Abstract
Skeletal muscle development and intramuscular fat (IMF) content, which positively contribute to meat production and quality, are regulated by precisely orchestrated processes. However, changes in three-dimensional chromatin structure and interaction, a newly emerged mediator of gene expression, during the skeletal muscle development and IMF deposition have remained unclear. In the present study, we analyzed the differences in muscle development and IMF content between one-day-old commercial Arbor Acres broiler (AA) and Chinese indigenous Lushi blue-shelled-egg chicken (LS) and performed Hi-C analysis on their breast muscles. Our results indicated that significantly higher IMF content, however remarkably lower muscle fiber diameter was detected in breast muscle of LS chicken compared to that of AA broiler. The chromatin intra-interaction was prior to inter-interaction in both AA and LS chicken, and chromatin inter-interaction was heavily focused on the small and gene-rich chromosomes. For genomic compartmentalization, no significant difference in the number of B type compartments was found, but AA had more A type compartments versus LS. The A/B compartment switching of AA versus LS showed more A to B switching than B to A switching. There were no significant differences in the average sizes and distributions of topologically associating domains (TAD). Additionally, approximately 50% of TAD boundaries were overlapping. The reforming and disappearing events of TAD boundaries were identified between AA and LS chicken breast muscles. Among these, the HMGCR gene was located in the TAD-boundary regions in AA broilers, but in TAD-interior regions in LS chickens, and the IGF2BP3 gene was located in the AA-unique TAD boundaries. Both HMGCR and IGF2BP3 genes exhibited increased mRNA expression in one-day-old AA broiler breast muscles. It was demonstrated that the IGF2BP3 and HMGCR genes regulated by TAD boundary sliding were potential biomarkers for chicken breast muscle development and IMF deposition. Our data not only provide a valuable understanding of higher-order chromatin dynamics during muscle development and lipid accumulation but also reveal new insights into the regulatory mechanisms of muscle development and IMF deposition in chicken.
Highlights
Chicken is often regarded as one of the most desirable meats worldwide due to its proteins, polyunsaturated fatty acids (PUFA), calcium, phosphorus, and iron content, as well as its potential medicinal function and low cost (Soriano-Santos, 2010)
The conspicuously superior intramuscular fat (IMF) content was uncovered in one-day-old Lushi blue-shelled-egg chicken (LS) chicken compared to the Arbor Acres broiler (AA) broiler (Figure 1C), but the latter exhibited a prominent breast muscle fiber diameter in pectorals (Figure 1D)
Significantly increased TG level was observed in the muscle of one-day-old LS chicken compared to AA (p 0.0010) (Figure 1E), and there was no significant difference of muscle total cholesterol (T-CHO) between them (p 0.1048) (Figure 1F)
Summary
Chicken is often regarded as one of the most desirable meats worldwide due to its proteins, polyunsaturated fatty acids (PUFA), calcium, phosphorus, and iron content, as well as its potential medicinal function and low cost (Soriano-Santos, 2010). The genetic selection for body weight, growth rate, and feed conversion rate of broiler chickens has contributed to a prominent increase in production efficiency, such as meat yield; there has been a parallel decrease in meat quality. Skeletal muscle constitutes the largest proportion and most valuable component of meat yield, and its development and composition are of extreme importance in meat production efficiency and quality, breast muscle in poultry. Compared to slow-growing native chicken, fast-growing commercial broilers showed a significant increase in diameter, cross-sectional area, and density of breast muscle fibers at hatching. The increased activity of muscle satellite cells in the late stage of the embryo could make breast muscle development faster (Velleman et al, 2000; Sklan et al, 2003)
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