Trapping a somatic endogenous retrovirus into a germline piRNA cluster immunizes the germline against further invasion

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Abstract

Abstract Background For species survival, the germline must faithfully transmit the genetic information to the progeny. Transposable elements (TEs), which are major components of eukaryotic genomes, constitute a significant threat to genome stability due to their mobility. In the metazoan germline, their mobilization is limited by a class of small RNAs that are called PIWI-interacting RNAs (piRNAs) and are produced by dedicated genomic loci called piRNA clusters. Although the piRNA pathway is an adaptive genomic immunity system, it remains unclear how the germline is protected from transposon invasion. To address this question, we used Drosophila melanogaster lines harboring a deletion within flamenco, a major piRNA cluster that is specifically expressed in somatic follicular cells. This deletion leads to derepression of the retrotransposon ZAM and to germline genome invasion. Results In this mutant line that express ZAM in somatic follicular cells, we identified de novo production of sense and antisense ZAM- derived piRNAs that displayed a germinal molecular signature. These piRNAs originated from a new ZAM insertion into a germline dual-strand piRNA cluster and silenced ZAM expression specifically in germ cells. Finally, we found that ZAM trapping in a germinal piRNA cluster is a frequent event that occurs early during the isolation of the mutant line. Conclusions Transposons can hijack the host developmental process to propagate whenever their silencing is lost. Here, we show that the germline can protect itself by trapping invading somatic-specific TEs into germline piRNA clusters. This is the first demonstration of “auto-immunization” of the germline endangered by mobilization of a surrounding somatic TE.

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