Expansion of ruminant-specific microRNAs shapes target gene expression divergence between ruminant and non-ruminant species

Background: Understanding how species-specific microRNAs (miRNAs) contribute to species-specific phenotypes is a central topic in biology. This study aimed to elucidate the role of ruminant-specific miRNAs in shaping mRNA expression divergence between ruminant and non-ruminant species. Results: We analyzed miRNA and mRNA transcriptomes generated by Illumina sequencing from whole blood samples of cattle and a closely related non-ruminant species, pig. We found evidence of expansion of cattle-specific miRNAs by analyzing miRNA conservation among 57 vertebrate species. The emergence of cattle-specific miRNAs was accompanied by accelerated sequence evolution at their target sites. Further, the target genes of cattle-specific miRNAs show markedly reduced expression compared to their pig and human orthologues. We found that target genes with conserved or non-conserved target sites of cattle-specific miRNAs exhibit reduced expression. One of the significantly enriched KEGG pathway terms for the target genes of the cattle-specific miRNAs is the insulin signalling pathway, raising the possibility that some of these miRNAs may modulate insulin resistance in ruminants. Conclusions: We provide evidence of rapid miRNA-mediated regulatory evolution in the ruminant lineage. Cattle-specific miRNAs play an important role in shaping gene expression divergence between ruminant and nonruminant species, by influencing the expression of targets genes through both conserved and cattle-specific target sites.