The Evolutionary Volte-Face of Transposable Elements: From Harmful Jumping Genes to Major Drivers of Genetic Innovation

Transposable elements (TEs) are self-replicating DNA elements that constitute major fractions of eukaryote genomes. Their ability to transpose can modify the genome structure with potentially deleterious effects. To repress TE activity, host cells have developed numerous strategies, including epigenetic pathways, such as DNA methylation or histone modifications. Although TE neo-insertions are mostly deleterious or neutral, they can become advantageous for the host under specific circumstances. The phenomenon leading to the appropriation of TE-derived sequences by the host is known as TE exaptation or co-option. TE exaptation can be of different natures, through the production of coding or non-coding DNA sequences with ultimately an adaptive benefit for the host. In this review, we first give new insights into the silencing pathways controlling TE activity. We then discuss a model to explain how, under specific environmental conditions, TEs are unleashed, leading to a TE burst and neo-insertions, with potential benefits for the host. Finally, we review our current knowledge of coding and non-coding TE exaptation by providing several examples in various organisms and describing a method to identify TE co-option events.