DDX3 Regulates Reproduction in Locusta migratoria Potentially via Insulin/Insulin-like Growth Factor Signaling

<i>Locusta migratoria</i> (Orthoptera: Acrididae) is a major agricultural pest, characterized by its strong reproductive capacity and rapid reproduction rate. Consequently, identifying novel targets to control or reduce the fecundity of locusts is of significant practical importance. Insulin/insulin-like growth factor signaling (IIS) and the DEAD-box RNA helicase 3 (<i>DDX3</i>) exhibit extensive functional convergence; both govern key life-history traits in insects, including lifespan, metabolic homeostasis, and fecundity. Strikingly, each pathway can influence oogenesis through Notch signaling. Thus, we hypothesize that <i>DDX3</i> may modulate insect reproduction associated with this pathway. After silencing <i>DDX3</i> through RNA interference (RNAi), we found that the key genes of IIS were significantly downregulated and the content of trehalose and glycogen decreased significantly, proving that <i>DDX3</i> inhibits reproduction associated with IIS. In addition, <i>DDX3</i> interference led to a marked reduction in the mRNA expression of <i>Vg</i>s (<i>VgA</i>/<i>B</i>) and <i>JHAMT</i>, which was accompanied by a significant decrease in ovarian development. Furthermore, integrating our previous findings, we posit that <i>DDX3</i> engages in locust reproduction via the regulation of pivotal IIS pathway genes such as <i>InR</i> and <i>FOXO</i>, thereby completing the putative regulatory circuitry through which <i>DDX3</i> modulates reproductive processes. Our findings deepen the understanding of the endogenous circuitry governing locust reproduction and provide novel theoretical justification for targeting <i>DDX3</i> in locust management strategies.