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

## TL;DR

This study shows that the DDX3 protein helps control reproduction in locusts by influencing insulin signaling and energy reserves.

## Contribution

The study identifies DDX3 as a novel regulator of locust reproduction through its interaction with insulin signaling.

## Key findings

- DDX3 knockdown reduced insulin signaling and energy reserves in locusts.
- DDX3 silencing led to decreased expression of genes involved in egg production.
- DDX3 integrates metabolic and reproductive signaling in locusts.

## Abstract

Locusta migratoria owes its significant agricultural impact to its exceptionally high reproductive output. We demonstrate that the conserved RNA helicase DDX3 functions as a key endogenous regulator of fecundity. RNAi-mediated knockdown of DDX3 (i) attenuated insulin/insulin-like growth factor signaling (IIS), (ii) depleted hemolymph trehalose and fat-body glycogen reserves, and (iii) transcriptionally repressed the yolk protein precursors VgA/B and the juvenile hormone regulator JHAMT. Consequently, ovarian maturation was arrested and egg production was significantly reduced. By establishing DDX3 as a critical node that integrates metabolic and reproductive signaling, our study provides additional predictions regarding the signaling pathways through which DDX3 regulates locust reproduction.

Locusta migratoria (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 (DDX3) 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 DDX3 may modulate insect reproduction associated with this pathway. After silencing DDX3 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 DDX3 inhibits reproduction associated with IIS. In addition, DDX3 interference led to a marked reduction in the mRNA expression of Vgs (VgA/B) and JHAMT, which was accompanied by a significant decrease in ovarian development. Furthermore, integrating our previous findings, we posit that DDX3 engages in locust reproduction via the regulation of pivotal IIS pathway genes such as InR and FOXO, thereby completing the putative regulatory circuitry through which DDX3 modulates reproductive processes. Our findings deepen the understanding of the endogenous circuitry governing locust reproduction and provide novel theoretical justification for targeting DDX3 in locust management strategies.