IAP retrotransposons contribute to the transcriptional diversity of the murine placenta

Transposable elements (TEs) have made important contributions to the evolution of the placenta, and are argued to have played a role in the wide inter-species diversification of this critical developmental organ. Co-option of TEs by host genomes has led to the genesis of important placental genes, as well as trophoblast-specific gene regulatory elements. But whilst multiple TE subfamilies have been shown to act as transcriptional enhancers in early mouse trophoblast development, it remains unclear to what extent TEs regulate placental gene expression after the establishment of a functional fetal-maternal interface. Here, we characterised the TE regulatory and transcriptional landscape in mouse placenta and gauged their evolutionary dynamics through a comparative approach. We found that overall, the gene regulatory potential of TEs is greatly diminished in differentiated mouse trophoblast when compared to their stem cell counterpart. However, evolutionarily young intracisternal A particle (IAP) elements are highly expressed in the placenta and create several alternative, placenta-specific transcriptional start sites for protein-coding genes. IAP elements that are active in the placenta drive species-specific expression of associated genes and display wide genetic diversity between mouse strains. These putative co-option events are therefore evolutionarily recent and may represent a prime example of how TE activity can drive fast placental evolution.