The piRNA pathway mediates transcriptional silencing of LTR retrotransposons in the soma and germline of Aedes mosquitoes

The PIWI-interacting RNA (piRNA) pathway is crucial for maintaining genomic integrity by suppressing transposable elements in animal germlines. Despite its well-established function in the animal germline, piRNAs and PIWI proteins are expressed in somatic tissues across arthropod species, raising questions about piRNA functions outside the gonads. For example, Aedes albopictus mosquitoes express four PIWI genes, Piwi4, Piwi5, Piwi6 and Ago3, in both germline and somatic tissues. We generated Piwi6 knockout Ae. albopictus cell lines and observed a substantial upregulation of Long Terminal Repeat (LTR)-retrotransposons, among which a full-length endogenous retrovirus that we named AalERV1. We found that Piwi6 silences AalERV1 at the transcriptional level by guiding the deposition of the repressive H3K9me3 histone mark. Importantly, the control of AalERV1 is recapitulated in vivo as Piwi6 knockdown increased AalERV1 expression in both somatic and germline tissues of Ae. albopictus mosquitoes. These results establish Aedes mosquitoes as a model to study nuclear PIWI functions and suggest that somatic piRNA-mediated transposon silencing is evolutionarily conserved across arthropod species.