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Dual-layer transposon repression in heads of Drosophila melanogaster

Abstract : piRNA-mediated repression of transposable elements (TE) in the germline limits the accumulation of heritable mutations caused by their transposition in the genome. It is not clear whether the piRNA pathway plays a functional role in adult, non-gonadal tissues in ​ Drosophila melanogaster. To address this question, we first analyzed the small RNA content of adult ​ Drosophila melanogaster heads. We found that varying amount of piRNA-sized, ping-pong positive molecules in heads correlates with contamination by gonadal tissue during RNA extraction, suggesting that most of piRNAs detected in head sequencing libraries originate from gonads. We next sequenced the heads of wild type and ​ piwi mutants to address whether ​ piwi ​ loss of function would affect the low amount of piRNA-sized, ping-pong negative molecules that are still detected in heads hand-checked to avoid gonadal contamination. We find that loss of ​ piwi ​ does not affect significantly these 24-28 RNA molecules. Instead, we observe increased siRNA levels against the majority of ​ Drosophila transposable element families. To determine the effect of this siRNA level change on transposon expression, we sequenced the transcriptome of wild type, ​ piwi​ , ​ dicer-2 and ​ piwi, dicer-2 double-mutant fly heads. We find that RNA expression levels of the majority of TE families in ​ piwi or ​ dicer-2 mutants remain unchanged and that TE transcript abundance increases significantly only in ​ piwi, dicer-2 double-mutants. These results lead us to suggest a dual-layer model for TE repression in adult somatic tissues. Piwi-mediated transcriptional gene silencing (TGS) established during embryogenesis constitutes the first layer of TE repression whereas Dicer-2-dependent siRNA-mediated post-transcriptional gene silencing (PTGS) provide a backup mechanism to repress TEs that escape silencing by ​ piwi​-mediated TGS.
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Marius van den Beek, Bruno da Silva, Juliette Pouch, Mohammed El Amine Ali Chaouche, Clément Carré, et al.. Dual-layer transposon repression in heads of Drosophila melanogaster. RNA, Cold Spring Harbor Laboratory Press, 2018, 24 (12), pp.1749-1760. ⟨10.1261/rna.067173.118⟩. ⟨hal-01949507⟩

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