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

The endophagous parasitoid <i>Toxoneuron nigriceps</i> (Viereck) (Hymenoptera, Braconidae) of the larval stages of the tobacco budworm <i>Heliothis virescens</i> (Fabricius) (Lepidoptera, Noctuidae) injects the egg, the venom, the calyx fluid, which includes a Polydnavirus (&...

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Main Authors: Rosanna Salvia, Flora Cozzolino, Carmen Scieuzo, Annalisa Grimaldi, Antonio Franco, S. Bradleigh Vinson, Maria Monti, Patrizia Falabella
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/13/2/144
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author Rosanna Salvia
Flora Cozzolino
Carmen Scieuzo
Annalisa Grimaldi
Antonio Franco
S. Bradleigh Vinson
Maria Monti
Patrizia Falabella
author_facet Rosanna Salvia
Flora Cozzolino
Carmen Scieuzo
Annalisa Grimaldi
Antonio Franco
S. Bradleigh Vinson
Maria Monti
Patrizia Falabella
author_sort Rosanna Salvia
collection DOAJ
description The endophagous parasitoid <i>Toxoneuron nigriceps</i> (Viereck) (Hymenoptera, Braconidae) of the larval stages of the tobacco budworm <i>Heliothis virescens</i> (Fabricius) (Lepidoptera, Noctuidae) injects the egg, the venom, the calyx fluid, which includes a Polydnavirus (<i>T. nigriceps</i> BracoVirus: <i>Tn</i>BV) and the Ovarian Proteins (OPs) into the host body during oviposition. The host metabolism and immune system are disrupted prematurely shortly after parasitization by the combined action of the <i>Tn</i>BV, venom, and OPs. OPs are involved in the early suppression of host immune response, before <i>Tn</i>BV infects and expresses its genes in the host tissues. In this work, we evaluated the effect of HPLC fractions deriving from <i>in toto</i> OPs. Two fractions caused a reduction in hemocyte viability and were subsequently tested to detect changes in hemocyte morphology and functionality. The two fractions provoked severe oxidative stress and actin cytoskeleton disruption, which might explain the high rate of hemocyte mortality, loss of hemocyte functioning, and hence the host’s reduced hemocyte encapsulation ability. Moreover, through a transcriptome and proteomic approach we identify the proteins of the two fractions: eight proteins were identified that might be involved in the observed host hemocyte changes. Our findings will contribute to a better understanding of the secreted ovarian components and their role in parasitoid wasp strategy for evading host immune responses.
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spelling doaj.art-0932015fdc6041a4a746fc70b95ff2512023-11-23T20:26:55ZengMDPI AGInsects2075-44502022-01-0113214410.3390/insects13020144Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune ResponseRosanna Salvia0Flora Cozzolino1Carmen Scieuzo2Annalisa Grimaldi3Antonio Franco4S. Bradleigh Vinson5Maria Monti6Patrizia Falabella7Department of Sciences, University of Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, ItalyDepartment of Chemical Sciences, University of Naples Federico II, 80126 Naples, ItalyDepartment of Sciences, University of Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, ItalyDepartment of Biotechnology and Life Science, University of Insubria, Via J. H. Dunant 3, 21100 Varese, ItalyDepartment of Sciences, University of Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, ItalyDepartment of Entomology, Texas A&M University, 370 Olsen Blvd, College Station, TX 77843, USADepartment of Chemical Sciences, University of Naples Federico II, 80126 Naples, ItalyDepartment of Sciences, University of Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, ItalyThe endophagous parasitoid <i>Toxoneuron nigriceps</i> (Viereck) (Hymenoptera, Braconidae) of the larval stages of the tobacco budworm <i>Heliothis virescens</i> (Fabricius) (Lepidoptera, Noctuidae) injects the egg, the venom, the calyx fluid, which includes a Polydnavirus (<i>T. nigriceps</i> BracoVirus: <i>Tn</i>BV) and the Ovarian Proteins (OPs) into the host body during oviposition. The host metabolism and immune system are disrupted prematurely shortly after parasitization by the combined action of the <i>Tn</i>BV, venom, and OPs. OPs are involved in the early suppression of host immune response, before <i>Tn</i>BV infects and expresses its genes in the host tissues. In this work, we evaluated the effect of HPLC fractions deriving from <i>in toto</i> OPs. Two fractions caused a reduction in hemocyte viability and were subsequently tested to detect changes in hemocyte morphology and functionality. The two fractions provoked severe oxidative stress and actin cytoskeleton disruption, which might explain the high rate of hemocyte mortality, loss of hemocyte functioning, and hence the host’s reduced hemocyte encapsulation ability. Moreover, through a transcriptome and proteomic approach we identify the proteins of the two fractions: eight proteins were identified that might be involved in the observed host hemocyte changes. Our findings will contribute to a better understanding of the secreted ovarian components and their role in parasitoid wasp strategy for evading host immune responses.https://www.mdpi.com/2075-4450/13/2/144ovarian proteinshost-parasitoid interaction<i>Heliothis virescens</i><i>Toxoneuron nigriceps</i>proteomic and transcriptomic approach
spellingShingle Rosanna Salvia
Flora Cozzolino
Carmen Scieuzo
Annalisa Grimaldi
Antonio Franco
S. Bradleigh Vinson
Maria Monti
Patrizia Falabella
Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
Insects
ovarian proteins
host-parasitoid interaction
<i>Heliothis virescens</i>
<i>Toxoneuron nigriceps</i>
proteomic and transcriptomic approach
title Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
title_full Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
title_fullStr Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
title_full_unstemmed Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
title_short Identification and Functional Characterization of <i>Toxoneuron nigriceps</i> Ovarian Proteins Involved in the Early Suppression of Host Immune Response
title_sort identification and functional characterization of i toxoneuron nigriceps i ovarian proteins involved in the early suppression of host immune response
topic ovarian proteins
host-parasitoid interaction
<i>Heliothis virescens</i>
<i>Toxoneuron nigriceps</i>
proteomic and transcriptomic approach
url https://www.mdpi.com/2075-4450/13/2/144
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