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Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps

Fabrice Legeai, Bernardo F. Santos, Stéphanie Robin, Anthony Bretaudeau, Rebecca B. Dikow, Claire Lemaitre, Véronique Jouan, Marc Ravallec, Jean-Michel Drezen, Denis Tagu, Gabor Gyapay, Xin Zhou, Shanlin Liu, Bruce A. Webb, Seán G. Brady, Anne-Nathalie Volkoff
doi: https://doi.org/10.1101/861310
Fabrice Legeai
1IGEPP, Agrocampus Ouest, INRA, Université de Rennes 1, 35650 Le Rheu, France
2Université Rennes 1, INRIA, CNRS, IRISA, F-35000 Rennes, France
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Bernardo F. Santos
3Department of Entomology, National Museum of Natural History, Smithsonian Institution, 10th and Constitution Avenue NW, Washington, DC 20560-0165, USA
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Stéphanie Robin
1IGEPP, Agrocampus Ouest, INRA, Université de Rennes 1, 35650 Le Rheu, France
2Université Rennes 1, INRIA, CNRS, IRISA, F-35000 Rennes, France
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Anthony Bretaudeau
1IGEPP, Agrocampus Ouest, INRA, Université de Rennes 1, 35650 Le Rheu, France
2Université Rennes 1, INRIA, CNRS, IRISA, F-35000 Rennes, France
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Rebecca B. Dikow
3Department of Entomology, National Museum of Natural History, Smithsonian Institution, 10th and Constitution Avenue NW, Washington, DC 20560-0165, USA
4Data Science Lab, Office of the Chief Information Officer, Smithsonian Institution, 10th and Constitution Avenue NW, Washington, DC 20560-0165, USA
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Claire Lemaitre
2Université Rennes 1, INRIA, CNRS, IRISA, F-35000 Rennes, France
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Véronique Jouan
5DGIMI, INRA, University of Montpellier, Montpellier, France
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Marc Ravallec
5DGIMI, INRA, University of Montpellier, Montpellier, France
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Jean-Michel Drezen
6Institut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS - Université de Tours, UFR des Sciences et Techniques, Parc de Grandmont, Tours, France
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Denis Tagu
1IGEPP, Agrocampus Ouest, INRA, Université de Rennes 1, 35650 Le Rheu, France
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Gabor Gyapay
7Commissariat à l’Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, Evry 91057, France
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Xin Zhou
8Department of Entomology, China Agricultural University, Beijing 100193, People’s Republic of China
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Shanlin Liu
8Department of Entomology, China Agricultural University, Beijing 100193, People’s Republic of China
9China National GeneBank, BGI-Shenzhen, Shenzhen, Guangdong Province, 518083, People’s Republic of China
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Bruce A. Webb
10Department of Entomology, University of Kentucky, Lexington, USA
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Seán G. Brady
3Department of Entomology, National Museum of Natural History, Smithsonian Institution, 10th and Constitution Avenue NW, Washington, DC 20560-0165, USA
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Anne-Nathalie Volkoff
5DGIMI, INRA, University of Montpellier, Montpellier, France
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  • For correspondence: anne-nathalie.volkoff@inra
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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.

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Posted December 02, 2019.
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Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps
Fabrice Legeai, Bernardo F. Santos, Stéphanie Robin, Anthony Bretaudeau, Rebecca B. Dikow, Claire Lemaitre, Véronique Jouan, Marc Ravallec, Jean-Michel Drezen, Denis Tagu, Gabor Gyapay, Xin Zhou, Shanlin Liu, Bruce A. Webb, Seán G. Brady, Anne-Nathalie Volkoff
bioRxiv 861310; doi: https://doi.org/10.1101/861310
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Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps
Fabrice Legeai, Bernardo F. Santos, Stéphanie Robin, Anthony Bretaudeau, Rebecca B. Dikow, Claire Lemaitre, Véronique Jouan, Marc Ravallec, Jean-Michel Drezen, Denis Tagu, Gabor Gyapay, Xin Zhou, Shanlin Liu, Bruce A. Webb, Seán G. Brady, Anne-Nathalie Volkoff
bioRxiv 861310; doi: https://doi.org/10.1101/861310

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