Ichnovirus

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Bruce A. Webb - One of the best experts on this subject based on the ideXlab platform.

  • genes as members of the repeat element gene family
    2016
    Co-Authors: Roland Hilgarth, Bruce A. Webb, S. Hilgarth
    Abstract:

    Ichnovirus segment I genes as members of the repeat element gene famil

  • 2002. Characterization of Campoletis sonorensis Ichnovirus segment I genes Int
    2016
    Co-Authors: S. Hilgarth, Bruce A. Webb
    Abstract:

    Campoletis sonorensis Ichnovirus (CsIV) is a symbiotic virus associated with the endoparasitic wasp C. sonorensis. The virus is injected into the wasp’s host, Heliothis virescens, during oviposition. One CsIV gene has been identified as a repeat element (rep) gene and encodes a ubiquitous imperfectly conserved 540 bp sequence. We report the sequencing and mapping of a rep-containing segment, segment I, that hybridizes to a known rep sequence from segment O1. Analysis of this 8–6 kbp segment identified three ORFs having high similarity to the 540 bp rep sequence. All three rep sequence ORFs were expressed in parasitized H. virescens as well as in C. sonorensis tissues. Two of these rep genes, I 0.9 and I 1.1, have single copies of the 540 bp repeat sequence, while the third rep gene, I 1.2, has two imperfect copies, which are more similar to each other than to sequences on the segment I single-motif genes. Like the CsIV BHv 0.9 rep gene, the segment I rep genes lack introns and a signal peptide, suggesting that they are not secreted. Based on their similarity in nucleotide sequence, predicted amino acid sequence and gene structure, the three segment I repeat-containing genes, I 0.9, I 1.1 and I 1.2, are new members of the rep gene family

  • Specificities of Ichnoviruses associated with campoplegine wasps: genome, genes and role in host–parasitoid interaction
    Current Opinion in Insect Science, 2014
    Co-Authors: Tristan Doremus, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Marie Frayssinet, Bruce A. Webb, Michel Cusson, Don B. Stoltz, Anne Nathalie Volkoff
    Abstract:

    Ichnoviruses (IVs), unique symbiotic viruses carried by ichneumonid campoplegine wasps, derive from integration of a paleo-Ichnovirus into an ancestral wasp genome. The modern ‘genome’ is composed of both regions that are amplified, circularized and encapsidated into viral particles and non-encapsidated viral genomic regions involved in particle morphogenesis. Packaged genomes include multiple circular dsDNAs encoding many genes mostly organized in gene families. Virus particles are assembled in specialized ovarian cells from which they exit into the oviduct lumen; mature virions are injected during oviposition into the insect host. Expression of viral proteins in infected cells correlates with physiological alterations of the host enabling success of parasitism.

  • analysis of gene transcription and relative abundance of the cys motif gene family from campoletis sonorensis Ichnovirus csiv and further characterization of the most abundant cys motif protein whv1 6
    Insect Molecular Biology, 2013
    Co-Authors: Torrence A Gill, Bruce A. Webb
    Abstract:

    The cys-motif gene family associated with Campoletis sonorensis Ichnovirus contains 10 members, WHv1.6, WHv1.0, VHv1.1, VHv1.4, AHv1.0, A'Hv0.8, FHv1.4, LHv2.8, UHv0.8, and UHv0.8a. The results of this study indicated that, within the encapsidated virion, WHv1.6 is the most abundant cys-motif gene, while the combined AHv genes are the least abundant. During parasitization of Heliothis virescens by Campoletis sonorenis, WHv1.6 transcripts were the mostly highly expressed, while the combined UHv genes had the lowest expression. Further proteomic analysis of WHv1.6 showed that it accumulates at high levels in parasitized plasma by 6 h, and is detectable in the haemocytes, fat body, malpighian tubules, nerve cord and epidermis by 2 days after parasitization. Localization experiments led us to conclude that WHv1.6 interacts with the cell membrane along with other organelles within a virus-infected cell and prevents immunocytes from spreading or adhering to a foreign surface. Similarly to VHv1.4 and VHv1.1, WHv1.6 is able to inhibit the translation of haemocyte and Malpighian tubule RNAs. Our results showed that the expression of cys-motif genes during parasitization is related to the gene copy number of each gene within the encapsidated virion and may also be dependent upon cis-regulatory element activity in different target tissues. In addition, WHv1.6 plays a major role in inhibiting the cellular encapsulation response by H. virescens.

  • the campoletis sonorensis Ichnovirus vankyrin protein p vank 1 inhibits apoptosis in insect sf9 cells
    Insect Molecular Biology, 2009
    Co-Authors: Angelika Fathgoodin, Jeremy A Kroemer, Bruce A. Webb
    Abstract:

    : The Campoletis sonorensis Ichnovirus (CsIV) vankyrin genes encode proteins containing truncated ankyrin repeat domains with sequence homology to the inhibitory domains of NF-kappaB transcription factor inhibitors, IkappaBs. The CsIV vankyrin proteins are thought to be involved in the suppression of NF-kappaB activity during immune response and/or developmental events in the parasitized host. Here we report that when P-vank-1 was expressed stably from Sf9 cells, prolonged survival of these cells was observed after baculovirus infection, UV irradiation, and treatment with the apoptosis-inducing chemical camptothecin compared to untransformed Sf9 cells. Furthermore, P-vank-1 inhibited nuclear and internucleosomal degradation and caspase activity after induction of apoptosis in Sf9 cells stably expressing P-vank-1. This is the first report of a polydnavirus protein with anti-apoptotic function.

Anne Nathalie Volkoff - One of the best experts on this subject based on the ideXlab platform.

  • Les Polydnavirus, un exemple unique de machinerie virale domestiquée par des insectes parasitoïdes.
    Virologie (Montrouge France), 2020
    Co-Authors: Ange Lorenzi, Anne Nathalie Volkoff
    Abstract:

    Polydnaviruses are unique mutualistic viruses associated with thousands of parasitoid wasps. They are characterized by a segmented packaged DNA genome and are necessary for parasitic success. Virus particles are produced in the wasp ovaries from a set of "viral" sequences integrated into the wasp genome. The polydnavirus/wasp associations as observed today result from the integration of a viral genomes into the wasp genome during evolution. Recent years have been marked by the discovery of the viral ancestors of the two known types of polydnavirus, bracovirus and Ichnovirus, which has helped to shed some light on the evolution of the symbiosis. Some of the viral genes have been conserved in the genome of the parasitoid, allowing the latter to produce non-replicative viral particles, that contain DNA molecules encoding essentially "virulence" genes, probably of insect origin. Thus polydnaviruses can be considered as endogenous viral elements (EVE) that have been domesticated by the wasp to become a "weapon" allowing its survival.

  • Les Polydnavirus, un exemple unique de machinerie virale domestiquée par des insectes parasitoïdes.
    Virologie, 2020
    Co-Authors: Ange Lorenzi, Anne Nathalie Volkoff
    Abstract:

    Les Polydnavirus illustrent un exemple unique d’interactions symbiotiques entre un virus et un organisme eucaryote. Ces sont des mutualistes obligatoires, associés à de nombreuses espèces d’hyménoptères parasitoïdes. Ils sont caractérisés par un génome encapsidé constitué de plusieurs molécules d’ADN et sont nécessaires à la réussite parasitaire. Les particules virales sont produites dans les ovaires à partir d’un corpus de séquences « virales » intégrées au génome de la guêpe. Les associations polydnavirus/guêpe telles qu’observées aujourd’hui résultent d’événements d’intégration de génomes viraux dans le génome des guêpes survenus au cours de l’évolution. Ces dernières années ont été marquées par la découverte des ancêtres viraux des deux types de Polydnavirus connus, les Bracovirus et les Ichnovirus, ce qui a permis d’éclairer en partie l’évolution de la symbiose. Une partie des gènes viraux a été conservée dans le génome du parasitoïde, permettant à ce dernier de produire des particules virales non réplicatives, car contenant un génome constitué essentiellement de gènes dits de « virulence », probablement d’origine insecte. Les Polydnavirus peuvent être considérés comme des éléments endogènes viraux (EVE) qui ont été domestiqués par la guêpe pour devenir au fil du temps une « arme » garantissant sa survie.

  • Decoding morphogenesis of Ichnovirus associated to the parasitic wasp H. didymator by RNA interference
    2019
    Co-Authors: Ange Lorenzi, Marc Ravallec, Véronique Jouan, Magali Eychenne, Anne Nathalie Volkoff
    Abstract:

    Decoding morphogenesis of Ichnovirus associated to the parasitic wasp [i]H. didymator[/i] by RNA interference. SIP/IOBC

  • The dual life of Ichnoviruses
    Current Opinion in Insect Science, 2019
    Co-Authors: Isabelle Darboux, Michel Cusson, Anne Nathalie Volkoff
    Abstract:

    Ichnoviruses (IVs) are mutualistic, double-stranded DNA viruses playing a key role in the successful parasitism of thousands of endoparasitoid wasp species. IV particles are produced exclusively in the female wasp reproductive tract. They are co-injected along with the parasitoid egg into caterpillar hosts upon parasitization. The expression of viral genes by infected host cells leads to an immunosuppressive state and delayed development of the host, two pathologies that are critical to the successful development of the wasp egg and larva. Ichnovirus is one of the two recognized genera within the family Polydnaviridae (polydnaviruses or PDVs), the other genus being Bracovirus (BV), associated with braconid wasps. IVs are associated with ichneumonid wasps belonging to the subfamilies Campopleginae and Banchinae; attempts to identify IV particles in other ichneumonid subfamilies have so far been unsuccessful. Functional studies targeting IV genes expressed in parasitized hosts, along with investigations of the molecular mechanisms responsible for viral morphogenesis in the female wasp, have resulted in a better understanding of the biology of these atypical viruses.

  • Evidence for an Ichnovirus machinery in parasitoids of coleopteran larvae
    Virus Research, 2019
    Co-Authors: Stéphanie Robin, Marc Ravallec, Véronique Jouan, Marie Frayssinet, Fabrice Legeai, James Whitfield, Anne Nathalie Volkoff
    Abstract:

    Bathyplectes spp. are ichneumonid solitary larval parasitoids of the alfalfa weevil which have been classified in the subfamily Campopleginae and which harbor atypical virus particles. Despite the morphological differences between Bathyplectes spp. particles and the polydnaviruses carried by a number of related campoplegine species, called Ichnoviruses, the process by which they are produced is very similar to that of Ichnoviruses. To address the question of the nature and origin of these atypical particles, the Bathyplectes anurus ovary transcriptome has been analyzed. We found a number of highly expressed transcripts displaying similarities with genes belonging to the machinery involved in the production of Ichnovirus particles. In addition, transcripts with similarities with repeat-element genes, which are characteristic of the packaged campoplegine Ichnovirus genome were identified. Altogether, our results provide evidence that Bathyplectes particles are related to Ichnoviruses.

Michel Cusson - One of the best experts on this subject based on the ideXlab platform.

  • The dual life of Ichnoviruses
    Current Opinion in Insect Science, 2019
    Co-Authors: Isabelle Darboux, Michel Cusson, Anne Nathalie Volkoff
    Abstract:

    Ichnoviruses (IVs) are mutualistic, double-stranded DNA viruses playing a key role in the successful parasitism of thousands of endoparasitoid wasp species. IV particles are produced exclusively in the female wasp reproductive tract. They are co-injected along with the parasitoid egg into caterpillar hosts upon parasitization. The expression of viral genes by infected host cells leads to an immunosuppressive state and delayed development of the host, two pathologies that are critical to the successful development of the wasp egg and larva. Ichnovirus is one of the two recognized genera within the family Polydnaviridae (polydnaviruses or PDVs), the other genus being Bracovirus (BV), associated with braconid wasps. IVs are associated with ichneumonid wasps belonging to the subfamilies Campopleginae and Banchinae; attempts to identify IV particles in other ichneumonid subfamilies have so far been unsuccessful. Functional studies targeting IV genes expressed in parasitized hosts, along with investigations of the molecular mechanisms responsible for viral morphogenesis in the female wasp, have resulted in a better understanding of the biology of these atypical viruses.

  • Specificities of Ichnoviruses associated with campoplegine wasps: genome, genes and role in host–parasitoid interaction
    Current Opinion in Insect Science, 2014
    Co-Authors: Tristan Doremus, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Marie Frayssinet, Bruce A. Webb, Michel Cusson, Don B. Stoltz, Anne Nathalie Volkoff
    Abstract:

    Ichnoviruses (IVs), unique symbiotic viruses carried by ichneumonid campoplegine wasps, derive from integration of a paleo-Ichnovirus into an ancestral wasp genome. The modern ‘genome’ is composed of both regions that are amplified, circularized and encapsidated into viral particles and non-encapsidated viral genomic regions involved in particle morphogenesis. Packaged genomes include multiple circular dsDNAs encoding many genes mostly organized in gene families. Virus particles are assembled in specialized ovarian cells from which they exit into the oviduct lumen; mature virions are injected during oviposition into the insect host. Expression of viral proteins in infected cells correlates with physiological alterations of the host enabling success of parasitism.

  • Ultrastructural and genomic characterization of a second banchine polydnavirus confirms the existence of shared features within this Ichnovirus lineage.
    Journal of General Virology, 2013
    Co-Authors: Abdelmadjid Djoumad, Don Stoltz, Catherine Béliveau, Brian Boyle, Lisa Kuhn, Michel Cusson
    Abstract:

    Polydnaviruses (PDVs) are symbiotic viruses carried by endoparasitic wasps and transmitted to caterpillar hosts during parasitization. Although they share several features, including a segmented dsDNA genome, a unique life cycle where replication is restricted to the wasp host, and immunodepressive/developmental effects on the caterpillar host, PDVs carried by ichneumonid and braconid wasps (referred to as Ichnoviruses and bracoviruses, respectively) have different evolutionary origins. In addition, Ichnoviruses (IVs) form two distinct lineages, with viral entities found in wasps belonging to the subfamilies Campopleginae and Banchinae displaying strikingly different virion morphologies and genomic features. However, the current description for banchine IVs is based on the characterization of a single species, namely that of the Glypta fumiferanae IV (GfIV). Here we provide an ultrastructural and genomic analysis of a second banchine IV isolated from the wasp Apophua simplicipes, and we show that this virus shares many features with GfIV, including a multi-nucleocapsid virion, an aggregate genome size of ~300 kb, genome segments

  • ultrastructural and genomic characterization of a second banchine polydnavirus confirms the existence of shared features within this Ichnovirus lineage
    Journal of General Virology, 2013
    Co-Authors: Michel Cusson, Don Stoltz, Catherine Béliveau, Abdelmadjid Djoumad, Brian Boyle, Lisa Kuhn
    Abstract:

    Polydnaviruses (PDVs) are symbiotic viruses carried by endoparasitic wasps and transmitted to caterpillar hosts during parasitization. Although they share several features, including a segmented dsDNA genome, a unique life cycle where replication is restricted to the wasp host, and immunodepressive/developmental effects on the caterpillar host, PDVs carried by ichneumonid and braconid wasps (referred to as Ichnoviruses and bracoviruses, respectively) have different evolutionary origins. In addition, Ichnoviruses (IVs) form two distinct lineages, with viral entities found in wasps belonging to the subfamilies Campopleginae and Banchinae displaying strikingly different virion morphologies and genomic features. However, the current description for banchine IVs is based on the characterization of a single species, namely that of the Glypta fumiferanae IV (GfIV). Here we provide an ultrastructural and genomic analysis of a second banchine IV isolated from the wasp Apophua simplicipes, and we show that this virus shares many features with GfIV, including a multi-nucleocapsid virion, an aggregate genome size of ~300 kb, genome segments <5 kb, an impressively high degree of genome segmentation and a very similar gene content (same gene families in both viruses). Altogether, the data presented here confirm the existence of shared characteristics within this banchine IV lineage.

  • Characterization of the polydnaviral 'T. rostrale virus' (TrV) gene family: TrV1 expression inhibits in vitro cell proliferation.
    The Journal of general virology, 2013
    Co-Authors: Abdelmadjid Djoumad, Frédéric Dallaire, Christopher J Lucarotti, Michel Cusson
    Abstract:

    Tranosema rostrale Ichnovirus (TrIV) is a polydnavirus (PDV) transmitted by the endoparasitic wasp T. rostrale to its host Choristoneura fumiferana during oviposition. PDV genes are expressed in infected caterpillars, causing physiological disturbances that promote the survival of the developing endoparasite. The previously sequenced genome of TrIV contains ~86 genes organized in multigene families and distributed on multiple segments of circular dsDNA. Among these, the 'T. rostrale virus' (TrV) family comprises seven genes that are absent in other PDV genomes examined to date and whose function(s) remain(s) unknown. Here, we initiated a functional analysis of the TrV family using qPCR, transfection and RNAi approaches. TrV family genes were weakly expressed in wasp ovaries, but some displayed high transcript abundance in parasitized caterpillars. Whilst TrV1 was the most highly transcribed TrV gene in infected caterpillars, transcript levels for TrV5 and TrV6 were nearly undetectable, indicating that they may be pseudogenes. Temporal and tissue-specific patterns of transcript abundance were similar for all expressed TrV family genes, indicative of an apparent lack of difference in function or tissue specificity. Infection of Cf-203 and Sf-21 insect cells with TrIV led to a dose-dependent inhibition of cell proliferation with no sign of apoptosis. Whilst similar inhibition was observed following transfection of cells with a cloned genome segment carrying the TrV1 gene, RNA interference targeting TrV1 largely restored cell growth in TrIV-infected cells, indicating that TrV1 expression was responsible for the observed inhibition. We suggest that TrV genes may contribute to host developmental disruption by interfering with host-cell proliferation during parasitism.

Marc Ravallec - One of the best experts on this subject based on the ideXlab platform.

  • Genomic architecture of endogenous Ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps
    BMC Biology, 2020
    Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Jean-michel Drezen, Stéphanie Robin, Bernardo Santos, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Denis Tagu
    Abstract:

    Background Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. PDVs include the Ichnoviruses and bracoviruses that originate from independent viral acquisitions in ichneumonid and braconid wasps respectively. PDV genomes are fully incorporated into the wasp genomes and consist of (1) genes involved in viral particle production, which derive from the viral ancestor and are not encapsidated, and (2) proviral segments harboring virulence genes, which are packaged into the viral particle. To help elucidating the mechanisms that have facilitated viral domestication in ichneumonid wasps, we analyzed the structure of the viral insertions by sequencing the whole genome of two Ichnovirus-carrying wasp species,Hyposoter didymatorandCampoletis sonorensis. Results Assemblies with long scaffold sizes allowed us to unravel the organization of the endogenous Ichnovirus and revealed considerable dispersion of the viral loci within the wasp genomes. Proviral segments contained species-specific sets of genes and occupied distinct genomic locations in the two ichneumonid wasps. In contrast, viral machinery genes were organized in clusters showing highly conserved gene content and order, with some loci located in collinear wasp genomic regions. This genomic architecture clearly differs from the organization of PDVs in braconid wasps, in which proviral segments are clustered and viral machinery elements are more dispersed. Conclusions The contrasting structures of the two types of Ichnovirus genomic elements are consistent with their different functions: proviral segments are vehicles for virulence proteins expected to adapt according to different host defense systems, whereas the genes involved in virus particle production in the wasp are likely more stable and may reflect ancestral viral architecture. The distinct genomic architectures seen in Ichnoviruses versus bracoviruses reveal different evolutionary trajectories that have led to virus domestication in the two wasp lineages.

  • RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps.
    PLoS pathogens, 2019
    Co-Authors: Ange Lorenzi, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don Stoltz
    Abstract:

    There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called Ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a 'virulence gene delivery vehicle' that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals.

  • Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps
    2019
    Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Jean-michel Drezen, Stéphanie Robin, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Bernardo F. Santos, Denis Tagu
    Abstract:

    Polydnaviruses (PDVs) are mutualistic endogenous viruses associated with some lineages of parasitoid wasps that allow successful development of the wasps within their hosts. PDVs include two taxa resulting from independent virus acquisitions in braconid (bracoviruses) and ichneumonid wasps (Ichnoviruses). PDV genomes are fully incorporated into the wasp genomes and comprise (1) virulence genes located on proviral segments that are packaged into the viral particle, and (2) genes involved in the production of the viral particles, which are not encapsidated. Whereas the genomic organization of bracoviruses within the wasp genome is relatively well known, the architecture of endogenous Ichnoviruses remains poorly understood. We sequenced the genome of two Ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Complete assemblies with long scaffold sizes allowed identification of the integrated Ichnovirus, highlighting an extreme dispersion within the wasp genomes of the viral loci, i.e. isolated proviral segments and clusters of replication genes. Comparing the two wasp species, proviral segments harbor distinct gene content and variable genomic environment, whereas viral machinery clusters show conserved gene content and order, and can be inserted in collinear wasp genomic regions. This distinct architecture is consistent with the biological properties of the two viral elements: proviral segments producing virulence proteins allowing parasitism success are fine-tuned to the host physiology, while an ancestral viral architecture was likely maintained for the genes involved in virus particle production. Finding a distinct genomic architecture of Ichnoviruses and bracoviruses highlights different evolutionary trajectories leading to virus domestication in the two wasp lineages.

  • Decoding morphogenesis of Ichnovirus associated to the parasitic wasp H. didymator by RNA interference
    2019
    Co-Authors: Ange Lorenzi, Marc Ravallec, Véronique Jouan, Magali Eychenne, Anne Nathalie Volkoff
    Abstract:

    Decoding morphogenesis of Ichnovirus associated to the parasitic wasp [i]H. didymator[/i] by RNA interference. SIP/IOBC

  • RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps
    PLoS Pathogens, 2019
    Co-Authors: Ange Lorenzi, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don Stoltz
    Abstract:

    There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called Ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a 'virulence gene delivery vehicle' that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals. Author summary Thousands of parasitic wasp from the ichneumonid family rely on virus-derived particles, named Ichnoviruses (Polydnavirus family), to ensure their successful development. The particles are produced in a specialized ovarian tissue of the female wasp named calyx. Virions are assembled in the calyx cell nuclei and stored in the oviduct before being transferred to the parasitoid host upon female wasp oviposition. Genes encoding proteins associated with the particles had been previously identified. These genes are localized in clusters of genes in the wasp genome (named IVSPER for "Ichnovirus structural proteins encoding regions"), they are specifically transcribed in the calyx but not encapsidated. IVSPER genes were thus hypothesized to derive from the integration of a virus, however still undetermined. Indeed, none of the identified genes had similarity to known sequence, making in addition unclear their function in particle production. In this work, we use the RNA interference technology to decipher the function of six IVSPER genes from the ichneumonid wasp Hyposoter didymator. Thanks to this approach, combined with transmission electron microscopy, we show that the studied IVSPER genes are required in different steps of particle morphogenesis and trafficking, and that their functions are those expected of a typical virus.

Don Stoltz - One of the best experts on this subject based on the ideXlab platform.

  • RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps.
    PLoS pathogens, 2019
    Co-Authors: Ange Lorenzi, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don Stoltz
    Abstract:

    There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called Ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a 'virulence gene delivery vehicle' that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals.

  • RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps
    PLoS Pathogens, 2019
    Co-Authors: Ange Lorenzi, Isabelle Darboux, Marc Ravallec, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don Stoltz
    Abstract:

    There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called Ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a 'virulence gene delivery vehicle' that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals. Author summary Thousands of parasitic wasp from the ichneumonid family rely on virus-derived particles, named Ichnoviruses (Polydnavirus family), to ensure their successful development. The particles are produced in a specialized ovarian tissue of the female wasp named calyx. Virions are assembled in the calyx cell nuclei and stored in the oviduct before being transferred to the parasitoid host upon female wasp oviposition. Genes encoding proteins associated with the particles had been previously identified. These genes are localized in clusters of genes in the wasp genome (named IVSPER for "Ichnovirus structural proteins encoding regions"), they are specifically transcribed in the calyx but not encapsidated. IVSPER genes were thus hypothesized to derive from the integration of a virus, however still undetermined. Indeed, none of the identified genes had similarity to known sequence, making in addition unclear their function in particle production. In this work, we use the RNA interference technology to decipher the function of six IVSPER genes from the ichneumonid wasp Hyposoter didymator. Thanks to this approach, combined with transmission electron microscopy, we show that the studied IVSPER genes are required in different steps of particle morphogenesis and trafficking, and that their functions are those expected of a typical virus.

  • Genomic and proteomic analyses indicate that banchine and campoplegine polydnaviruses have similar, if not identical, viral ancestors
    Journal of Virology, 2015
    Co-Authors: Catherine Béliveau, Anne Nathalie Volkoff, Georges Periquet, Don Stoltz, Brian Boyle, Lisa Kuhn, Cohen Alejandro, Stewart Don, Djoumad Abdelmadjid, Elisabeth A. Herniou
    Abstract:

    Polydnaviruses form a group of unconventional double-stranded DNA (dsDNA) viruses transmitted by endoparasitic wasps during egg laying into caterpillar hosts, where viral gene expression is essential to immature wasp survival. A copy of the viral genome is present in wasp chromosomes, thus ensuring vertical transmission. Polydnaviruses comprise two taxa, Bracovirus and Ichnovirus, shown to have distinct viral ancestors whose genomes were "captured" by ancestral wasps. While evidence indicates that bracoviruses derive from a nudivirus ancestor, the identity of the Ichnovirus progenitor remains unknown. In addition, Ichnoviruses are found in two ichneumonid wasp subfamilies, Campopleginae and Banchinae, where they constitute morphologically and genomically different virus types. To address the question of whether these two Ichnovirus subgroups have distinct ancestors, we used genomic, proteomic, and transcriptomic analyses to characterize particle proteins of the banchine Glypta fumiferanae Ichnovirus and the genes encoding them. Several proteins were found to be homologous to those identified earlier for campoplegine Ichnoviruses while the corresponding genes were located in clusters of the wasp genome similar to those observed previously in a campoplegine wasp. However, for the first time in a polydnavirus system, these clusters also revealed sequences encoding enzymes presumed to form the replicative machinery of the progenitor virus and observed to be overexpressed in the virogenic tissue. Homology searches pointed to nucleocytoplasmic large DNA viruses as the likely source of these genes. These data, along with an analysis of the chromosomal form of five viral genome segments, provide clear evidence for the relatedness of the banchine and campoplegine Ichnovirus ancestors.

  • Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if not Identical, Viral Ancestors
    Journal of virology, 2015
    Co-Authors: Catherine Béliveau, Anne Nathalie Volkoff, Georges Periquet, Don Stoltz, Abdelmadjid Djoumad, Brian Boyle, Lisa Kuhn, Alejandro Cohen, Don Stewart, Elisabeth A. Herniou
    Abstract:

    ABSTRACT Polydnaviruses form a group of unconventional double-stranded DNA (dsDNA) viruses transmitted by endoparasitic wasps during egg laying into caterpillar hosts, where viral gene expression is essential to immature wasp survival. A copy of the viral genome is present in wasp chromosomes, thus ensuring vertical transmission. Polydnaviruses comprise two taxa, Bracovirus and Ichnovirus, shown to have distinct viral ancestors whose genomes were “captured” by ancestral wasps. While evidence indicates that bracoviruses derive from a nudivirus ancestor, the identity of the Ichnovirus progenitor remains unknown. In addition, Ichnoviruses are found in two ichneumonid wasp subfamilies, Campopleginae and Banchinae, where they constitute morphologically and genomically different virus types. To address the question of whether these two Ichnovirus subgroups have distinct ancestors, we used genomic, proteomic, and transcriptomic analyses to characterize particle proteins of the banchine Glypta fumiferanae Ichnovirus and the genes encoding them. Several proteins were found to be homologous to those identified earlier for campoplegine Ichnoviruses while the corresponding genes were located in clusters of the wasp genome similar to those observed previously in a campoplegine wasp. However, for the first time in a polydnavirus system, these clusters also revealed sequences encoding enzymes presumed to form the replicative machinery of the progenitor virus and observed to be overexpressed in the virogenic tissue. Homology searches pointed to nucleocytoplasmic large DNA viruses as the likely source of these genes. These data, along with an analysis of the chromosomal form of five viral genome segments, provide clear evidence for the relatedness of the banchine and campoplegine Ichnovirus ancestors. IMPORTANCE Recent work indicates that the two recognized polydnavirus taxa, Bracovirus and Ichnovirus, are derived from distinct viruses whose genomes integrated into the genomes of ancestral wasps. However, the identity of the Ichnovirus ancestor is unknown, and questions remain regarding the possibility that the two described Ichnovirus subgroups, banchine and campoplegine Ichnoviruses, have distinct origins. Our study provides unequivocal evidence that these two Ichnovirus types are derived from related viral progenitors. This suggests that morphological and genomic differences observed between the Ichnovirus lineages, including features unique to banchine Ichnovirus genome segments, result from evolutionary divergence either before or after their endogenization. Strikingly, analysis of selected wasp genomic regions revealed genes presumed to be part of the replicative machinery of the progenitor virus, shedding new light on the likely identity of this virus. Finally, these genes could well play a role in Ichnovirus replication as they were overexpressed in the virogenic tissue.

  • Ultrastructural and genomic characterization of a second banchine polydnavirus confirms the existence of shared features within this Ichnovirus lineage.
    Journal of General Virology, 2013
    Co-Authors: Abdelmadjid Djoumad, Don Stoltz, Catherine Béliveau, Brian Boyle, Lisa Kuhn, Michel Cusson
    Abstract:

    Polydnaviruses (PDVs) are symbiotic viruses carried by endoparasitic wasps and transmitted to caterpillar hosts during parasitization. Although they share several features, including a segmented dsDNA genome, a unique life cycle where replication is restricted to the wasp host, and immunodepressive/developmental effects on the caterpillar host, PDVs carried by ichneumonid and braconid wasps (referred to as Ichnoviruses and bracoviruses, respectively) have different evolutionary origins. In addition, Ichnoviruses (IVs) form two distinct lineages, with viral entities found in wasps belonging to the subfamilies Campopleginae and Banchinae displaying strikingly different virion morphologies and genomic features. However, the current description for banchine IVs is based on the characterization of a single species, namely that of the Glypta fumiferanae IV (GfIV). Here we provide an ultrastructural and genomic analysis of a second banchine IV isolated from the wasp Apophua simplicipes, and we show that this virus shares many features with GfIV, including a multi-nucleocapsid virion, an aggregate genome size of ~300 kb, genome segments