Evolutionarily conserved but mechanistically diverse piRNA defense against gypsy in insect ovaries

ABSTRACT: Organisms possess highly adaptive defence systems to silence rapidly evolving mobile genetic elements such as transposons. While individual transposons may appear and disappear over time, the evolutionary stability of the defence pathways targeting them remains unclear. In the ovarian somatic cells of Drosophila, envelope-carrying gypsy LTR retrotransposons are silenced by the piRNA pathway, which relies solely on Piwi - an evolutionary derivative of an Aubergine/Piwi gene duplication specific to flies. Recent studies, however, have revealed that envelope-carrying gypsy elements are widespread across metazoans and particularly abundant in insect genomes. This prompted us to investigate whether and how the piRNA pathway targets ovarian somatic gypsy elements in other insects. We found that Aedes and Anopheles mosquitoes, as well as stingless bees and crickets, all express piRNAs targeting gypsy elements in ovarian somatic cells, indicating a continuous arms race for more than 400 million years of insect evolution. Interestingly, we found that Aedes aegypti activate the same set of piRNA clusters in ovarian somatic cells as in other somatic tissues where they are known to target RNA viruses. This suggests that piRNA-based antiviral defence in mosquitoes may have originated from the ovarian somatic piRNA pathway. Moreover, we discovered that the mechanisms of piRNA biogenesis in ovarian somatic cells differ among insects: slicing-independent phasing dominates in dipterans, ping-pong amplification in bees, and slicing-dependent phasing in crickets. These findings indicate that distinct piRNA pathways have independently evolved at different timepoints to silence the same class of retrotransposons in insect evolution.

ORGANISM(S): Teleogryllus oceanicus Eristalis tenax Tetragonula carbonaria Acheta domesticus Bactrocera tryoni Anopheles stephensi Aedes aegypti

PROVIDER: GSE305623 | GEO | 2025/09/17

REPOSITORIES: GEO