblush3 (P = 0.030). The genes in the significant modules confirmed the results obtained for the DEGs, and the analysis with “cytoHubba” indicated genes controlling RNA splicing and cell differentiation as hub genes. Among the complex molecular processes affecting muscle fat depots, genes involved in primary cilia may have an important role, and the transcriptional reprogramming observed in high IMF pigs may be related to an FGF-related molecular cascade and to ciliogenesis, which in the literature have been associated with fibro-adipogenic precursor differentiation.
Highlights
Pork meat represents one of the main sources of protein and fat for humans, accounting for about 30% of meat consumption worldwide [1]
The present study was conceived with the objectives of i) evaluating in the Semimembranosus muscle (SM) the gene expression differences between two groups of Italian Large White purebred heavy pigs divergent for intramuscular fat (IMF) content and identifying the pathways in which the differentially expressed genes are involved; ii) investigating the gene co-expression patterns related to the divergent deposition of IMF and interpreting the possible molecular mechanisms related to the variability noticed for this trait
The genes identified in this study associated with IMF in pigs were mainly involved in the regulation of DNA transcription and cell differentiation, in primary cilia morphogenesis, and with several intracellular signaling cascades
Summary
Pork meat represents one of the main sources of protein and fat for humans, accounting for about 30% of meat consumption worldwide [1]. The important role of muscle-interspersed adipocytes in muscle energy metabolism has been highlighted by the increasing evidence of the involvement of IMF in the modulation of cardiovascular risk factors [16] and insulin resistance [17], and in the existence of a muscle-tofat “crosstalk” mediated by biologically active molecules such as adipokines and myokines [18, 19] In this scenario, the investigation of the molecular patterns related to IMF deposition may provide new information useful for a more efficient selection aimed at increasing IMF in pork and pork products quality without negatively affecting lean mass deposition. The present study was conceived with the objectives of i) evaluating in the SM the gene expression differences between two groups of Italian Large White purebred heavy pigs divergent for IMF content and identifying the pathways in which the differentially expressed genes are involved; ii) investigating the gene co-expression patterns related to the divergent deposition of IMF and interpreting the possible molecular mechanisms related to the variability noticed for this trait
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