Piwi/piRNA controls feeding behavior by regulating neuropeptide F signaling in locusts

Over the past decade, much emphasis has been placed on identifying the molecular mechanisms of PIWI proteins in the germline function, yet their somatic function remains elusive. In this study, the divergence analysis of PIWI proteins in the arthropod genomes showed that the locust harboring three typical PIWI proteins can serve as a representative to determine the PIWI function in non-Drosophila insects. The analysis of expression quantification and the oxidized small RNA sequencing showed that locust brains exhibit somatic expression of Piwi1/Ago3 and piRNA. The measurements of a series of phenotypic traits using RNA inference assays revealed that the knockdown of Piwi1 expression results in reducing feeding behavior and suppression of anabolic process. To explore the underlying molecular mechanism, we further identified neuropeptide NPF1 acting as the target gene downstream of Piwi1 in reducing feeding behavior through the intronic piRNA-mediated regulation. The results presented here reveal the essential somatic function of PIWI/piRNA pathway as a critical neuropeptide regulator for controlling feeding behavior in locusts.