Aphidius ervi venom regulates Buchnera contribution to host nutritional suitability

The association between the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), and the endophagous parasitoid wasp Aphidius ervi Haliday (Hymenoptera: Braconidae) offers a unique model system for studying the molecular mechanisms underlying the complex interactions between the parasitoid, its host and the associated primary symbiont. Here, we investigate in vivo the functional role of the most abundant component of A. ervi venom, Ae-γ-glutamyl transpeptidase (Ae-γ-GT), which is known to induce host castration. Microinjections of double-stranded RNA into A. ervi pupae stably knocked down Ae-γ-GT1 and Ae-γ-GT2 paralogue genes in newly emerged females. These females were used to score the phenotypic changes both in parasitized hosts and in the parasitoid's progeny, as affected by a venom blend lacking Ae-γ-GT. Ae-γ-GT gene silencing enhanced growth both of host and parasitoid, supported by a higher load of the primary bacterial symbiont Buchnera aphidicola. Emerging adults showed a reduced survival and fecundity, suggesting a trade-off with body size. This demonstrates in vivo the primary role of Ae-γ-GT in host ovary degeneration and suggests that this protein counterbalances the proliferation of Buchnera likely triggered by other venom components. Our study provides a new approach to unravelling the complexity of aphid parasitoid venom in vivo, and sheds light on a novel role for Ae-γ-GT in host regulation.