The Roles of Transposable Elements in Transgenerational Inheritance and Genome Evolution

Transposable elements and related DNA sequences, such as remnants of retrotransposons, constitute a substantial portion of eukaryotic genomes. The widespread presence of these sequences suggests that, in an evolutionary context, they were either neutral or contributed to enhanced organismal fitness. This contribution occurred, in part, by providing the “raw sequence materials” necessary for genome expansion and diversification. The integration and transposition of these so-called “selfish” sequences led to the emergence of specialized control elements, such as enhancers or repressors, as well as structural organization sequences like centromeric repeats and their corresponding binding proteins. Additionally, enzymes encoded by transposons played a pivotal role in the development of the adaptive immune system and facilitated complex neurodevelopmental somatic genome mosaicism. These mechanisms also evolved to counteract the antagonistic effects of additional “selfish” sequences. A particularly intriguing development was the domestication and repurposing of a piggyBac-like transposase in ciliates. This adaptation enables ciliates to efficiently and precisely excise invasive sequences, showcasing a unique mechanism for combating the impact of “selfish” genetic elements. The process is regulated through a complex epigenetic network involving small RNA guided comparison of the germ line genome with the maternal somatic genome. This process represents a form of transgenerational inheritance and environmental conditions or modifications of the maternal somatic genome can lead to alternative outcomes in the new somatic genome of the offspring. Importantly, this process highlights the functional diversity enabled by transposable elements and their roles for the evolution of eukaryotic genomes and the genomic innovations transferable to the next generations.