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Lipidomic and Transcriptomic Analysis of the Longissimus Muscle of Luchuan and Duroc Pigs.

ABSTRACT: Meat is an essential food, and pork is the largest consumer meat product in China and the world. Intramuscular fat has always been the basis for people to select and judge meat products. Therefore, we selected the Duroc, a western lean pig breed, and the Luchuan, a Chinese obese pig breed, as models, and used the longissimus dorsi muscle for lipidomics testing and transcriptomics sequencing. The purpose of the study was to determine the differences in intramuscular fat between the two breeds and identify the reasons for the differences. We found that the intramuscular fat content of Luchuan pigs was significantly higher than that of Duroc pigs. The triglycerides and diglycerides related to flavor were higher in Luchuan pigs compared to Duroc pigs. This phenotype may be caused by the difference in the expression of key genes in the glycerolipid metabolism signaling pathway.

SUBMITTER: Zhang Z

PROVIDER: S-EPMC8154583 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Luchuan pig is a typical obese pig breed in China, and the diameter and area of its longissimus dorsi muscle fibers are significantly smaller than those of Duroc (lean) pig. Skeletal muscle fiber characteristics are related to meat quality of livestock. There is a significant correlation between the quality of different breeds of pork and the characteristics of muscle fiber, which is an important factor affecting the quality of pork. The diameter and area of muscle fibers are related to muscle growth and development. Therefore, we used the assay for transposase-accessible chromatin using sequencing (ATAC-seq) and RNA sequencing (RNA-seq) analysis to investigate the potential mechanism underlying the difference in skeletal muscle growth and development between the two types of pigs. First, transposase-accessible chromatin was analyzed to map the landscape of open chromatin regions and transcription factor binding sites. We identified several transcription factors that potentially affected muscle growth and development, including TFAP4, MAX, NHLH1, FRX5, and TGIF1. We also found that transcription factors with basic helix-loop-helix structures had a preference for binding to genes involved in muscle development. Then, by integrating ATAC-seq and RNA-seq, we found that the Wnt signaling pathway, the mTOR signaling pathway, and other classical pathways regulate skeletal muscle development. In addition, some pathways that might regulate skeletal muscle growth, such as parathyroid hormone synthesis, secretion, and action, synthesis and degradation of ketone bodies, and the thyroid hormone signaling pathway, which were significantly enriched. After further study, we identified a number of candidate genes (ASNS, CARNS1, G0S2, PPP1R14C, and SH3BP5) that might be associated with muscle development. We also found that the differential regulation of chromatin openness at the level of some genes was contrary to the differential regulation at the level of transcription, suggesting that transcription factors and transcriptional repressors may be involved in the regulation of gene expression. Our study provided an in-depth understanding of the mechanism behind the differences in muscle fibers from two species of pig and provided an important foundation for further research on improving the quality of pork.

Project description:Luchuan pig, an obese indigenous Chinese porcine breed, has a desirable meat quality and reproductive capacity. Duroc, a traditional western breed, shows a faster growth rate, high feed efficiency and high lean meat rate. Given the unique features these two porcine breeds have, it is of interest to investigate the underlying molecular mechanisms behind their distinctive nature. In this study, the metabolic and transcriptomic profiles of longissimus dorsi muscle from Duroc and Luchuan pigs were compared. A total of 609 metabolites were identified, 77 of which were significantly decreased in Luchuan compared to Duroc, and 71 of which were significantly elevated. Most differentially accumulated metabolites (DAMs) upregulated in Luchuan were glycerophospholipids, fatty acids, oxidized lipids, alcohols, and amines, while metabolites downregulated in Luchuan were mostly amino acids, organic acids and nucleic acids, bile acids and hormones. From our RNA-sequencing (RNA-seq) data we identified a total of 3638 differentially expressed genes (DEGs), 1802 upregulated and 1836 downregulated in Luchuan skeletal muscle compared to Duroc. Combined multivariate and pathway enrichment analyses of metabolome and transcriptome results revealed that many of the DEGs and DAMs are associated with critical energy metabolic pathways, especially those related to glucose and lipid metabolism. We examined the expression of important DEGs in two pathways, AMP-activated protein kinase (AMPK) signaling pathway and fructose and mannose metabolism, using Real-Time Quantitative Reverse Transcription PCR (qRT-PCR). Genes related to glucose uptake, glycolysis, glycogen synthesis, fatty acid synthesis (PFKFB1, PFKFB4, MPI, TPI1, GYS1, SLC2A4, FASN, IRS1, ULK1) are more activated in Luchuan, while genes related to fatty acid oxidation, cholesterol synthesis (CPT1A, HMGCR, FOXO3) are more suppressed. Energy utilization can be a decisive factor to the distinctive metabolic, physiological and nutritional characteristics in skeletal muscle of the two breeds we studied. Our research may facilitate future porcine breeding projects and can be used to reveal the potential molecular basis of differences in complex traits between various breeds.

Project description:Luchuan pig is a typical obese pig breed in China, and the diameter and area of its longissimus dorsi muscle fibers are significantly smaller than those of Duroc (lean) pig. Skeletal muscle fiber characteristics are related to meat quality of livestock. The smaller the diameter and area of muscle fiber, the better the meat quality. The diameter and area of muscle fibers are related to muscle growth and development. Therefore, we used the assay for transposase-accessible chromatin using sequencing (ATAC-seq) and RNA sequencing (RNA-seq) analysis to investigate the potential mechanism underlying the difference in skeletal muscle growth and development between the two types of pigs. First, transposase-accessible chromatin was analyzed to map the landscape of open chromatin regions and transcription factor binding sites. We identified several transcription factors that potentially affected muscle growth and development, including TFAP4, MAX, NHLH1, FRX5, and TGIF1. We also found that transcription factors with basic helix-loop-helix structures had a preference for binding to genes involved in muscle development. Then, by integrating ATAC-seq and RNA-seq, we found that the Wnt signaling pathway, the mTOR signaling pathway, and other classical pathways regulate skeletal muscle development. In addition, we found some pathways that might regulate skeletal muscle growth, such as parathyroid hormone synthesis, secretion, and action, synthesis and degradation of ketone bodies, and the thyroid hormone signaling pathway, which were significantly enriched. After further study, we identified a number of candidate genes (ASNS, CARNS1, G0S2, PPP1R14C, and SH3BP5) that might be associated with muscle development. We also found that the differential regulation of chromatin openness at the level of some genes was contrary to the differential regulation at the level of transcription, suggesting that transcription factors and transcriptional repressors may be involved in the regulation of gene expression. Our study provided an in-depth understanding of the mechanism behind the differences in muscle fibers from two species of pig and provided an important foundation for further research on improving the quality of pork.

Project description:BackgroundThe two main genetic types in Iberian pig production show important phenotypic differences in growth, fattening and tissue composition since early developmental stages. The objective of this work was the evaluation of muscle transcriptome profile in piglets of both genetic types, in order to identify genes, pathways and regulatory factors responsible for their phenotypic differences. Contemporary families coming from pure Iberian pigs (IB) or from crossing with Duroc boars (DU×IB) were generated. Piglets (14 from each genetic type) were slaughtered at weaning (28 days) and longissimus dorsi was sampled for composition and gene expression studies. RNA was obtained and hybridized to Affymetrix Porcine Genechip expression arrays.ResultsLoin muscle chemical composition showed significant differences between genetic types in intramuscular fat content (6.1% vs. 4.3% in IB and DUxIB animals, respectively, P = 0.009) and in saturated (P = 0.019) and monounsaturated fatty acid proportions (P = 0.044). The statistical analysis of gene expression data allowed the identification of 256 differentially expressed (DE) genes between genetic types (FDR < 0.10), 102 upregulated in IB and 154 upregulated in DU×IB. Transcript differences were validated for a subset of DE genes by qPCR. We observed alteration in biological functions related to extracellular matrix function and organization, cellular adhesion, muscle growth, lipid metabolism and proteolysis. Candidate genes with known effects on muscle growth were found among the DE genes upregulated in DU×IB. Genes related to lipid metabolism and proteolysis were found among those upregulated in IB. Regulatory factors (RF) potentially involved in the expression differences were identified by calculating the regulatory impact factors. Twenty-nine RF were found, some of them with known relationship with tissue development (MSTN, SIX4, IRX3), adipogenesis (CEBPD, PPARGC1B), or extracellular matrix processes (MAX, MXI1). Correlation among the expression of these RF and DE genes show relevant differences between genetic types.ConclusionThese results provide valuable information about genetic mechanisms determining the phenotypic differences on growth and meat quality between the genetic types studied, mainly related to the development and function of the extracellular matrix and also to some metabolic processes as proteolysis and lipid metabolism. Transcription factors and regulatory mechanisms are proposed for these altered biological functions.

Project description:Meat quality is a complex trait influenced by many factors, including genetics, nutrition, feeding environment, animal handling, and their interactions. To elucidate relevant factors affecting pork quality associated with oxidative stress and muscle development, we analyzed protein expression in high quality longissimus dorsi muscles (HQLD) and low quality longissimus dorsi muscles (LQLD) from Duroc pigs by liquid chromatographytandem mass spectrometry (LC-MS/MS)-based proteomic analysis. Between HQLD (n = 20) and LQLD (n = 20) Duroc pigs, 24 differentially expressed proteins were identified by LC-MS/MS. A total of 10 and 14 proteins were highly expressed in HQLD and LQLD, respectively. The 24 proteins have putative functions in the following seven categories: catalytic activity (31%), ATPase activity (19%), oxidoreductase activity (13%), cytoskeletal protein binding (13%), actin binding (12%), calcium ion binding (6%), and structural constituent of muscle (6%). Silver-stained image analysis revealed significant differential expression of lactate dehydrogenase A (LDHA) between HQLD and LQLD Duroc pigs. LDHA was subjected to in vitro study of myogenesis under oxidative stress conditions and LDH activity assay to verification its role in oxidative stress. No significant difference of mRNA expression level of LDHA was found between normal and oxidative stress condition. However, LDH activity was significantly higher under oxidative stress condition than at normal condition using in vitro model of myogenesis. The highly expressed LDHA was positively correlated with LQLD. Moreover, LDHA activity increased by oxidative stress was reduced by antioxidant resveratrol. This paper emphasizes the importance of differential expression patterns of proteins and their interaction for the development of meat quality traits. Our proteome data provides valuable information on important factors which might aid in the regulation of muscle development and the improvement of meat quality in longissimus dorsi muscles of Duroc pigs under oxidative stress conditions.

Project description:With the rapid development of economy, the demand for beef, with regard to quantity and quality, by consumers has been increasing in China. Chinese native cattle are characterized by their abundant genetic resources, unique origins, large breeding stocks, and robust environmental adaptability. Thus, to explore the genetic mechanisms on regulating meat quality in Chinese native cattle is of great importance to satisfy increased requirements for beef production. In this study, we investigated three breeds of cattle, namely Yunling, Wenshan, and Simmental, at the age of 12 months. Animals were classified into three groups (n = 5/breed). Growth traits including body weight and body size and plasma hormone levels were measured. Body weight of Wenshan cattle was significantly lower than that of Yunling and Simmental cattle (P < 0.05). Again, body size indexes, such as withers height, body slanting length, chest circumference, and hip and rump length, were significantly lower in Wenshan cattle than those in Yunling and Simmental cattle (P < 0.05). However, there were no significant differences in those indexes between Yunling and Simmental cattle (P > 0.05). Cattle were slaughtered at the age of 18 months and then meat color, pH, pressing losses, muscle tenderness, and cooking losses were measured at 0, 1, 2, 3, 5, and 7 days. Data revealed differences in meat quality among the three breeds analyzed. Based on transcriptomic sequencing and bioinformatic analysis, we observed 3,198 differentially expressed genes related to meat quality, of which 1,750 genes were upregulated. Moreover, we found two important signaling pathways closely linked to meat quality, namely adipocytokine signaling pathway [e.g., Leptin receptor (LEPR)] and protein processing in the endoplasmic reticulum [e.g., signal transducer and activator of transcription 3 (STAT3), heat shock protein (HSPA12A), and calpain 1 (CAPN1)]. The results of transcripts were further verified by qRT-PCR. Using correlation analysis between gene expression levels and shear force, we also identified two functional genes (e.g., HSPA12A and CAPN1) associated with meat quality. Overall, this study provides new sights into novel targets and underlying mechanisms to modulate meat quality in Chinese native cattle.

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Lipidomic and Transcriptomic Analysis of the Longissimus Muscle of Luchuan and Duroc Pigs.

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