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

BACKGROUND: For species survival, the germline must faithfully transmit genetic information to the progeny. Transposable elements (TEs) 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 called PIWI-interacting RNAs (piRNAs) produced by dedicated genomic loci called piRNA clusters. Although the piRNA pathway is an adaptive genomic immunity system, it remains unclear how the germline gains protection from a new transposon invasion. RESULTS: To address this question, we analyze Drosophila melanogaster lines harboring a deletion within flamenco, a major piRNA cluster specifically expressed in somatic follicular cells. This deletion leads to derepression of the retrotransposon ZAM in the somatic follicular cells and subsequent germline genome invasion. In this mutant line, we identify de novo production of sense and antisense ZAM-derived piRNAs that display a germinal molecular signature. These piRNAs originated from a new ZAM insertion into a germline dual-strand piRNA cluster and silence ZAM expression specifically in germ cells. Finally, we find 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 a germline endangered by mobilization of a surrounding somatic TE. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-019-1736-x) contains supplementary material, which is available to authorized users.