Apparent replication of an unusual virus-like particle in both a parasitoid wasp and its host

Stoltz, Donald B.; Faulkner, Gary

doi:10.1139/m78-241

Cited by 29 publications

(9 citation statements)

References 9 publications

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“…The electron microscopic studies by Stoltz and co-workers showed that parasitoid viruses are transmitted to host caterpillar tissues (29,31,32). Although viral replication was not observed, virus enters the host cells and is uncoated within the nuclei of these cells (29,31,32). These data corroborate the experimental data from biological studies by showing that parasitoid viruses interact at a cellular level with host cells in some manner which may result in protection of the parasitoid eggs from encapsulation.…”

supporting

confidence: 62%

“…In a separate study of a similar host-parasitoid relationship, purified calyx fluid particles from the parasitoid Nemeritis canescens were shown to prevent encapsulation of the eggs of this parasitoid in the hemocoel of its host, Ephestia kuehniella (3). The electron microscopic studies by Stoltz and co-workers showed that parasitoid viruses are transmitted to host caterpillar tissues (29,31,32). Although viral replication was not observed, virus enters the host cells and is uncoated within the nuclei of these cells (29,31,32).…”

mentioning

confidence: 99%

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Virus with a Multipartite Superhelical DNA Genome from the Ichneumonid Parasitoid Campoletis sonorensis

Krell¹,

Summers²,

Vinson³

1982

J Virol

133

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Virus was isolated from the lumen of the calyx region of ovaries in the parasitoid wasp Campoletis sonorensis (Hymenoptera: Ichneumonidae), and the nature of the viral DNA was analyzed. DNA purified from a homogeneous band of virus contained double-stranded superhelical molecules which were polydisperse in molecular weight. At least 25 different covalently closed circles were present, ranging in molecular weight from 4.0 x 106 to 13.6 x 106. The virus DNA was analyzed with restriction enzymes, and the nature of the genetic complexity was evaluated by Southern blot hybridization of native superhelical and relaxed circular virus DNA and of Salland HindIII-digested DNA. The data suggest that most of the variously sized covalently closed DNAs were composed primarily of nonhomologous sequences. The different size classes of covalently closed viral DNAs did not appear to exist in equimolar concentrations. However, there was no evidence from observation of virus particles in the electron microscope or from virus fractionation experiments that a mixture of viruses was present in the calyx fluid. The results from this study suggest, that the virus isolated from C. sonorensis, like those isolated from other endoparasitic hymenoptera, may belong to a new class of DNA viruses in which the genome is multipartite, with each DNA existing as a superhelical molecule. The virus-like particles which occur in many species of endoparasitic hymenoptera belonging to the superfamily Ichneumonoidea (for a review, see reference 34) (12, 15, 16, 20, 21, 28, 29, 31, 42) are currently classified as subgroup C baculoviruses (18). Virus replication in the female parasitoid is intranuclear and restricted to the nuclei of the calyx (a specialized region of the oviduct) epithelial cells (20, 21, 29, 31, 34). Virus is secreted from the calyx cells and accumulates to a high concentration within the calyx lumen as part of a "calyx fluid." It is injected with the parasitoid egg into host caterpillars during oviposition. Certain experimental evidence indicates that a component of the calyx fluid protects the parasitoid egg from encapsulation within the hemocoel of its habitual host (19, 29-34, 40, 41). A component(s) of the calyx fluid may also be involved in mediating some of the physiological changes that occur in the host after parasitization and which are apparently of some ultimate benefit to the parasitoid (5, 6, 9-11, 14, 38, 39). Vinson and co-workers initially demonstrated that the calyx fluid of Campoletis sonorensis prevents encapsulation of its eggs in its habitual

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supporting

confidence: 62%

mentioning

confidence: 99%

Virus with a Multipartite Superhelical DNA Genome from the Ichneumonid Parasitoid Campoletis sonorensis

Krell¹,

Summers²,

Vinson³

1982

J Virol

133

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“…However, after the discovery of a virus manipulating superparasitism behavior in L. boulardi (Varaldi et al 2003), it appears necessary to go back to those experiments and investigate whether the behavior that has been described could have been manipulated by a microparasite. Indeed, new viruses infecting parasitoid species are regularly discovered (Stoltz and Faulkner 1978;Styer et al 1987;de Buron and Beckage 1992;Stoltz and Makkay 2000;Lawrence 2005;Reineke and Asgari 2005;Stasiak et al 2005), some of which probably benefit from both horizontal and vertical transmission. For instance, a virus showing the same location (the wasps' oviducts) as the one observed in L. boulardi has been recently found in Venturia canescens (Reineke and Asgari 2005), a species that has been extensively used as a model for testing the adaptive nature of superparasitism behavior Hubbard et al 1999;Reineke et al 2004).…”

Section: Discussionmentioning

confidence: 99%

Superparasitism Evolution: Adaptation or Manipulation?

Gandon¹,

Rivero²,

Varaldi³

2006

The American Naturalist

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Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. This often yields intense competition among larvae that are sharing the same host. Why would a female oviposit in such hostile habitat instead of looking for a better quality, unparasitized host? Here we present a continuous-time model of host-parasitoid interaction and discuss alternative scenarios. This model is first used to analyze the evolution of the superparasitism behavior of a solitary proovigenic parasitoid under both time and egg limitation. Then, following the recent discovery by Varaldi et al., we allow the parasitoid to be infected by a virus that alters the superparasitism behavior of its host to enhance its own horizontal transmission. The analysis of the coevolution of this manipulative behavior with the oviposition behavior of uninfected females clarifies and quantifies the conflict that emerges between the parasitoid and its virus. The model also yields new testable predictions. For example, we expect that uninfected parasitoids should superparasite less after coevolving with the manipulative virus. More generally, this model provides a theoretical framework for analyzing the evolution of the manipulation of parasitoid life-history traits by microparasites.

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“…Similarly, ichneumonid wasps produce enveloped spindle-shaped particles classified as ichnoviruses that resemble virions of ascoviruses, viruses lethal to lepidopterans, which, interestingly, are vectored by endoparasitic wasps [15]. It must also be noted that ichnoviruses resemble other true virus particles that are structurally very similar to virions of ascoviruses, but which remain unclassified because the lack of information about their genomes [17][18][19][20][21]. However, ascoviruses and ichnoviruses display very different genome properties; similar genomic differences occur between bracoviruses and baculoviruses or nudiviruses, suggesting that convergent evolution led to the origin the different polydnavirus types from at least two different types of viruses.…”

Section: Introductionmentioning

confidence: 99%

Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis

et al. 2008

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BackgroundFemale endoparasitic ichneumonid wasps inject virus-like particles into their caterpillar hosts to suppress immunity. These particles are classified as ichnovirus virions and resemble ascovirus virions, which are also transmitted by parasitic wasps and attack caterpillars. Ascoviruses replicate DNA and produce virions. Polydnavirus DNA consists of wasp DNA replicated by the wasp from its genome, which also directs particle synthesis. Structural similarities between ascovirus and ichnovirus particles and the biology of their transmission suggest that ichnoviruses evolved from ascoviruses, although molecular evidence for this hypothesis is lacking.ResultsHere we show that a family of unique pox-D5 NTPase proteins in the Glypta fumiferanae ichnovirus are related to three Diadromus pulchellus ascovirus proteins encoded by ORFs 90, 91 and 93. A new alignment technique also shows that two proteins from a related ichnovirus are orthologs of other ascovirus virion proteins.ConclusionOur results provide molecular evidence supporting the origin of ichnoviruses from ascoviruses by lateral transfer of ascoviral genes into ichneumonid wasp genomes, perhaps the first example of symbiogenesis between large DNA viruses and eukaryotic organisms. We also discuss the limits of this evidence through complementary studies, which revealed that passive lateral transfer of viral genes among polydnaviral, bacterial, and wasp genomes may have occurred repeatedly through an intimate coupling of both recombination and replication of viral genomes during evolution. The impact of passive lateral transfers on evolutionary relationships between polydnaviruses and viruses with large double-stranded genomes is considered in the context of the theory of symbiogenesis.

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Apparent replication of an unusual virus-like particle in both a parasitoid wasp and its host

Cited by 29 publications

References 9 publications

Virus with a Multipartite Superhelical DNA Genome from the Ichneumonid Parasitoid Campoletis sonorensis

Virus with a Multipartite Superhelical DNA Genome from the Ichneumonid Parasitoid Campoletis sonorensis

Superparasitism Evolution: Adaptation or Manipulation?

Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis

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