The role of transposon activity in shaping cis-regulatory element evolution after whole genome duplication

Abstract

AbstractBackgroundTwo of the most potent drivers of genome evolution in eukaryotes are whole genome duplications (WGD) and transposable element (TE) activity. These two mutational forces can also play synergistic roles; WGDs result in both cellular stress and functional redundancy, which would allow TEs to escape host-silencing mechanisms and effectively spread with reduced impact on fitness. As TEs can function as, or evolve into, TE-derived cis-regulatory elements (TE-CREs), bursts of TE-activity following WGD are likely to impact evolution of gene regulation. However, the role of TEs in genome regulatory remodelling after WGDs is unclear. Here we used the genome of Atlantic salmon, which is known to have experienced massive expansion of TEs after a WGD ∼100 Mya, as a model system to explore the synergistic roles of TEs and WGDs on genome regulatory evolution.ResultsWe identified 61,309 putative TE-CREs in Atlantic salmon using chromatin accessibility data from brain and liver. Of these, 82% were tissue specific to liver (43%) or brain (39%) and TE-CREs originating from retroelements were twice as common as those originating from DNA elements. Signatures of selection shaping TE-CRE evolution were evident from depletion of TEs in open chromatin, a bias in tissue-shared TE-CREs towards older TE-insertions, as well as tissue-specific processes shaping the TE-CRE repertoire. The DTT elements (Tc1-Mariners), which exploded in numbers at the time of the WGD, were significantly less prone to evolve into TE-CREs and significantly less potent in driving or repressing transcription compared to other TE-derived sequences. A minority of TEs (16% of consensus TEs) accounted for the origin of 46% of all TE-CREs, but these ‘CRE-superspreaders’ were not temporally associated with the WGD. Rather, the majority of TE-CREs, including those found to be significantly associated with gene regulatory evolution and thus found to drive or repress transcription, evolved from TE activity occurring across tens of millions of years following the WGD event.ConclusionOur results do not support a WGD-associated TE-CRE rewiring of gene regulation. Instead we find that TEs from diverse superfamilies have been particularly effective in spreading TE-CREs and shaping gene regulatory networks under tissue-specific selection pressures, across millions of years following the salmonid WGD.