title: Genomic and Proteomic Analyses Indicate that Banchine and Campoplegine Polydnaviruses Have Similar, if Not Identical, Viral Ancestors.
abstract: Polydnaviruses form a group of unconventional double-stranded DNA (dsDNA) viruses transmitted by endoparasitic wasps during egg laying into caterpillar hosts, where viral gene expression is essential to immature wasp survival. A copy of the viral genome is present in wasp chromosomes, thus ensuring vertical transmission. Polydnaviruses comprise two taxa, Bracovirus and Ichnovirus, shown to have distinct viral ancestors whose genomes were "captured" by ancestral wasps. While evidence indicates that bracoviruses derive from a nudivirus ancestor, the identity of the ichnovirus progenitor remains unknown. In addition, ichnoviruses are found in two ichneumonid wasp subfamilies, Campopleginae and Banchinae, where they constitute morphologically and genomically different virus types. To address the question of whether these two ichnovirus subgroups have distinct ancestors, we used genomic, proteomic, and transcriptomic analyses to characterize particle proteins of the banchine Glypta fumiferanae ichnovirus and the genes encoding them. Several proteins were found to be homologous to those identified earlier for campoplegine ichnoviruses while the corresponding genes were located in clusters of the wasp genome similar to those observed previously in a campoplegine wasp. However, for the first time in a polydnavirus system, these clusters also revealed sequences encoding enzymes presumed to form the replicative machinery of the progenitor virus and observed to be overexpressed in the virogenic tissue. Homology searches pointed to nucleocytoplasmic large DNA viruses as the likely source of these genes. These data, along with an analysis of the chromosomal form of five viral genome segments, provide clear evidence for the relatedness of the banchine and campoplegine ichnovirus ancestors.
  
  
  OBJECTIVE
  Recent work indicates that the two recognized polydnavirus taxa, Bracovirus and Ichnovirus, are derived from distinct viruses whose genomes integrated into the genomes of ancestral wasps. However, the identity of the ichnovirus ancestor is unknown, and questions remain regarding the possibility that the two described ichnovirus subgroups, banchine and campoplegine ichnoviruses, have distinct origins. Our study provides unequivocal evidence that these two ichnovirus types are derived from related viral progenitors. This suggests that morphological and genomic differences observed between the ichnovirus lineages, including features unique to banchine ichnovirus genome segments, result from evolutionary divergence either before or after their endogenization. Strikingly, analysis of selected wasp genomic regions revealed genes presumed to be part of the replicative machinery of the progenitor virus, shedding new light on the likely identity of this virus. Finally, these genes could well play a role in ichnovirus replication as they were overexpressed in the virogenic tissue.
authors.affiliation: Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada.
authors.forename: Catherine
authors.initials: C
authors.lastname: Béliveau
authors.affiliation: Proteomics Core Facility, Dalhousie University, Halifax, Nova Scotia, Canada.
authors.forename: Alejandro
authors.initials: A
authors.lastname: Cohen
authors.affiliation: Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada.
authors.forename: Don
authors.initials: D
authors.lastname: Stewart
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, Université François-Rabelais et CNRS UMR 7261, Tours, France.
authors.forename: Georges
authors.initials: G
authors.lastname: Periquet
authors.affiliation: Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada.
authors.forename: Abdelmadjid
authors.initials: A
authors.lastname: Djoumad
authors.affiliation: Department of Microbiology and Immunology, Dalhousie University, Halifax, Nova Scotia, Canada.
authors.forename: Lisa
authors.initials: L
authors.lastname: Kuhn
authors.affiliation: Department of Microbiology and Immunology, Dalhousie University, Halifax, Nova Scotia, Canada.
authors.forename: Don
authors.initials: D
authors.lastname: Stoltz
authors.affiliation: Institut de Biologie Intégrative et des Systèmes, Université Laval, Quebec City, Quebec, Canada.
authors.forename: Brian
authors.initials: B
authors.lastname: Boyle
authors.affiliation: UMR 1333 INRA, Université Montpellier, Diversité, Génomes, Interactions Microorganismes-Insectes, Montpellier, France.
authors.forename: Anne-Nathalie
authors.initials: AN
authors.lastname: Volkoff
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, Université François-Rabelais et CNRS UMR 7261, Tours, France.
authors.forename: Elisabeth A
authors.initials: EA
authors.lastname: Herniou
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, Université François-Rabelais et CNRS UMR 7261, Tours, France.
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Drezen
authors.affiliation: Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada Département de Biochimie, de Microbiologie et de Bio-informatique, Université Laval, Quebec City, Quebec, Canada michel.cusson@nrcan-rncan.gc.ca.
authors.forename: Michel
authors.initials: M
authors.lastname: Cusson
mesh_terms: D000818:Animals; D001483:Base Sequence; D005075:Biological Evolution; D004279:DNA, Viral / Q000235:genetics*; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D016679:Genome, Viral; D023281:Genomics; D008969:Molecular Sequence Data; D018071:Polydnaviridae / Q000145:classification* / Q000201:enzymology / Q000235:genetics*; D017422:Sequence Analysis, DNA; D014764:Viral Proteins / Q000235:genetics; D014863:Wasps / Q000821:virology
chemical_list: D004279:DNA, Viral; D014764:Viral Proteins