Parasitoid Wasps Can Manipulate Host Trehalase to the Benefit of Their Offspring

SIMPLE SUMMARY: Trehalase plays a vital role in carbohydrate metabolism in insects. However, less attention has been paid to its role in the interaction between parasitoid wasps and their hosts. Here, we found that two trehalase genes, SlTre1 and SlTre2, were highly expressed in the third instar larvae of Spodoptera litura after they were parasitized by Meterous pulchricornis. Furthermore, we silenced SlTre1 and SlTre2 in parasitized S. litura larvae, and after that, the activity of trehalase and the content of glucose of the host larvae were decreased significantly. In addition, after knocking down SlTre1 or SlTre2 in parasitized S. litura larvae, the fitness of parasitoid offspring was negatively affected. The results obtained here suggested that parasitoid wasps can induce the upregulation of trehalase in their host larvae and support the development of their offsprings. The present study provides a theoretical base for functional research on trehalase genes in the coevolution between parasitoid wasps and their hosts. ABSTRACT: Trehalase is an essential hydrolase of trehalose in insects. However, whether and how trehalase performs in the association of parasitoid wasps and their hosts still remains unknown. Here, the exact function of trehalase of the general cutworm Spodoptera litura after it was parasitized by its predominant endoparasitoid Meterous pulchricornis was elucidated. Two trehalase genes (SlTre1, SlTre2) were identified, and they were highly expressed five days after parasitization by M. pulchricornis. Then, we successfully silenced SlTre1 and SlTre2 in parasitized third instar S. litura larvae. The content of glucose, which is the hydrolysate of trehalose, was significantly decreased after silencing SlTres in parasitized S. litura larvae, and the activities of trehalase were also notably reduced. In addition, the cocoon weight, the emergence rate, proportion of normal adults, and the body size of parasitoid offsprings were significantly decreased in SlTre1- or SlTre2-silenced groups compared to the controls. These results implied that parasitization by parasitoids regulated the trehalase of host larvae to create a suitable nutritional environment for the parasitoid offspring. The present study broadens the knowledge of trehalase in the interaction between parasitoids and their hosts and is of benefit to biological control of S. litura acting by parasitoid wasps.