Abstract
Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE expression in the ovary. However, the bursts of transposition that are expected to follow transposome derepression after piRNA pathway impairment have not yet been reported. Here, we show, at a genome-wide level, that piRNA loss in the ovarian somatic cells boosts several families of the endogenous retroviral subclass of TEs, at various steps of their replication cycle, from somatic transcription to germinal genome invasion. For some of these TEs, the derepression caused by the loss of piRNAs is backed up by another small RNA pathway (siRNAs) operating in somatic tissues at the post transcriptional level. Derepressed transposition during 70 successive generations of piRNA loss exponentially increases the genomic copy number by up to 10-fold.
Highlights
Large fractions of the genome of eukaryotes are made of families of parasitic DNA sequences that are able to replicate by transposing into new locations of the host genome [1]
Conditional knockdown of Piwi in ovarian somatic cells leads to endogenous retroviruses (ERVs) derepression while preserving female fertility The Piwi-interacting RNAs (piRNAs) pathway represses Transposable Elements (TEs) activity in gonads
No evidence for bursts of replicative transposition upon piRNA pathway impairment has been obtained so far. This is partly due to the fact that piRNA pathway mutants are sterile and do not produce the progeny where transposition can be demonstrated
Summary
Large fractions of the genome of eukaryotes are made of families of parasitic DNA sequences that are able to replicate by transposing into new locations of the host genome [1] These Transposable Elements (TEs) are broadly classified in two classes, retrotransposons and DNA transposons, depending on which nucleic acid intermediate (RNA and DNA, respectively) is used during the transposition process. Several exceptions have been reported of Drosophila melanogaster females exhibiting unusually high levels of germinal transposition of a given TE family. This happens, for instance, in females from hybrid dysgenic crosses that suffer from derepression of either a DNA transposon [4,5] or a non-LTR retrotransposon [6]. Observations of increased transposition rates include the case of two strains where either of two ERV families is derepressed in the somatic support cells of the ovary: in both cases, the somatic expression is assumed to lead to the production of virus-like particles that are able to infect the female germline and cause new proviral integrations in the progeny [7,8,9]
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