Multi-Omics Analysis of Transcriptomic and Metabolomics Profiles Reveal the Molecular Regulatory Network of Marbling in Early Castrated Holstein Steers

Abstract

The intramuscular fat (IMF), or so-called marbling, is known as potential determinant of the high quality beef in China, Korea, and Japan. Of the methods that affect IMF content in cattle, castration is markedly regarded as an effective and economical way to improve the deposition of IMF but with little attention to its multi-omics in early-castrated cattle. The aim of this study was to investigate the liver transcriptome and metabolome of early-castrated Holstein cattle and conduct a comprehensive analysis of two omics associated with the IMF deposition using transcriptomics and untargeted metabolomics under different treatments: non−castrated and slaughtered at 16 months of age (GL16), castrated at birth and slaughtered at 16 months of age (YL16), and castrated at birth and slaughtered at 26 months of age (YL26). The untargeted metabolome was analyzed using ultrahigh-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry. The transcriptome of the hepatic genes was analyzed to identify marbling-related genes. Using untargeted metabolomics, the main altered metabolic pathways in the liver of cattle, including those for lipid and amino acid metabolism, were detected in the YL16 group relative to the GL16 and YL26 groups. Significant increases in the presence of betaine, alanine, and glycerol 3-phosphate were observed in the YL16 group (p < 0.05), which might have contributed to the improved beef-marbling production. Compared to the GL16 and YL26 groups, significant increases in the presence of glutathione, acetylcarnitine, and riboflavin but decreases in diethanolamine and 2-hydroxyglutarate were identified in YL16 group (p < 0.05), which might have been beneficial to the beef’s enhanced functional quality. The gene expressions of GLI1 and NUF2 were downregulated and that of CYP3A4 was upregulated in the YL16 group; these results were strongly correlated with the alanine, betaine, and leucine, respectively, in the liver of the cattle. In conclusion, implementation of early castration modified the hepatic metabolites and the related biological pathways by regulating the relevant gene expressions, which could represent a better rearing method for production of high marbled and healthier beef products.

— Invited Review — Translational gut microbiome research for strategies to improve beef cattle production sustainability and meat quality

“…Higher levels of tricarboxylic acid (TCA) cycle (cis-aconitic acid, citric acid, isocitric acid), lipid synthesis (3-hydroxybutiric acid, glycerol 3-phosphate), FA metabolism (o-acetylcarnitine), diabetes (methylhistidine, asymmetric dimethylarginine), and glucose homeostasis (hippuric acid) were found for blood metabolme in Wagyu cattle compared to Holstein [ 46 ]. Early castration of Holstein calves was shown to improve beef marbling grade [ 47 ]. Untargeted metabolomics analysis of the liver showed that the early castration group had increased betaine, glycerol 3-phosphate, glutathione, acetylcarnitine, riboflavin, and alanine and decreased diethanolamine, glycine, and 2-hydroxyglutarate, which were associated with the increased marbling [ 47 ].…”

“…Early castration of Holstein calves was shown to improve beef marbling grade [ 47 ]. Untargeted metabolomics analysis of the liver showed that the early castration group had increased betaine, glycerol 3-phosphate, glutathione, acetylcarnitine, riboflavin, and alanine and decreased diethanolamine, glycine, and 2-hydroxyglutarate, which were associated with the increased marbling [ 47 ]. The above findings suggest that both host and microbial metabolites could play a role in affecting meat quality.…”

The Pathological and Ultrasonographic Evaluation of the Chemical Castration in Dogs using Calcium Chloride Injection

“…Currently, in the cattle breeding industry, there are many management difficulties with pain and distress on the animals. Thus, using castration techniques to improve animal interest benefits the said industry (8). The intracellular antioxidant levels decreased in the chemical-castrated animals by elevating reactive oxygen species (ROS) levels.…”