Abstract

The pupal ectoparasitoid Pachycrepoideus vindemiae injects venom into its fly hosts prior to oviposition. We have shown that this venom causes immune suppression in Drosophila melanogaster pupa but the mechanism involved remained unclear. Here, we show using transgenic D. melanogaster with fluorescent hemocytes that the in vivo number of plasmatocytes and lamellocytes decreases after envenomation while it has a limited effect on crystal cells. After in vitro incubation with venom, the cytoskeleton of plasmatocytes underwent rearrangement with actin aggregation around the internal vacuoles, which increased with incubation time and venom concentration. The venom also decreased the lamellocytes adhesion capacity and induced nucleus fragmentation. Electron microscopy observation revealed that the shape of the nucleus and mitochondria became irregular after in vivo incubation with venom and confirmed the increased vacuolization with the formation of autophagosomes-like structures. Almost all venom-treated hemocytes became positive for TUNEL assays, indicating massive induced apoptosis. In support, the caspase inhibitor Z-VAD-FMK attenuated the venom-induced morphological changes suggesting an involvement of caspases. Our data indicate that P. vindemiae venom inhibits D. melanogaster host immunity by inducing strong apoptosis in hemocytes. These assays will help identify the individual venom component(s) responsible and the precise mechanism(s)/pathway(s) involved.

Highlights

  • Female parasitoid wasps oviposit in or on a host, their eggs developing using the host as a food source and the host eventually dying as a result of the parasitoid’s development

  • The injection of purified virus like-particles (VLPs) from Meteorus pulchricornis into the larva of its host moth Pseudaletia separata led to rapid disassembly of the leading edge of filopodia and lamellipodia into the host granular cells, a kind of phagocytic cells and the parasitism as well as the injection of VLPs induced apoptosis of the host hemocytes [11,12]. Both the injection of PDVs from Microplitis demolitor into the hemocoele of Pseudoplusia includens larvae and the in vitro incubation with hemocytes induced apoptosis and chromatin condensation in the granular cells of the host [13]. It appeared that the injection of purified venosomes from Leptopilina species, endoparasitoids of Drosophila, selectively induced shape changes/death of the lamellocytes, the hemocyte type specialized in the encapsulation of parasitoid eggs and contributed to the success of parasitism [14,15,16]

  • The in vitro incubation of hemocytes with crude venom reveals the alterations it induces in the morphology and ultrastructure hemocytes with crude venom reveals the alterations it induces in the morphology and ultrastructure of bot h the plasmatocytes and lamellocytes, eventually leading to cell death

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Summary

Introduction

Female parasitoid wasps oviposit in or on a host, their eggs developing using the host as a food source and the host eventually dying as a result of the parasitoid’s development. Parasitoid wasps are natural enemies of many insects, including agricultural pests and are used as biological control agents Most of these wasps inject venom into their host prior or during oviposition, which contains various factors necessary to regulate the host physiology for the successful development of Insects 2020, 11, 363; doi:10.3390/insects11060363 www.mdpi.com/journal/insects. The injection of purified VLPs from Meteorus pulchricornis into the larva of its host moth Pseudaletia separata led to rapid disassembly of the leading edge of filopodia and lamellipodia into the host granular cells, a kind of phagocytic cells and the parasitism as well as the injection of VLPs induced apoptosis of the host hemocytes [11,12]. It appeared that the injection of purified venosomes from Leptopilina species, endoparasitoids of Drosophila, selectively induced shape changes/death of the lamellocytes, the hemocyte type specialized in the encapsulation of parasitoid eggs and contributed to the success of parasitism [14,15,16]

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