Integrated Multi-Omics of the Longissimus Dorsal Muscle Transcriptomics and Metabolomics Reveals Intramuscular Fat Accumulation Mechanism with Diet Energy Differences in Yaks

Abstract

IMF (intramuscular fat, IMF), as a key index for evaluating meat quality traits (shear force and cooking loss, etc.), and its deposition process are jointly regulated by nutritional and genetic factors. In this study, we analyzed the molecular regulation mechanism of IMF deposition in the LD (longissimus dorsal muscle, LD) by dietary energy level in Pamir yaks. Meat quality assessment showed that the meat quality of the High-energy diet group (1.53 MJ/Kg, G) and the Medium-energy diet group (1.38 MJ/Kg, Z) were significantly improved compared with that of the Low-energy diet group (0.75 MJ/Kg, C), in which IMF content in the LD of yaks in G group was significantly higher (p < 0.05) compared with Z and C groups. Further analysis by combined transcriptomics and lipid metabolomics revealed that the differences in IMF deposition mainly originated from the metabolism of lipids, such as TG (triglycerides, TG), PS (phosphatidylserine, PS), and LPC (lysophosphatidylcholine, LPC), and were influenced by SFRP4, FABP4, GADD45A, PDGFRA, RBP4, and DGAT2 genes, further confirming the importance of lipid-gene interactions in IMF deposition. This study reveals the energy-dependent epigenetic regulatory mechanism of IMF deposition in plateau ruminants, which provides molecular targets for optimizing yak nutritional strategies and quality meat production, while having important theoretical and practical value for the sustainable development of livestock husbandry on the Tibetan Plateau.

Keywords: intramuscular fat deposition; lipid metabolomics; longissimus dorsal muscle; transcriptomics; yak.

Figure 1

Histological analysis of the LD. hematoxylin–eosin staining of longitudinal sections of the longissimus dorsal muscle of yaks in groups G (a), Z (b), C (c). (d) Myofiber diameters of the LD of yaks in groups G, Z, C. Different letter marks indicate significant differences (p < 0.01).

Figure 2

(a) PCA score plot showing lipid profiles in yak dorsal muscle across dietary energy groups (C: green, Z: blue, G: orange). (b) OPLS-DA permutation test results with overall sample scores; R2 (R-squared), Q2 (Q-squared). (c) Thermograms depicting lipid variations in yak muscle, where red and blue represent increased and decreased SDL concentrations, respectively.

Figure 3

(a) Heatmap of differentially expressed genes in the longissimus dorsal muscle of yaks in groups C and Z, (b) PCA score plot of differentially expressed genes in yak dorsal muscle across dietary energy levels. (c) Heatmap showing gene expression differences between groups C and G. (d) Comparison of log2FC values for eight DEGs (COL11A2, HOXC10, FN1, FBN1, AGT, FOS, SCD, SLC27A6) between qPCR and mRNA-Seq results.

Figure 4

(a) Heatmap displaying the top 30 lipids and DEGs in yak dorsal muscle (groups C vs. Z). Red/blue indicate positive/negative correlations (“*” indicates that the correlation p-value is <0.05, “**” indicates that the correlation p-value is <0.01, and “***” indicates that the correlation p-value is <0.001.). (b) Network diagram of the top 20 lipids and differentially expressed genes in the longissimus dorsal muscle of yaks in group C vs. Z. Node shape, size, and color indicate the histological type, connectivity size, and corresponding degree of difference, respectively; and node color from red to blue corresponds to log2FoldChange from positive to negative. (c) Heatmap of the top 30 lipids and differentially expressed genes in the longissimus dorsal muscle of yaks from groups C and G. (d) Network diagram of the top 20 lipids and differentially expressed genes in the longissimus dorsal muscle of yaks in group C vs. G.

Figure 5

(a) Correlation heatmap of intramuscular fat content, DEGs and SDLs in yak dorsal muscle (groups C vs. Z). Red/blue indicate positive/negative correlations (“*” indicates that the correlation p-value is <0.05, “**” indicates that the correlation p-value is <0.01. (b) Corresponding analysis for groups C vs. G.