Abstract

Simple SummaryToxoneuron nigriceps is an endoparasitoid of the tobacco budworm Heliothis virescens. Parasitoid strategies to survive involve different regulating factors that are injected into the host body together with the egg: the venom and the calyx fluid, containing a Polydnavirus (PDV) and Ovarian Proteins (OPs). The combination of these factors increases the success of parasitism. Although many studies have been reported on venom protein components and the knowledge on PDVs is increasing, little is known on OPs. These secretions are able to interfere early with the host cellular immune response, acting specifically on host haemocytes, cells involved in immune response. Our results show that OPs induce several alterations on haemocytes, including cellular oxidative stress condition and modifications of actin cytoskeleton, so inducing both a loss of haemocyte functionality and cell death. Overall, in synergy with PDV and venom, OPs positively contribute to the evasion of the host immune response by T. nigriceps.Toxoneuron nigriceps (Viereck) (Hymenoptera, Braconidae) is an endophagous parasitoid of the larval stages of the tobacco budworm, Heliothis virescens (Fabricius) (Lepidoptera, Noctuidae). During oviposition, T. nigriceps injects into the host body, along with the egg, the venom, the calyx fluid, which contains a Polydnavirus (T. nigriceps BracoVirus: TnBV), and the Ovarian Proteins (OPs). Although viral gene expression in the host reaches detectable levels after a few hours, a precocious disruption of the host metabolism and immune system is observed right after parasitization. This alteration appears to be induced by female secretions including TnBV venom and OPs. OPs, originating from the ovarian calyx cells, are involved in the induction of precocious symptoms in the host immune system alteration. It is known that OPs in braconid and ichneumonid wasps can interfere with the cellular immune response before Polydnavirus infects and expresses its genes in the host tissues. Here we show that T. nigriceps OPs induce several alterations on host haemocytes that trigger cell death. The OP injection induces an extensive oxidative stress and a disorganization of actin cytoskeleton and these alterations can explain the high-level of haemocyte mortality, the loss of haemocyte functionality, and so the reduction in encapsulation ability by the host.

Highlights

  • Parasitoid insects have developed in some species a great variety of adaptations in terms of physiological integration which make them similar to parasites, which constitute the most specialized forms of zoophagy [1]

  • The cell viability of haemocytes cultured in the presence of T. nigriceps Ovarian Proteins (OPs) for 24 h did not vary according to their concentration

  • The cell viability percentages equal to 34% and 38% referred to, respectively, samples treated with OPs deriving from 1 or 2 equivalent T. nigriceps females

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Summary

Introduction

Parasitoid insects have developed in some species a great variety of adaptations in terms of physiological integration which make them similar to parasites, which constitute the most specialized forms of zoophagy [1]. Parasitoids develop at the expense of a single victim, the host, killing it [3]. They can be classified by different parameters, such as the number of deposited eggs per host and the parasitization mode [3]. Their host can be an egg, a larva, a pupa or, rarely, adult insects. Parasitoids are generally defined as ectoparasitoids when the juvenile stages feed on the host from the outside of the body and endoparasitoids when the development of the parasitoid takes place inside the host body [4]

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