Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.

BACKGROUND:The ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenet...

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Main Authors: Yves Bigot, Sylvaine Renault, Jacques Nicolas, Corinne Moundras, Marie-Véronique Demattei, Sylvie Samain, Dennis K Bideshi, Brian A Federici
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-07-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2712680?pdf=render
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spelling doaj-581503aa2bb94ba895969e0035ef1fa22020-11-25T02:05:19ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-07-0147e639710.1371/journal.pone.0006397Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.Yves BigotSylvaine RenaultJacques NicolasCorinne MoundrasMarie-Véronique DematteiSylvie SamainDennis K BideshiBrian A FedericiBACKGROUND:The ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is also likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae). METHODOLOGY/PRINCIPAL FINDINGS:To clarify the evolutionary relationships of these large double-stranded DNA viruses, we sequenced the genome of DpAV4a and undertook phylogenetic analyses of the above viruses and others, including iridoviruses pathogenic to vertebrates. The DpAV4a genome consisted of 119,343 bp and contained at least 119 open reading frames (ORFs), the analysis of which confirmed the relatedness of this virus to iridoviruses and other ascoviruses. CONCLUSIONS:Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related. Nevertheless, our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure (icosahedral to bacilliform), genome configuration (linear to circular), and cytopathology (plasmalemma blebbing to virion-containing vesicles). Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage. Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.http://europepmc.org/articles/PMC2712680?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yves Bigot
Sylvaine Renault
Jacques Nicolas
Corinne Moundras
Marie-Véronique Demattei
Sylvie Samain
Dennis K Bideshi
Brian A Federici
spellingShingle Yves Bigot
Sylvaine Renault
Jacques Nicolas
Corinne Moundras
Marie-Véronique Demattei
Sylvie Samain
Dennis K Bideshi
Brian A Federici
Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
PLoS ONE
author_facet Yves Bigot
Sylvaine Renault
Jacques Nicolas
Corinne Moundras
Marie-Véronique Demattei
Sylvie Samain
Dennis K Bideshi
Brian A Federici
author_sort Yves Bigot
title Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
title_short Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
title_full Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
title_fullStr Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
title_full_unstemmed Symbiotic virus at the evolutionary intersection of three types of large DNA viruses; iridoviruses, ascoviruses, and ichnoviruses.
title_sort symbiotic virus at the evolutionary intersection of three types of large dna viruses; iridoviruses, ascoviruses, and ichnoviruses.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2009-07-01
description BACKGROUND:The ascovirus, DpAV4a (family Ascoviridae), is a symbiotic virus that markedly increases the fitness of its vector, the parasitic ichneumonid wasp, Diadromus puchellus, by increasing survival of wasp eggs and larvae in their lepidopteran host, Acrolepiopsis assectella. Previous phylogenetic studies have indicated that DpAV4a is related to the pathogenic ascoviruses, such as the Spodoptera frugiperda ascovirus 1a (SfAV1a) and the lepidopteran iridovirus (family Iridoviridae), Chilo iridescent virus (CIV), and is also likely related to the ancestral source of certain ichnoviruses (family Polydnaviridae). METHODOLOGY/PRINCIPAL FINDINGS:To clarify the evolutionary relationships of these large double-stranded DNA viruses, we sequenced the genome of DpAV4a and undertook phylogenetic analyses of the above viruses and others, including iridoviruses pathogenic to vertebrates. The DpAV4a genome consisted of 119,343 bp and contained at least 119 open reading frames (ORFs), the analysis of which confirmed the relatedness of this virus to iridoviruses and other ascoviruses. CONCLUSIONS:Analyses of core DpAV4a genes confirmed that ascoviruses and iridoviruses are evolutionary related. Nevertheless, our results suggested that the symbiotic DpAV4a had a separate origin in the iridoviruses from the pathogenic ascoviruses, and that these two types shared parallel evolutionary paths, which converged with respect to virion structure (icosahedral to bacilliform), genome configuration (linear to circular), and cytopathology (plasmalemma blebbing to virion-containing vesicles). Our analyses also revealed that DpAV4a shared more core genes with CIV than with other ascoviruses and iridoviruses, providing additional evidence that DpAV4a represents a separate lineage. Given the differences in the biology of the various iridoviruses and ascoviruses studied, these results provide an interesting model for how viruses of different families evolved from one another.
url http://europepmc.org/articles/PMC2712680?pdf=render
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