Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp's genome and excised only in later pupal and adult stages of the female

Gruber, Andreas; Stettler, Peter; Heiniger, P; Schümperli, Daniel; Lanzrein, Beatrice

doi:10.1099/0022-1317-77-11-2873

Cited by 88 publications

(93 citation statements)

References 18 publications

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“…First viral DNA sequences have to be amplified within wasp cells in nuclear virus factories. Contrary to initial hypotheses [44,45], it is not the circles themselves that are amplified from proviral segment excision but larger molecules [46] that are replicated linearly [36]. In C. congregata, two segments were found to amplify together within the same molecule as well as sequences not packaged in the particles [46].…”

Section: (Iii) Bracovirus Replicationmentioning

confidence: 64%

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Herniou

Huguet

Thézé

et al. 2013

Phil. Trans. R. Soc. B

157

172

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International audienceThe Polydnaviridae (PDV), including the Bracovirus (BV) and Ichnovirus genera, originated from the integration of unrelated viruses in the genomes of two parasitoid wasp lineages, in a remarkable example of convergent evolution. Functionally active PDVs represent the most compelling evolutionary success among endogenous viral elements (EVEs). BV evolved from the domestication by braconid wasps of a nudivirus 100 Ma. The nudivirus genome has become an EVE involved in BV particle production but is not encapsidated. Instead, BV genomes have co-opted virulence genes, used by the wasps to control the immunity and development of their hosts. Gene transfers and duplications have shaped BV genomes, now encoding hundreds of genes. Phylogenomic studies suggest that BVs contribute largely to wasp diversification and adaptation to their hosts. A genome evolution model explains how multidirectional wasp adaptation to different host species could have fostered PDV genome extension. Integrative studies linking ecological data on the wasp to genomic analyses should provide new insights into the adaptive role of particular BV genes. Forthcoming genomic advances should also indicate if the associations between endoparasitoid wasps and symbiotic viruses evolved because of their particularly intimate interactions with their hosts, or if similar domesticated EVEs could be uncovered in other parasites

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Section: (Iii) Bracovirus Replicationmentioning

confidence: 64%

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Herniou

Huguet

Thézé

et al. 2013

Phil. Trans. R. Soc. B

157

172

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“…All proviral segments from all BVs analysed to date are terminated by direct repeats at both extremities, termed DRJs [12,13,16,29,30,32]. Bracovirus circles contain a unique sequence (circle junction) produced from a recombination event between these DRJs [12,33].…”

Section: (C) Proviral Segment Extremities Are Conservedmentioning

confidence: 99%

Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata : insights into the evolutionary dynamics of bracoviruses

Bézier

Louis

Jancek

et al. 2013

Phil. Trans. R. Soc. B

151

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International audienceBracoviruses represent the most complex endogenous viral elements (EVEs) described to date. Nudiviral genes have been hosted within parasitoid wasp genomes since approximately 100 Ma. They play a crucial role in the wasp life cycle as they produce bracovirus particles, which are injected into parasitized lepidopteran hosts during wasp oviposition. Bracovirus particles encapsidatemultiple dsDNAcircles encoding virulence genes. Their expression in parasitized caterpillars is essential for wasp parasitism success. Here, we report on the genomic organization of the proviral segments (i.e. master sequences used to produce the encapsidated dsDNA circles) present in the Cotesia congregata parasitoid wasp genome. The provirus is composed of a macrolocus, comprising two-thirds of the proviral segments and of seven dispersed loci, each containing one to three segments. Comparative genomic analyses with closely related species gave insights into the evolutionary dynamics of bracovirus genomes. Conserved synteny in the differentwasp genomes showed the orthology of the proviral macrolocus across different species. The nudiviral gene odv-e66-like1 is conserved within themacrolocus, suggesting an ancient co-localization of the nudiviral genome and bracovirus proviral segments. By contrast, the evolution of proviral segments within the macrolocus has involved a series of lineage-specific duplications

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“…The morphogenesis of the ovary in the course of pupal-adult development is strictly correlated with the pigmentation pattern of the pupae and has been subdivided into stages 1-6 (Albrecht et al, 1994). Excision and circularization of viral DNA has been shown to commence at stage 3b (Gruber et al, 1996;Wyder et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…We used the braconid wasp C. inanitus and its polydnavirus (CiV) as a model system. The excision sites of two viral segments (CiV12 and CiV14) have been analysed and it has been shown that excision occurs through a sitespecific recombinational event and that, after excision, flanking regions are rejoined (Gruber et al, 1996;Wyder et al, 2002). Proviral CiV segments appear to be clustered in the genome of the wasp, as flanking regions of CiV12 and CiV14 have been shown to hybridize to other viral segments (Wyder et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…The initiation of virus replication has been shown to be associated with a specific phase in pupal-adult development in the ichneumonid Campoletis sonorensis (Norton & Vinson, 1983) and the two braconids Chelonus inanitus and Cotesia congregata (Albrecht et al, 1994;Gruber et al, 1996;Savary et al, 1999;Pasquier-Barre et al, 2002). In C. sonorensis it has been proposed, on the basis of ligation and in vitro application of 20-hydroxyecdysone (20E), that this hormone may regulate polydnavirus replication (Webb & Summers, 1992).…”

Section: Introductionmentioning

confidence: 99%

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Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres

Marti

Grossniklaus-Bürgin

Wyder

et al. 2003

Journal of General Virology

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Polydnaviruses are unique symbiotic viruses that are replicated in the calyx cells of the ovary of some parasitic wasps. They have a segmented genome of circular double-stranded DNA and are injected along with the wasp's egg into the host, where they are essential for successful parasitism. Polydnaviruses replicate from integrated proviral DNA, and after excision of viral segments, flanking DNA is rejoined. Little is known about ovarian morphogenesis, the mode of amplification of the viral DNA and the involvement of ecdysteroids. Here we have analysed these parameters in the course of pupal-adult development in the braconid wasp Chelonus inanitus. Immediately after pupation, ovarian cells proliferated and calyx cells began to differentiate; at this stage ecdysteroids, in particular 20-hydroxyecdysone, were highest. Thereafter, calyx cells began to increase in size and DNA content and eventually became gigantic. Amplification of non-viral DNA (actin) and viral DNA in its integrated and excised form and of corresponding rejoined flanking regions was measured by quantitative real-time PCR. In the early phase of calyx cell differentiation, copy numbers of actin and integrated viral DNA increased to a similar extent. This, along with the increase in nuclear volume and DNA content in the absence of extensive cell proliferation, suggested polyploidization of the early stage calyx cells. In the following phase, integrated viral DNA was selectively and intensively amplified and eventually excised and circularized. As copy numbers of excised circular viral DNA and rejoined flanking DNA reached similarly high levels, excised viral DNA appeared not to replicate. After adult eclosion, amplification of viral DNA declined.

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Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp's genome and excised only in later pupal and adult stages of the female

Cited by 88 publications

References 18 publications

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata : insights into the evolutionary dynamics of bracoviruses

Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres

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