A venom protein of ectoparasitoid Pachycrepoideus vindemiae, PvG6PDH, contributes to parasitism by inhibiting host glucose‐6‐phosphate metabolism

Abstract

To achieve successful development, female parasitoids, while laying eggs, introduce various virulence factors, mainly venoms, into host insects to manipulate their physiology. Although numerous studies have been conducted to characterize the components of venoms that regulate host immune responses, few systematic investigations have been conducted on the roles of venom proteins in host metabolic regulation. In this investigation, we characterized a novel venom protein in Pachycrepoideus vindemiae called glucose‐6‐phosphate dehydrogenase (PvG6PDH) and showed it has a vital role in regulating host carbohydrate metabolism. PvG6PDH encodes 510 amino acids and features a signal peptide and two conserved “G6PDH” domains. Multiple sequence alignment showed it has high amino acid identity with G6PDH from other pteromalids, and quantitative polymerase chain reaction analysis and immunofluorescent staining demonstrated a significantly higher expression of PvG6PDH in the venom apparatus compared with the carcass. We report that PvG6PDH contributes to parasitism by inhibiting the glucose‐6‐phosphate (G6P) metabolism of host Drosophila melanogaster, as demonstrated by PvG6PDH injection and RNA interference analysis. Further tests revealed that the accumulation of host G6P was caused by the transcriptional inhibition of G6P‐metabolism‐related genes. These findings greatly contribute to our understanding of venom‐mediated host metabolic regulation, further laying the foundation for the development of venom proteins as biological agents for pest control.

Host Transcriptome Analysis of Spodoptera frugiperda Larvae Parasitized by Microplitis manilae

“…Moreover, Zhou et al (2021) screened 278 carbohydrate digestion-related genes differently expressed upon 24 h and 48 wasp parasitization based on transcriptome analysis, which was in good accordance with our present study. In a recent investigation, we reported that the glucose-6-phosphate metabolism of host Drosophila was inhibited after 24 h and 48 h Pachycrepoideus vindemiae parasitization [ 46 ], broadly supporting our present work that most metabolism-related DEGs were significantly downregulated at 24 h and 48 h post-parasitization. To further validate the expression levels of metabolism-related DEGs in parasitized FAW and to contrast with the unparasitized host, 20 genes were randomly selected for qPCR verification, which well correlated with the data of RNA-seq for quantifying the transcriptional levels of these DEGs.…”

“…In one relevant example, the host polysaccharides were hydrolyzed upon P. puparum parasitism to obtain energy for the development of parasitoid offspring [ 15 ]. Similarly, it was further demonstrated that P. vindemiae has a vital role in regulating host glucose metabolism [ 46 ]. These cases provided a possible explanation for the enrichment of purine pentose, glutathione, and other metabolism-related DEGs in KEGG pathways.…”

G6PDH as a key immunometabolic and redox trigger in arthropods

“…The wasp enzyme causes transcriptional inhibition of D. melanogaster G6PDH, leading to increased G6P levels in the host, which can be used as a substrate for wasp development. In RNAi-treated wasps, a lower infectivity capacity is observed when compared to control insects, supporting the idea of immunometabolic interactions involving PPP enzymes ( Yang et al, 2022 ). The findings discussed thus far highlight the promising potential of targeting the immune system and metabolic pathways, particularly PPP, for the development of novel strategies to control arthropods.…”

The Key Role of Fatty Acid Synthase in Lipid Metabolism and Metamorphic Development in a Destructive Insect Pest, Spodoptera litura (Lepidoptera: Noctuidae)

“…Our results suggest that the expression of these genes changes to varying degrees after knocking down SlFAS1 , indicating that these genes may be connected with SlFAS1 to jointly regulate the synthesis of lipids in the body. Yang et al [ 38 ] revealed that the glucose-6-phosphate (G6P) metabolism of the host D. melanogaster parasitized by Pachycrepoideus vindemmiae is affected by PvG6PDH ; the expression levels of the host G6P-metabolism-related genes changed at different time points after the host was injected with PvG6PDH , suggesting the expression of nutrition–related genes can be affected by other genes. In a recent study, Wang et al [ 13 ] also reported that silencing GpylFAS1 affected the expressions of the other fatty acid synthesis-related genes in G. pyloalis .…”