A piRNA-lncRNA regulatory network initiates responder and trailer piRNA formation during mosquito embryonic development

Abstract

PIWI-interacting (pi)RNAs are small silencing RNAs that are crucial for the defense against transposable elements in germline tissues of animals. In <i>Aedes aegypti</i> mosquitoes, the piRNA pathway also contributes to gene regulation in somatic tissues, illustrating additional roles for piRNAs and PIWI proteins besides transposon repression. Here, we identify a highly abundant endogenous piRNA (propiR1) that associates with both Piwi4 and Piwi5. PropiR1-mediated target silencing requires base-pairing in the seed region with supplemental base-pairing at the piRNA 3' end. Yet, propiR1 represses a limited set of targets, among which is the lncRNA <i>AAEL027353</i> (<i>lnc027353</i>). Slicing of <i>lnc027353</i> initiates production of responder and trailer piRNAs from the cleavage fragment. Expression of propiR1 commences early during embryonic development and mediates degradation of maternally provided <i>lnc027353</i> Both propiR1 and its lncRNA target are conserved in the closely related <i>Aedes albopictus</i> mosquito, underscoring the importance of this regulatory network for mosquito development.