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Marc Ravallec - One of the best experts on this subject based on the ideXlab platform.
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Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps
BMC Biology, 2020Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Stéphanie Robin, Bernardo Santos, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Jean-michel Drezen, Denis TaguAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps.
PLoS pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps
PLoS Pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels
BMC Genomics, 2006Co-Authors: Mouna Barat-houari, F-x Jousset, Frédérique Hilliou, Luc Sofer, Marc Ravallec, Emeline Deleury, Pierre Delobel, Javier Rocher, Laurent Galibert, René FeyereisenAbstract:BackgroundGenomic approaches provide unique opportunities to study interactions of insects with their pathogens. We developed a cDNA microarray to analyze the gene transcription profile of the lepidopteran pest Spodoptera frugiperda in response to injection of the polydnavirus HdIV associated with the Ichneumonid wasp Hyposoter didymator. Polydnaviruses are associated with parasitic ichneumonoid wasps and are required for their development within the lepidopteran host, in which they act as potent immunosuppressive pathogens. In this study, we analyzed transcriptional variations in the two main effectors of the insect immune response, the hemocytes and the fat body, after injection of filter-purified HdIV.ResultsResults show that 24 hours post-injection, about 4% of the 1750 arrayed host genes display changes in their transcript levels with a large proportion (76%) showing a decrease. As a comparison, in S. frugiperda fat body, after injection of the pathogenic JcDNV densovirus, 8 genes display significant changes in their transcript level. They differ from the 7 affected by HdIV and, as opposed to HdIV injection, are all up-regulated. Interestingly, several of the genes that are modulated by HdIV injection have been shown to be involved in lepidopteran innate immunity. Levels of transcripts related to calreticulin, prophenoloxidase-activating enzyme, immulectin-2 and a novel lepidopteran scavenger receptor are decreased in hemocytes of HdIV-injected caterpillars. This was confirmed by quantitative RT-PCR analysis but not observed after injection of heat-inactivated HdIV. Conversely, an increased level of transcripts was found for a galactose-binding lectin and, surprisingly, for the prophenoloxidase subunits. The results obtained suggest that HdIV injection affects transcript levels of genes encoding different components of the host immune response (non-self recognition, humoral and cellular responses).ConclusionThis analysis of the host-polydnavirus interactions by a microarray approach indicates that the presence of HdIV induces, directly or indirectly, variations in transcript levels of specific host genes, changes that could be responsible in part for the alterations observed in the parasitized host physiology. Development of such global approaches will allow a better understanding of the strategies employed by parasites to manipulate their host physiology, and will permit the identification of potential targets of the immunosuppressive polydnaviruses.
Don Stoltz - One of the best experts on this subject based on the ideXlab platform.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps.
PLoS pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps
PLoS Pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
Véronique Jouan - One of the best experts on this subject based on the ideXlab platform.
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Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps
BMC Biology, 2020Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Stéphanie Robin, Bernardo Santos, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Jean-michel Drezen, Denis TaguAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps.
PLoS pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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Western European populations of the Ichneumonid wasp Hyposoter didymator belong to a single taxon
2019Co-Authors: Marie Frayssinet, Philippe Audiot, Antonino Cusumano, Apolline Pichon, Lisa Malm, Véronique Jouan, Marin Vabre, Serge Malavieille, Magalie Delalande, Enrique Vargas-osunaAbstract:Western European populations of the Ichneumonid wasp Hyposoter didymator belong to a single taxon. 6. International Entomophagous Insects Conference
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps
PLoS Pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
Fabrice Legeai - One of the best experts on this subject based on the ideXlab platform.
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Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps
BMC Biology, 2020Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Stéphanie Robin, Bernardo Santos, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Jean-michel Drezen, Denis TaguAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps.
PLoS pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps
PLoS Pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
Stéphanie Robin - One of the best experts on this subject based on the ideXlab platform.
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Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps
BMC Biology, 2020Co-Authors: Fabrice Legeai, Marc Ravallec, Véronique Jouan, Stéphanie Robin, Bernardo Santos, Anthony Bretaudeau, Rebecca Dikow, Claire Lemaitre, Jean-michel Drezen, Denis TaguAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps.
PLoS pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
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RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in Ichneumonid wasps
PLoS Pathogens, 2019Co-Authors: Ange Lorenzi, Marc Ravallec, Isabelle Darboux, Véronique Jouan, Magali Eychenne, Stéphanie Robin, Fabrice Legeai, Anne-sophie Gosselin-grenet, Mathieu Sicard, Don StoltzAbstract: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.
