Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis

<p>Abstract</p> <p>Background</p> <p>Female 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...

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Main Authors: Augé-Gouillou Corinne, Samain Sylvie, Bigot Yves, Federici Brian A
Format: Article
Language:English
Published: BMC 2008-09-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/8/253
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spelling doaj-5f9a6fae975544ecac4fe1dfb67c55282021-09-02T05:28:05ZengBMCBMC Evolutionary Biology1471-21482008-09-018125310.1186/1471-2148-8-253Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesisAugé-Gouillou CorinneSamain SylvieBigot YvesFederici Brian A<p>Abstract</p> <p>Background</p> <p>Female 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.</p> <p>Results</p> <p>Here we show that a family of unique pox-D5 NTPase proteins in the <it>Glypta fumiferanae </it>ichnovirus are related to three <it>Diadromus pulchellus </it>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.</p> <p>Conclusion</p> <p>Our 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.</p> http://www.biomedcentral.com/1471-2148/8/253
collection DOAJ
language English
format Article
sources DOAJ
author Augé-Gouillou Corinne
Samain Sylvie
Bigot Yves
Federici Brian A
spellingShingle Augé-Gouillou Corinne
Samain Sylvie
Bigot Yves
Federici Brian A
Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
BMC Evolutionary Biology
author_facet Augé-Gouillou Corinne
Samain Sylvie
Bigot Yves
Federici Brian A
author_sort Augé-Gouillou Corinne
title Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
title_short Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
title_full Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
title_fullStr Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
title_full_unstemmed Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
title_sort molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2008-09-01
description <p>Abstract</p> <p>Background</p> <p>Female 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.</p> <p>Results</p> <p>Here we show that a family of unique pox-D5 NTPase proteins in the <it>Glypta fumiferanae </it>ichnovirus are related to three <it>Diadromus pulchellus </it>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.</p> <p>Conclusion</p> <p>Our 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.</p>
url http://www.biomedcentral.com/1471-2148/8/253
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