Role of Ovarian Proteins Secreted by Toxoneuron nigriceps (Viereck) (Hymenoptera, Braconidae) in the Early Suppression of Host Immune Response

Abstract

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.

Effects of Envenomation on Survival and Development of the Host-Parasitoid System of Galleria mellonella (Lepidoptera: Pyralidae) and Bracon hebetor (Hymenoptera: Braconidae)

“…Different studies reveal that reproductive secretions. e.g., venom (Wago and Kitano, 1985) and ovarian proteins (Webb and Luckhart, 1994) inserted by parasitizing females can disrupt cytoskeleton of the host hemocytes resulting in reduced cellular immunity (Salvia et al, 2021). The ectoparasitoid's venom primarily arrests development of the host through paralysis or by inhibiting host ecdysis (Beard, 1952(Beard, , 1978Shaw, 1981;Pike et al, 1982;Visser et al, 1983;Piek and Spanjer, 1986;Coudron et al, 1990;Coudron, 1991;Rivers et al,1993;Rivers and Denlinger, 1994), followed by prevention of the parasitic wasp progeny from being disrupted throughout development.…”

Effects of Varying Temperature on the Reproduction and Survival of Mealybug Parasitoid, Aenasius Arizonensis (Hymenoptera: Encyrtidae)

“…Parasitoids are generally divided into 2 groups i.e., ecto-and endoparasitoids: ectoparasitoids lay their eggs on external surface/skin of the host body while endoparasitoids insert their eggs to the interior of the host (Asgari and Rivers, 2011). Ectoparasitoids are able to parasitize the victim thanks to their venom (Scieuzo et al, 2021) while Hymenopteran endoparasitoids have combined strategies of parasitization, induced by female secretions (venom and ovarian protein and sometimes polydnaviruses) (Varricchio et al, 1999;Malva et al, 2004;Laurino et al, 2016;Salvia et al, 2021) Aenasius arizonensis (Girault) (Hymenoptera: Encyrtidae) is an important solitary nymphal endoparasitic wasp of P. solenopsis in India (Hayat, 2009), Pakistan (Mahmood, 2008), China (Chen et al, 2010), Iran (Abdin et al, 2012) and Australia (Khan et al, 2012). It is a key mortality factor of mealybugs under field conditions (Ram et.al., 2009).…”

Identification and Functional Characterization of Toxoneuron nigriceps Ovarian Proteins Involved in the Early Suppression of Host Immune Response

“…The proteins of the ovarian calyx are synthesized in the female reproductive system of the parasitoid and injected into the hemocelic cavity of the host upon oviposition [18]. These proteins play an important role in the success of parasitization and persist in the plasma of parasitized insects, in continuous contact with circulating hemocytes, up to 96 h after oviposition [19,20]. These proteins inhibit the encapsulation process, i.e., the ability of hemocytes to form a multilayered capsule around a foreign body (such as the parasitoid egg) which is eliminated through the action of toxic substances produced by the capsule itself, including melanin [21,22].…”