Integrated three-dimensional genomic analysis reveals that dynamic changes in chromatin structure are associated with...

Egg-laying performance varies significantly among different chicken breeds. The liver, as the central organ responsible for yolk precursor synthesis, largely determines the egg production performance of poultry. However, the underlying genetic basis of these phenotypic differences remains poorly understood. In this study, we systematically compared the transcriptomic differences and dynamic changes in three-dimensional (3D) genome organization in the livers of a high-producing commercial breed (White Leghorn) and a low-producing indigenous breed (Wenchang chicken) during the laying period. Transcriptomic analysis revealed that significantly upregulated genes in White Leghorns were highly enriched in lipid metabolism-related pathways, including CPT1A, ACSL1, ACACB, ACOX1, EHHADH, DHCR7, and SQLE, whereas highly expressed genes in Wenchang chickens were mainly enriched in pathways such as the ribosome. 3D genomic analysis demonstrated that although the global chromatin framework of the liver was relatively conserved between the two breeds, significant breed-specific remodeling occurred in local spatial organization. At the compartment level, key metabolic genes such as BBOX1 and GRB14 underwent B-to-A compartment switching and transcriptional activation in White Leghorns, which may be associated with their high laying trait. At the topologically associating domain (TAD) level, the livers of White Leghorns exhibited relatively weaker boundary insulation and a looser intra-domain folding state. Furthermore, the functional enrichment results of breed-specific TAD boundary genes were relatively consistent with the transcriptomic profiles. At the chromatin loop level, White Leghorns displayed stronger intra-loop spatial interactions. Critically, White Leghorn-specific chromatin loops precisely anchored and upregulated some key genes involved in lipid metabolism, such as ACSL1, ACOX1, and EHHADH, whereas Wenchang chicken-specific loops primarily drove the expression of ribosome-related genes. In summary, this study reveals a close correlation between the dynamic changes in the 3D chromatin structure and the transcription differences in the livers of the two chicken breeds, and these differences may be linked to egg production performance. These findings provide new insights into the genetic basis underlying the liver's role in regulating poultry laying performance.