Abstract

DNA methylation modifications are implicated in many biological processes. As the most common epigenetic mechanism DNA methylation also affects muscle growth and development. The majority of previous studies have focused on different varieties of yak, but little is known about the epigenetic regulation mechanisms in different age groups of animals. The development of muscles in the different stages of yak growth remains unclear. In this study, we selected the longissimus dorsi muscle tissue at three different growth stages of the yak, namely, 90-day-old fetuses (group E), six months old (group M), and three years old (group A). Using RNA-Seq transcriptome sequencing and methyl-RAD whole-genome methylation sequencing technology, changes in gene expression levels and DNA methylation status throughout the genome were investigated during the stages of yak development. Each group was represented by three biological replicates. The intersections of expression patterns of 7694 differentially expressed genes (DEGs) were identified (padj < 0.01, |log2FC| > 1.2) at each of the three developmental periods. Time-series expression profile clustering analysis indicated that the DEGs were significantly arranged into eight clusters which could be divided into two classes (padj < 0.05), class I profiles that were downregulated and class II profiles that were upregulated. Based on this cluster analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that DEGs from class I profiles were significantly (padj < 0.05) enriched in 21 pathways, the most enriched pathway being the Axon guidance signaling pathway. DEGs from the class II profile were significantly enriched in 58 pathways, the pathway most strongly enriched being Metabolic pathway. After establishing the methylation profiles of the whole genomes, and using two groups of comparisons, the three combinations of groups (M-vs.-E, M-vs.-A, A-vs.-E) were found to have 1344, 822, and 420 genes, respectively, that were differentially methylated at CCGG sites and 2282, 3056, and 537 genes, respectively, at CCWGG sites. The two sets of data were integrated and the negative correlations between DEGs and differentially methylated promoters (DMPs) analyzed, which confirmed that TMEM8C, IGF2, CACNA1S and MUSTN1 were methylated in the promoter region and that expression of the modified genes was negatively correlated. Interestingly, these four genes, from what was mentioned above, perform vital roles in yak muscle growth and represent a reference for future genomic and epigenomic studies in muscle development, in addition to enabling marker-assisted selection of growth traits.

Highlights

  • Yaks (Bos grunniens) are large native plateau mammals that have a population of more than 14 million worldwide, principally distributed at high altitudes of 3000 to 5000 m [1]

  • differentially expressed genes (DEGs) related to yak muscle growth and development were identified using RNA-Seq technology

  • We systematically identified DEGs associated with yak skeletal muscle development and investigated their temporal expression profiles during skeletal muscle development across three developmental stages using RNA-Seq

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Summary

Introduction

Yaks (Bos grunniens) are large native plateau mammals that have a population of more than 14 million worldwide, principally distributed at high altitudes of 3000 to 5000 m [1]. Domestication of the yak is believed to have occurred during the introduction of farming techniques into the Qinghai-Tibet plateau in the Neolithic Age, approximately 7000–10,000 years ago [2]. Domesticated yaks have since become the most important livestock in the Qinghai-Tibet Plateau and have dispersed throughout the region, following the migration patterns of the Tibetan population [3]. Accelerating growth to improve the rate of meat production has become the principal research focus in yak breeding. Rates of animal muscle growth and development vary among breeds as important quantitative traits [5,6]

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