Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome

Anne-Nathalie Volkoff, Veronique Jouan, Serge Urbach, Sylvie Samain, Max Bergoin, Patrick Wincker, Edith Demettre, Francois Cousserans, Bertille Provost, Fasseli Joseph Coulibaly, Fabrice Legeai, Catherine Beliveau, Michel Cusson, Gabor Gyapay, Jean-Michel Drezen

Research output: Contribution to journalArticleResearchpeer-review

Abstract

The polydnaviruses (PDVs) are a unique virus type used by an organism (a parasitic wasp) to manipulate the physiology of another organism (a lepidopteran host) in order to ensure successful parasitism. The evolutionary origin of these unusual viruses, found in a??17,500 braconid wasps (Bracoviruses) and a??15,000 ichneumonid wasps (Ichnoviruses), has been a major question for the last decade. We thus undertook an exclusive work aiming at investigating this origin via the characterization of genes encoding structural components for both types of PDVs. The present paper constitutes the first report on the identity and genome organisation of the viral machinery producing Ichnovirus virions. Our results strongly suggest that Ichnoviruses originated from a virus belonging to a group as yet uncharacterized that integrated its genome into that of an ichneumonid wasp ancestor. More importantly, our results demonstrate that the ancestor of Ichnoviruses differs from that of Bracoviruses, which originated from a nudivirus. We have now identified, for the two types of PDVs, the non packaged viral genes and their products involved in producing particles injected into the host during oviposition. Together, these data provide an example of convergent evolution where different groups of wasps have independently domesticated viruses to deliver genes into their hosts.
Original languageEnglish
Pages (from-to)1 - 10
Number of pages10
JournalPLoS Pathogens
Volume6
Issue number5 (e1000923)
DOIs
Publication statusPublished - 2010

Cite this

Volkoff, A-N., Jouan, V., Urbach, S., Samain, S., Bergoin, M., Wincker, P., ... Drezen, J-M. (2010). Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathogens, 6(5 (e1000923)), 1 - 10. https://doi.org/10.1371/journal.ppat.1000923
Volkoff, Anne-Nathalie ; Jouan, Veronique ; Urbach, Serge ; Samain, Sylvie ; Bergoin, Max ; Wincker, Patrick ; Demettre, Edith ; Cousserans, Francois ; Provost, Bertille ; Coulibaly, Fasseli Joseph ; Legeai, Fabrice ; Beliveau, Catherine ; Cusson, Michel ; Gyapay, Gabor ; Drezen, Jean-Michel. / Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. In: PLoS Pathogens. 2010 ; Vol. 6, No. 5 (e1000923). pp. 1 - 10.
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abstract = "The polydnaviruses (PDVs) are a unique virus type used by an organism (a parasitic wasp) to manipulate the physiology of another organism (a lepidopteran host) in order to ensure successful parasitism. The evolutionary origin of these unusual viruses, found in a??17,500 braconid wasps (Bracoviruses) and a??15,000 ichneumonid wasps (Ichnoviruses), has been a major question for the last decade. We thus undertook an exclusive work aiming at investigating this origin via the characterization of genes encoding structural components for both types of PDVs. The present paper constitutes the first report on the identity and genome organisation of the viral machinery producing Ichnovirus virions. Our results strongly suggest that Ichnoviruses originated from a virus belonging to a group as yet uncharacterized that integrated its genome into that of an ichneumonid wasp ancestor. More importantly, our results demonstrate that the ancestor of Ichnoviruses differs from that of Bracoviruses, which originated from a nudivirus. We have now identified, for the two types of PDVs, the non packaged viral genes and their products involved in producing particles injected into the host during oviposition. Together, these data provide an example of convergent evolution where different groups of wasps have independently domesticated viruses to deliver genes into their hosts.",
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Volkoff, A-N, Jouan, V, Urbach, S, Samain, S, Bergoin, M, Wincker, P, Demettre, E, Cousserans, F, Provost, B, Coulibaly, FJ, Legeai, F, Beliveau, C, Cusson, M, Gyapay, G & Drezen, J-M 2010, 'Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome' PLoS Pathogens, vol. 6, no. 5 (e1000923), pp. 1 - 10. https://doi.org/10.1371/journal.ppat.1000923

Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. / Volkoff, Anne-Nathalie; Jouan, Veronique; Urbach, Serge; Samain, Sylvie; Bergoin, Max; Wincker, Patrick; Demettre, Edith; Cousserans, Francois; Provost, Bertille; Coulibaly, Fasseli Joseph; Legeai, Fabrice; Beliveau, Catherine; Cusson, Michel; Gyapay, Gabor; Drezen, Jean-Michel.

In: PLoS Pathogens, Vol. 6, No. 5 (e1000923), 2010, p. 1 - 10.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome

AU - Volkoff, Anne-Nathalie

AU - Jouan, Veronique

AU - Urbach, Serge

AU - Samain, Sylvie

AU - Bergoin, Max

AU - Wincker, Patrick

AU - Demettre, Edith

AU - Cousserans, Francois

AU - Provost, Bertille

AU - Coulibaly, Fasseli Joseph

AU - Legeai, Fabrice

AU - Beliveau, Catherine

AU - Cusson, Michel

AU - Gyapay, Gabor

AU - Drezen, Jean-Michel

PY - 2010

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N2 - The polydnaviruses (PDVs) are a unique virus type used by an organism (a parasitic wasp) to manipulate the physiology of another organism (a lepidopteran host) in order to ensure successful parasitism. The evolutionary origin of these unusual viruses, found in a??17,500 braconid wasps (Bracoviruses) and a??15,000 ichneumonid wasps (Ichnoviruses), has been a major question for the last decade. We thus undertook an exclusive work aiming at investigating this origin via the characterization of genes encoding structural components for both types of PDVs. The present paper constitutes the first report on the identity and genome organisation of the viral machinery producing Ichnovirus virions. Our results strongly suggest that Ichnoviruses originated from a virus belonging to a group as yet uncharacterized that integrated its genome into that of an ichneumonid wasp ancestor. More importantly, our results demonstrate that the ancestor of Ichnoviruses differs from that of Bracoviruses, which originated from a nudivirus. We have now identified, for the two types of PDVs, the non packaged viral genes and their products involved in producing particles injected into the host during oviposition. Together, these data provide an example of convergent evolution where different groups of wasps have independently domesticated viruses to deliver genes into their hosts.

AB - The polydnaviruses (PDVs) are a unique virus type used by an organism (a parasitic wasp) to manipulate the physiology of another organism (a lepidopteran host) in order to ensure successful parasitism. The evolutionary origin of these unusual viruses, found in a??17,500 braconid wasps (Bracoviruses) and a??15,000 ichneumonid wasps (Ichnoviruses), has been a major question for the last decade. We thus undertook an exclusive work aiming at investigating this origin via the characterization of genes encoding structural components for both types of PDVs. The present paper constitutes the first report on the identity and genome organisation of the viral machinery producing Ichnovirus virions. Our results strongly suggest that Ichnoviruses originated from a virus belonging to a group as yet uncharacterized that integrated its genome into that of an ichneumonid wasp ancestor. More importantly, our results demonstrate that the ancestor of Ichnoviruses differs from that of Bracoviruses, which originated from a nudivirus. We have now identified, for the two types of PDVs, the non packaged viral genes and their products involved in producing particles injected into the host during oviposition. Together, these data provide an example of convergent evolution where different groups of wasps have independently domesticated viruses to deliver genes into their hosts.

UR - http://www.ncbi.nlm.nih.gov/pubmed/20523890

U2 - 10.1371/journal.ppat.1000923

DO - 10.1371/journal.ppat.1000923

M3 - Article

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Volkoff A-N, Jouan V, Urbach S, Samain S, Bergoin M, Wincker P et al. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathogens. 2010;6(5 (e1000923)):1 - 10. https://doi.org/10.1371/journal.ppat.1000923