Allele-specific regulatory effects on the pig transcriptome

Allele-specific expression (ASE) refers to the preferential expression of one allele over the other and contributes to adaptive phenotypic plasticity. Here, we used a reciprocal cross-model between phenotypically divergent European Berkshire and Asian Tibetan pigs to characterize 2 ASE classes: imprinting (i.e., the unequal expression between parental alleles) and sequence dependent (i.e., unequal expression between breed-specific alleles). We examined 3 transcript types, including protein-coding genes (PCGs), long noncoding RNAs, and transcripts of unknown coding potential, across 7 representative somatic tissues from hybrid pigs generated by reciprocal crosses.

We identified a total of 92 putative imprinted transcripts, 69 (75.00%) of which are described here for the first time. By combining the transcriptome from purebred Berkshire and Tibetan pigs, we found ∼6.59% of PCGs are differentially expressed between breeds that are regulated by trans-elements (e.g., transcriptional factors), while only ∼1.35% are attributable to cis (e.g., promoters). The higher prevalence of trans-PCGs indicates the dominated effects of trans-regulation in driving expression differences and shaping adaptive phenotypic plasticity between breeds, which were supported by functional enrichment analysis. We also found strong evidence that expression changes mediated by cis-effects were associated with accumulated variants in promoters.

Our study provides a comprehensive map of expression regulation that constitutes a valuable resource for the agricultural improvement of pig breeds.