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      Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica

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          Abstract

          During natural parasitization, Asobara japonica wasps introduce lateral oviduct (LO) components into their Drosophila hosts soon after the venom injection to neutralize its strong toxicity; otherwise, the host will die. Although the orchestrated relationship between the venom and LO components necessary for successful parasitism has attracted the attention of many researchers in this field, the molecular natures of both factors remain ambiguous. We here showed that precipitation of the venom components by ultracentrifugation yielded a toxic fraction that was inactivated by ultraviolet light irradiation, boiling, and sonication, suggesting that it is a virus-like entity. Morphological observation of the precipitate after ultracentrifugation showed small spherical heterogeneous virus-like particles 20–40 nm in diameter. The venom’s detrimental effect on D. melanogaster larvae was not directly neutralized by the LO components but blocked by a hemolymphal neutralizing factor activated by the LO factor. Furthermore, we found that A. japonica venom and LO components acted similarly on the larvae of the common cutworm Spodoptera litura: the venom injection caused mortality but coinjection of the LO factor protected S. litura larvae from the venom’s toxicity. In contrast, D. ficusphila and D. bipectinata, which are closely related to D. melanogaster but non-habitual host species of A. japonica, were not negatively affected by A. japonica venom due to an intrinsic neutralizing activity in their hemolymph, indicating that these species must have acquired a neutralizer of A. japonica venom during evolution. These results give new insights into the characteristics of both the venom and LO components: A. japonica females have utilized the virus-like toxic venom factor to exploit a wider range of host species after the evolutionary process enabled them to use the LO factor for activation of the host hemolymph neutralizer precursor, although the non-habitual host Drosophila species possess an active intrinsic neutralizer in their hemolymph.

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          Most cited references38

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          The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex.

          Acute bee paralysis virus (ABPV), Kashmir bee virus (KBV) and Israeli acute paralysis virus (IAPV) are part of a complex of closely related viruses from the Family Dicistroviridae. These viruses have a widespread prevalence in honey bee (Apis mellifera) colonies and a predominantly sub-clinical etiology that contrasts sharply with the extremely virulent pathology encountered at elevated titres, either artificially induced or encountered naturally. These viruses are frequently implicated in honey bee colony losses, especially when the colonies are infested with the parasitic mite Varroa destructor. Here we review the historical and recent literature of this virus complex, covering history and origins; the geographic, host and tissue distribution; pathology and transmission; genetics and variation; diagnostics, and discuss these within the context of the molecular and biological similarities and differences between the viruses. We also briefly discuss three recent developments relating specifically to IAPV, concerning its association with Colony Collapse Disorder, treatment of IAPV infection with siRNA and possible honey bee resistance to IAPV. Crown Copyright 2009. Published by Elsevier Inc. All rights reserved.
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            Immunological basis for compatibility in parasitoid-host relationships.

            The insect immune system serves as a key defense against attack by parasitoids. Incompatible hosts often eliminate parasitoids by encapsulation, a process in which hemocytes form a multilayered envelope around the invading organism. Capsule formation involves cooperation between one or more classes of hemocytes and is likely mediated by cytokines and adhesion molecules. Reciprocally, parasitoids have evolved a variety of strategies for overcoming host immune responses. Some parasitoids passively avoid elimination by developing in locations inaccessible to host hemocytes or by possessing surface features that fail to elicit an immune response. Other species actively disrupt the host immune system by injecting specific factors into the host at oviposition. In particular, polydnaviruses associated with several taxa of parasitoids disrupt capsule formation by killing hemocytes or altering their ability to adhere to foreign surfaces. These symbionts have likely played a critical role in evolution of host range and in defining parasitoid-host compatibility.
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              Functional analysis of structural motifs in dicistroviruses.

              The family Dicistroviridae is composed of positive-stranded RNA viruses which have monopartite genomes. These viruses carry genome-linked virus proteins (VPg) and poly (A) tails. The 5' untranslated region (UTR) is approximately 500 nucleotides and contains an internal ribosome entry site (IRES). These features resemble those of vertebrate picornaviruses, but dicistroviruses have other distinct characteristics. Picornaviruses have a single large open reading frame (ORF) encoding the capsid proteins at the 5'-end and the replicases at the 3'-end. In contrast, dicistroviruses have two nonoverlapping ORFs. The 5'-proximal ORF encodes the replicases and the 3'-proximal ORF encodes the capsid proteins. Usually, positive-stranded viruses which have capsid protein genes in the 3' part of the genome produce subgenomic RNA for synthesis of the capsid proteins, because abundant quantities of the capsid proteins are required for the viral replication cycle. In dicistroviruses, translation of the capsid proteins is controlled by an additional IRES. This IRES is located in the intergenic region (IGR) between the replicase and capsid coding regions, and mediates the initiation of translation for the capsid proteins. The IGR-IRES has a multiple stem-loop structure containing three pseudoknots. We describe the characteristics of dicistroviruses, including the RNA elements and viral proteins.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 July 2016
                2016
                : 11
                : 7
                : e0160210
                Affiliations
                [1 ]Department of Applied Biological Sciences, Saga University, Saga 840–8502, Japan
                [2 ]Research and Education Center for Prevention of Global Infectious Diseases of Animals, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183–8509, Japan
                [3 ]Department of Virology II, National Institute of Infectious Diseases, Tokyo, 280–0011, Japan
                Institute of Plant Physiology and Ecology, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: YH SF. Performed the experiments: SF T. Matsumura MH HM YH T. Mizutani NN MK YK TO. Analyzed the data: SF MH HM YH. Contributed reagents/materials/analysis tools: SF MH HM. Wrote the paper: YH.

                Article
                PONE-D-16-12450
                10.1371/journal.pone.0160210
                4965004
                27467595
                fd2593c1-b0cd-4468-81a6-258b5880d859
                © 2016 Furihata et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 27 March 2016
                : 16 July 2016
                Page count
                Figures: 7, Tables: 0, Pages: 14
                Funding
                The authors have no support or funding to report.
                Categories
                Research Article
                Biology and Life Sciences
                Toxicology
                Toxic Agents
                Toxins
                Venoms
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Toxicology
                Toxic Agents
                Toxins
                Venoms
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Larvae
                Research and Analysis Methods
                Model Organisms
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Toxicology
                Toxicity
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Toxicology
                Toxicity
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Research and Analysis Methods
                Separation Processes
                Centrifugation
                Ultracentrifugation
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Custom metadata
                All relevant data are within the paper.

                Uncategorized
                Uncategorized

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