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Open Access Research

Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps

Christopher A Desjardins16*, Dawn E Gundersen-Rindal2, Jessica B Hostetler1, Luke J Tallon17, Douglas W Fadrosh18, Roger W Fuester3, Monica J Pedroni29, Brian J Haas110, Michael C Schatz4, Kristine M Jones17, Jonathan Crabtree17, Heather Forberger1 and Vishvanath Nene15

Author Affiliations

1 J Craig Venter Institute, Rockville, MD 20850, USA

2 USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, Beltsville, MD 20705, USA

3 USDA-ARS Beneficial Insect Introduction Research Laboratory, Newark, DE 19713, USA

4 Center for Bioinformatics and Computational Biology, University of Maryland, College Park, MD 20742, USA

5 Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA

6 Current address: Department of Biology, University of Rochester, Rochester, NY 14627, USA

7 Current address: Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD 21201, USA

8 Current address: J Craig Venter Institute, La Jolla, CA 92121, USA

9 Current address: Department of Veterinary Microbiology and Pathology, Washington State University, WA 99164, USA

10 Current address: The Broad Institute, Cambridge, MA 02142, USA

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Genome Biology 2008, 9:R183  doi:10.1186/gb-2008-9-12-r183

Published: 30 December 2008

Abstract

Background

Polydnaviruses, double-stranded DNA viruses with segmented genomes, have evolved as obligate endosymbionts of parasitoid wasps. Virus particles are replication deficient and produced by female wasps from proviral sequences integrated into the wasp genome. These particles are co-injected with eggs into caterpillar hosts, where viral gene expression facilitates parasitoid survival and, thereby, survival of proviral DNA. Here we characterize and compare the encapsidated viral genome sequences of bracoviruses in the family Polydnaviridae associated with Glyptapanteles gypsy moth parasitoids, along with near complete proviral sequences from which both viral genomes are derived.

Results

The encapsidated Glyptapanteles indiensis and Glyptapanteles flavicoxis bracoviral genomes, each composed of 29 different size segments, total approximately 517 and 594 kbp, respectively. They are generated from a minimum of seven distinct loci in the wasp genome. Annotation of these sequences revealed numerous novel features for polydnaviruses, including insect-like sugar transporter genes and transposable elements. Evolutionary analyses suggest that positive selection is widespread among bracoviral genes.

Conclusions

The structure and organization of G. indiensis and G. flavicoxis bracovirus proviral segments as multiple loci containing one to many viral segments, flanked and separated by wasp gene-encoding DNA, is confirmed. Rapid evolution of bracovirus genes supports the hypothesis of bracovirus genes in an 'arms race' between bracovirus and caterpillar. Phylogenetic analyses of the bracoviral genes encoding sugar transporters provides the first robust evidence of a wasp origin for some polydnavirus genes. We hypothesize transposable elements, such as those described here, could facilitate transfer of genes between proviral segments and host DNA.