Abstract
As in most arthropods, the PIWI-interacting RNA (piRNA) pathway in the vector mosquito Aedes aegypti is active in diverse biological processes in both soma and germline. To gain insights into piRNA biogenesis and effector complexes, we mapped the interactomes of the somatic PIWI proteins Ago3, Piwi4, Piwi5, and Piwi6 and identify numerous specific interactors as well as cofactors associated with multiple PIWI proteins. We describe the Piwi5 interactor AAEL014965, the direct ortholog of the Drosophila splicing factor pasilla. We find that Ae. aegypti Pasilla encodes a nuclear isoform and a cytoplasmic isoform, the latter of which is required for efficient piRNA production. In addition, we characterize a splice variant of the Tudor protein AAEL008101/Atari that associates with Ago3 and forms a scaffold for PIWI proteins and target RNAs to promote ping-pong amplification of piRNAs. Our study provides a useful resource for follow-up studies of somatic piRNA biogenesis, mechanism, and function in Aedes mosquitoes.
Highlights
In most animal germlines, the PIWI-interactingRNA pathway represses the activity of selfish genetic elements called transposons (Brennecke et al, 2007)
Our study provides a resource for studying PIWI-interacting RNA (piRNA) biogenesis and piRNA-guided effector complexes in Aedes mosquitoes
Ae. aegypti PIWI proteins associate with highly specific sets of interactors Drosophila is an unusual case among insects, given that expression of piRNAs and PIWI proteins is restricted to germline tissues of this species
Summary
The PIWI-interacting (pi)RNA pathway represses the activity of selfish genetic elements called transposons (Brennecke et al, 2007). In the Drosophila germline, genomically encoded piRNAs associate with the PIWI protein Aubergine (Aub) to guide cleavage of transposon mRNAs in the ping-pong amplification loop, triggering the production of Ago3-bound responder piRNAs (Gunawardane et al, 2007). While slicing in the ping-pong loop generates piRNA 50 ends, their 30 ends are generally generated by downstream endonucleolytic cleavage by Zucchini (Zuc) or another piRNA-loaded PIWI protein (Hayashi et al, 2016). Such cleavage events generate pre-piRNAs that may be trimmed by Nibbler (Nbr) to produce mature piRNAs (Hayashi et al, 2016). While Aub and Ago act post-transcriptionally by slicing transposon RNAs in the cytoplasm, Piwi recruits a nuclear effector complex to induce transcriptional silencing (Le Thomas et al, 2013; Batki et al, 2019; Fabry et al, 2019; Murano et al, 2019; Zhao et al, 2019; Yu et al, 2015; Sienski et al, 2015; Donertas et al, 2013; Ohtani et al, 2013)
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