Spatiotemporal coordination of 3D chromatin architecture and gene expression dynamics during ovine embryonic myogenesis

BACKGROUND: Sheep (Ovis aries) are economically important agricultural animals, which provide meat, wool, and fur for humans. The growth and development of embryonic skeletal muscle are crucial for ovine muscle quality and yield. Increasing evidence has shown the three-dimensional (3D) genome structure is involved in gene transcriptional regulation and a variety of biological processes. Although the 3D genome structure in various species and cell types has been characterized, the dynamic remodeling of chromatin architecture during ovine skeletal muscle development remain poorly understood. RESULTS: Using Hi-C, RNA-seq, and ChIP-seq methods, we systematically explored the dynamics of the 3D genome structure, transcriptome, and epigenome in ovine skeletal muscle tissue from 90-day-old (D90) and 120-day-old fetuses (D120). Compared to the D90, the D120 exhibited a decrease in slow muscle fibers and an increase in fast muscle fibers. Additionally, we observed significant reorganization in chromatin compartments, topologically associating domains (TADs), and loop structures during muscle development. Notably, 18.07 % of A/B compartments switched, with A compartments transitioning to B compartments (9.09 %) and B compartments shifting to A compartments (8.98 %). The number of TADs was slightly lower in D120 (6937) compared to D90 (7036). Additionally, the number of loops increased from 7201 in D90 to 10,008 in D120. We also identified distal regulatory elements of SOX6 and PIK3R1, which play crucial roles in regulating sheep muscle development through loop structures. These findings provide valuable insights into the 3D genome architecture and its role in muscle development. CONCLUSIONS: Our study provides the dynamic 3D chromatin structure of ovine middle and late fetuses skeletal muscle and revealed 3D genome structure is involved in gene expression of fetus skeletal muscle during development. In addition, we identified several potential cis-regulatory elements that regulate gene expression through long range chromatin interactions. We present the first 3D genome data for ovine fetuses skeletal muscle, providing valuable information for epigenome studies. This study offers novel insights into the regulatory mechanism underlying growth and development of ovine muscles.