Deciphering the epigenomic regulatory variations reveals function diversity in adipose lineage among different adipose depots of pigs

The distribution of adipose depots in different body parts affects pig production value and human health, governed by complex epigenomic mechanisms. Limited studies on pig adipose depots have hindered the genetic improvement of fat-related economic traits and their biomedical applications. To address this issue, we generated epigenomic maps for backfat, belly fat, groin fat, and intermuscular fat (IMF) in Meishan pigs, integrating ChIP-seq, ATAC-seq, RNA-seq, Hi-C, and public whole-genome sequencing data. Our results reveal that belly/backfat share similar chromatin states, while groin fat/IMF exhibit distinct H3K27ac modification, super-enhancer (SE) dynamics, and open chromatin landscapes compared to belly/backfat. The spatially specific expressions of adipogenic transcription factors (TFs), such as lipid synthesis-related TFs PPARA and SOX6, which are highly expressed in back/belly fat, and adipocyte differentiation TF KLF4 was driven by a groin fat specific SE, underlie these chromatin state disparities. These results also suggest enhanced lipid synthesis in belly/backfat and adipocyte differentiation in groin fat. Moreover, candidate functional variants identified in IMF-gained H3K27ac peaks are primarily associated with meat quality traits. Genes linked to pig backfat thickness may also serve as candidate genes for human obesity due to the conserved cis-regulatory elements and gene expression patterns between humans and pigs. Overall, our epigenomic landscape enhances understanding of adipose depot regulation in mammals, facilitating cross-species insights and precision breeding.