piRNA and transposon dynamics in drosophila: A female story

Abstract

The germlines of metazoans contain transposable elements (TEs) causing genetic instability and affecting fitness. To protect the germline from TE activity, gonads of metazoans produce TE-derived PIWI-interacting RNAs (piRNAs) that silence TE expression. In Drosophila, our understanding of piRNA biogenesis is mainly based on studies of the Drosophila melanogaster female germline. However, it is not knownwhether piRNAfunctions are also important in themale germline orwhether andhowpiRNAs are affected by the global genomic context. To address these questions, we compared genome sequences, transcriptomes, and small RNA libraries extracted fromentire testes and ovaries of twosister species:D.melanogaster andDrosophila simulans.We found that most TE-derived piRNAswere produced in ovaries and that piRNA pathway geneswere strongly overexpressed in ovaries comparedwith testes, indicating that the silencing of TEs by the piRNA pathway mainly took place in the female germline. To study the relationship between host piRNAs and TE landscape,we analyzed TE genomic features andhowthey correlatewith piRNAproduction in the two species. In D. melanogaster, we found that TE-derived piRNAs target recently active TEs. In contrast, although Drosophila simulans TEs do not display any features of recent activity, the host still intensively produced silencing piRNAs targeting old TE relics. Together, our results showthat the piRNAsilencingresponsemainly takes place inDrosophila ovaries andindicate that thehost piRNAresponse is implemented following a burst of TE activity and could persist long after the extinction of active TE families.