Production of Early Expressed Parasitism-Specific Proteins in Alternate Sphingid Hosts of the Braconid WaspCotesia congregata

Harwood, Steven H.; McElfresh, J. Steven; Nguyen, Anthony; Conlan, Christopher A.; Beckage, Nancy E.

doi:10.1006/jipa.1997.4745

Cited by 42 publications

(22 citation statements)

References 36 publications

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“…C. congregata wasps (Hymenoptera: Braconidae) were reared under laboratory conditions on their natural host, the tobacco hornworm, M. sexta (Lepidoptera: Sphingidae). M. sexta larvae were reared on an artificial diet at 27°C under a 16-h-light/ 8-h-dark photoperiod and 70% Ϯ 5% relative humidity, as previously described (32). Five fourth-instar M. sexta larvae were exposed to C. congregata females until at least two ovipositions were observed on each larva.…”

Section: Methodsmentioning

confidence: 99%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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Bracoviruses (BVs) from the Polydnaviridae family are symbiotic viruses used as biological weapons by parasitoid wasps to manipulate lepidopteran host physiology and induce parasitism success. BV particles are produced by wasp ovaries and injected along with the eggs into the caterpillar host body, where viral gene expression is necessary for wasp development. Recent sequencing of the proviral genome of Cotesia congregata BV (CcBV) identified 222 predicted virulence genes present on 35 proviral segments integrated into the wasp genome. To date, the expressions of only a few selected candidate virulence genes have been studied in the caterpillar host, and we lacked a global vision of viral gene expression. In this study, a large-scale transcriptomic analysis by 454 sequencing of two immune tissues (fat body and hemocytes) of parasitized Manduca sexta caterpillar hosts allowed the detection of expression of 88 CcBV genes expressed 24 h after the onset of parasitism. We linked the expression profiles of these genes to several factors, showing that different regulatory mechanisms control viral gene expression in the host. These factors include the presence of signal peptides in encoded proteins, diversification of promoter regions, and, more surprisingly, gene position on the proviral genome. Indeed, most genes for which expression could be detected are localized in particular proviral regions globally producing higher numbers of circles. Moreover, this polydnavirus (PDV) transcriptomic analysis also reveals that a majority of CcBV genes possess at least one intron and an arthropod transcription start site, consistent with an insect origin of these virulence genes. IMPORTANCEBracoviruses (BVs) are symbiotic polydnaviruses used by parasitoid wasps to manipulate lepidopteran host physiology, ensuring wasp offspring survival. To date, the expressions of only a few selected candidate BV virulence genes have been studied in caterpillar hosts. We performed a large-scale analysis of BV gene expression in two immune tissues of Manduca sexta caterpillars parasitized by Cotesia congregata wasps. Genes for which expression could be detected corresponded to genes localized in particular regions of the viral genome globally producing higher numbers of circles. Our study thus brings an original global vision of viral gene expression and paves the way to the determination of the regulatory mechanisms enabling the expression of BV genes in targeted organisms, such as major insect pests. In addition, we identify sequence features suggesting that most BV virulence genes were acquired from insect genomes.

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Section: Methodsmentioning

confidence: 99%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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“…For PDV reintegration into wasp DNA, PDV circles would need to enter the wasp germline and to stably integrate into the wasp genome during the phase when parasitoid wasp eggs and larvae are exposed to virus circles in the haemolymph of the lepidopteran host. Concerning integration and transmission of PDV sequences in Lepidoptera, this implies wasp oviposition in semipermissive or non-permissive lepidopteran hosts that survive parasitism, and therefore 'live to tell the tale' of PDV integration [77,78].…”

Section: (D) Bracovirus Segment Reintegration Within Wasp and Lepidopmentioning

confidence: 99%

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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“…Cotesia congregata generally are restricted to larvae of Sphingidae as hosts; however, Krombein et al (1979) list only 15 sphingid species as hosts and also list Trichoplusia ni (Noctuidae) as a host. In laboratory experiments, Hyles lineata (Sphingidae) also was shown to be a permissive host, Pachysphinx occidentalis was a refractory host, showing complete encapsulation, and Sphinx vashti was considered semi-permissive, showing some encapsulation (Harwood et al, 1998). In another experiment, T. ni was a semi-permissive host (Beckage and Tan, 2002).…”

Section: Introductionmentioning

confidence: 97%

Caterpillar Chemical Defense and Parasitoid Success: Cotesia congregata Parasitism of Ceratomia catalpae

2010

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Sequestration of plant compounds by herbivorous insects as a defense against predators is well documented; however, few studies have examined the effectiveness of sequestration as a defense against parasitoids. One assumption of the "nasty host" hypothesis is that sequestration of plant defense compounds is deleterious to parasitoid development. We tested this hypothesis with larvae of the sequestering sphingid Ceratomia catalpae, which is heavily parasitized by the endoparasitoid Cotesia congregata, despite sequestering high concentrations of the iridoid glycoside catalpol from their catalpa host plants. We collected C. catalpae and catalpa leaves from six populations in the Eastern US, and allowed any C. congregata to emerge in the lab. Leaf iridoid glycosides and caterpillar iridoid glycosides were quantified, and we examined associations between sequestered caterpillar iridoid glycosides and C. congregata performance. Caterpillar iridoid glycosides were not associated with C. congregata field parasitism or number of offspring produced. Although wasp survival was over 90% in all populations, there was a slight negative relationship between caterpillar iridoid glycosides and wasp survival. Iridoid glycosides were present in caterpillars at levels that are deterrent to a variety of vertebrate and invertebrate predators. Thus, our results support the alternative hypothesis that unpalatable, chemically defended hosts are "safe havens" for endoparasitoids. Future trials examining the importance of catalpol sequestration to potential natural enemies of C. congregata and C. catalpae are necessary to strengthen this conclusion.

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Production of Early Expressed Parasitism-Specific Proteins in Alternate Sphingid Hosts of the Braconid WaspCotesia congregata

Cited by 42 publications

References 36 publications

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

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

Caterpillar Chemical Defense and Parasitoid Success: Cotesia congregata Parasitism of Ceratomia catalpae

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