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Nancy E Beckage - One of the best experts on this subject based on the ideXlab platform.
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parasitization of manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response
Journal of Insect Physiology, 2005Co-Authors: Kevin E Amaya, Richard Jung, Melissa Hongskula, Sassan Asgari, Nancy E BeckageAbstract:During oviposition, the parasitoid wasp Cotesia congregata injects polydnavirus, venom, and parasitoid eggs into larvae of its lepidopteran host.. the tobacco hornworm, Manduca sexta. Polydnaviruses (PDVs) suppress the immune system of the host and allow the juvenile parasitoids to develop without being encapsulated by host hemocytes mobilized by the immune system. Previous work identified a gene in the Cotesia rubecula PDV (CrV1) that is responsible for depolymerization of actin in hemocytes of the host Pieris rapae during a narrow temporal window from 4 to 8 h post-parasitization. Its expression appears temporally correlated with hemocyte dysfunction. After this time, the hemocytes recover, and encapsulation is then inhibited by other mechanism(s). In contrast, in parasitized tobacco hornworm larvae this type of inactivation in hemocytes of parasitized M. sexta larvae leads to irreversible cellular disruption. We have characterized the temporal pattern of expression of the CrV1-homolog from the C. congregata PDV in host fat body and hemocytes using Northern blots, and localized the protein in host hemocytes with polyclonal antibodies to CrV1 protein produced in P. rapae in response to expression of the CrV1 protein. Host hemocytes stained with FITC-labeled phalloidin, which binds to filamentous actin, were used to observe hemocyte disruption in parasitized and virus-injected hosts and a comparison was made to hemocytes of nonparasitized control larvae. At 24 h post-parasitization host hemocytes were significantly altered compared to those of nonparasitized larvae. Hemocytes front newly parasitized hosts displayed blebbing, inhibition of spreading and adhesion, and overall cell disruption. A CrV1-homolog gene product was localized in host hemocytes using polyclonal CrV1 antibodies, suggesting that CrV1-like gene products of C. congregata's bracovirus are responsible for the impaired immune response of the host. (C) 2005 Elsevier Ltd. All rights reserved.
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persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm manduca sexta
Journal of Insect Physiology, 2003Co-Authors: Sassan Asgari, K. Amaya, Frances F. Tan, Nancy E BeckageAbstract:The gregarious braconid wasp Cotesia congregata parasitizes host larvae of Manduca sexta, and several other sphingid species. Parasitism induces host immunosuppression due to the disruptive action of the wasp's polydnavirus (PDV) on host blood cells. During the initial stages of parasitism, these cells undergo apoptosis followed by cell clumping, which clears the hemolymph of a large number of cells. In this study, the persistence and expression of Cotesia congregata PDV (CcPDV) were examined using Southern and Northern blots, respectively. Digoxygenin-labelled total polydnaviral DNA was used to probe genomic DNA isolated from fat body and brains of hosts with emerged wasps taken 6 days following egress of the parasitoids, and significant cross-hybridization between the host fat body genomic DNA with viral DNA was seen. Thus, the virus persists in the host for the duration of parasitism, even during the post-emergence period, and may even be integrated in the host caterpillar DNA. Viral gene expression was examined using Northern blots and probes to the Cotesia rubecula CrV1 homolog, and the CrV1-like mRNAs were expressed as early as 4 h post-parasitization for at least 72 h and faint hybrization is even seen at the time the wasps eclose. In contrast, in Pieris rapae larvae the CrV1 transcript is expressed only for a brief time, during which time hemocyte function is disrupted. The effect is transitory, and hemocytes regain their normal functions after the parasites emerge as first instars.The genome of CcPDV contains one copy of the CrV1-like homolog as shown on Southern blots of viral genomic DNA. In conjunction with our earlier studies of the PDV-encoded early protein 1, the current work suggests multiple viral transcripts are produced following parasitization of the host, and likely target host hemocytes to induce their apoptosis, thereby preventing encapsulation of the parasitoid's eggs. Whether viral DNAs are integrated in the host's genomic DNA remains to be proven, but our results provide preliminary evidence that viral DNAs are detected in the host's fat body cells examined at the time of wasp emergence and several days later.
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Persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm, Manduca sexta.
Journal of Insect Physiology, 2003Co-Authors: Sassan Asgari, K. Amaya, Frances F. Tan, Nancy E BeckageAbstract:The gregarious braconid wasp Cotesia congregata parasitizes host larvae of Manduca sexta, and several other sphingid species. Parasitism induces host immunosuppression due to the disruptive action of the wasp's polydnavirus (PDV) on host blood cells. During the initial stages of parasitism, these cells undergo apoptosis followed by cell clumping, which clears the hemolymph of a large number of cells. In this study, the persistence and expression of Cotesia congregata PDV (CcPDV) were examined using Southern and Nor-them blots, respectively. Digoxygenin-labelled total polydnaviral DNA was used to probe genomic DNA isolated from fat body and brains of hosts with emerged wasps taken 6 days following egress of the parasitoids, and significant cross-hybridization between the host fat body genomic DNA with viral DNA was seen. Thus, the virus persists in the host for the duration of parasitism. even during the post-emergence period, and may even be integrated in the host caterpillar DNA. Viral gene expression was examined using Northern blots and probes to the Cotesia rubecula CrV1 homolog, and the CrV1-like mRNAs were expressed as early as 4 h post-parasitization for at least 72 h and faint hybrization is even seen at the time the wasps eclose. In contrast, in Pieris rapae larvae the CrV1 transcript is expressed only for a brief time, during which time hemocyte function is disrupted. The effect is transitory, and hemocytes regain their normal functions after the parasites emerge as first instars. The genome of CcPDV contains one copy of the CrV1-like homolog as shown on Southern blots of viral genomic DNA. In conjunction with our earlier studies of the PDV-encoded early protein 1, the current work suggests multiple viral transcripts are produced following parasitization of the host. and likely target host hemocytes to induce their apoptosis, thereby preventing encapsulation of the parasitoid's eggs. Whether viral DNAs are integrated in the host's genomic DNA remains to be proven, but our results provide preliminary evidence that viral DNAs are detected in the host's fat body cells examined at the time of wasp ernergence and several days later. (C) 2003 Elsevier Science Ltd. All rights reserved.
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Inhibition of the larval ecdysis and emergence behavior of the parasitoid Cotesia congregata by methoprene.
Journal of Insect Physiology, 2002Co-Authors: Nancy E Beckage, Regina C. Foreman, Crystal M. Palmatier, Frances F. TanAbstract:Abstract Parasitism of the tobacco hornworm, Manduca sexta, by the braconid wasp Cotesia congregata, induces developmental arrest of the host in the larval stage. During the final instar of the host, its juvenile hormone (JH) titer is elevated, preventing host metamorphosis. This study investigated the effects of hormonal manipulation of the host on the parasitoid’s emergence behavior. The second larval ecdysis of the wasps coincides with their emergence from the host, and application of the juvenile hormone analogue methoprene to day 4 fifth instar hosts either delayed or totally suppressed the subsequent emergence of the wasps. Effects of methoprene were dose-dependent and no parasitoids emerged following treatment of host larvae with doses >50 μg. Parasitoids which failed to emerge eventually succumbed as unecydsed pharate third instar larvae in the hemocoel of the host. Effects of host methoprene treatment on parasitoid metamorphosis were also assessed, and metamorphic disruption occurred at much lower dosages compared with doses necessary to suppress parasitoid emergence behavior. The inhibitory effect of methoprene on parasitoid emergence behavior appears to be mediated by effects of this hormone on the synthesis or release of ecdysis-triggering hormone (ETH) in the parasitoid, the proximate endocrine cue which triggers ecdysis behavior in free-living insects. ETH accumulated in the epitracheal Inka cells of parasitoids developing in methoprene-treated hosts, suggestive of a lack of hormone release. Thus, the hormonal modulation of parasitoid emergence behavior appears to be complex, involving a suite of hormones including JH, ecdysteroid, and peptide hormones.
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co infection of manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by autographa californica m nucleopolyhedrovirus
Journal of Insect Physiology, 2000Co-Authors: Jan O Washburn, Nancy E Beckage, Eric J Haasstapleton, Loy E VolkmanAbstract:Abstract We investigated pathogenesis of Autographa californica M Nucleopolyhedrovirus in the semipermissive host, Manduca sexta, using a lacZ recombinant virus (AcMNPV-hsp70/lacZ) to track the temporal progression of infection. Results from time course studies monitoring infections initiated orally in fourth instars demonstrated that primary infection of midgut columnar cells began at 3 h post inoculation (hpi). We observed secondary infections in midgut-associated tracheae as early as 9 hpi, showing that the early events of pathogenesis in M. sexta are similar to those of permissive noctuid larvae. In M. sexta, however, unlike in permissive hosts, hemocytes rapidly surrounded infected tracheal cells and formed capsules. Subsequently, baculovirus infections failed to spread and ultimately were cleared, suggesting that a cellular immune response had been triggered. To assess the effects of immunosuppression on baculovirus-induced disease, we compared the outcome of infections in immunocompetent hosts with those that were immunocompromised either by parasitization with the braconid, Cotesia congregata, or by injection of the parasitoid's polydnavirus. During the first 9 days after inoculation, parasitized and polydnavirus-inoculated M. sexta larvae died more quickly and at higher levels than nonparasitized and sham-injected controls, suggesting that the cellular immune response was a factor in conferring resistance to fatal infection by AcMNPV-hsp70/lacZ.
Jean-michel Drezen - One of the best experts on this subject based on the ideXlab platform.
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Cotesia congregata Bracovirus Circles Encoding PTP and Ankyrin Genes Integrate into the DNA of Parasitized Manduca sexta Hemocytes.
Journal of Virology, 2018Co-Authors: Germain Chevignon, Karine Musset, Jean-michel Drezen, Georges Periquet, Gabor Gyapay, Nathalie Vega-czarny, Elisabeth HuguetAbstract:Polydnaviruses (PDVs) are essential for the parasitism success of tens of thousands of species of parasitoid wasps. PDVs are present in wasp genomes as proviruses, which serve as the template for the production of double-stranded circular viral DNA carrying virulence genes that are injected into lepidopteran hosts. PDV circles do not contain genes coding for particle production, thereby impeding viral replication in caterpillar hosts during parasitism. Here, we investigated the fate of PDV circles of Cotesia congregata bracovirus during parasitism of the tobacco hornworm, Manduca sexta, by the wasp Cotesia congregata Sequences sharing similarities with host integration motifs (HIMs) of Microplitis demolitor bracovirus (MdBV) circles involved in integration into DNA could be identified in 12 CcBV circles, which encode PTP and VANK gene families involved in host immune disruption. A PCR approach performed on a subset of these circles indicated that they persisted in parasitized M. sexta hemocytes as linear forms, possibly integrated in host DNA. Furthermore, by using a primer extension capture method based on these HIMs and high-throughput sequencing, we could show that 8 out of 9 circles tested were integrated in M. sexta hemocyte genomic DNA and that integration had occurred specifically using the HIM, indicating that an HIM-mediated specific mechanism was involved in their integration. Investigation of BV circle insertion sites at the genome scale revealed that certain genomic regions appeared to be enriched in BV insertions, but no specific M. sexta target site could be identified.IMPORTANCE The identification of a specific and efficient integration mechanism shared by several bracovirus species opens the question of its role in braconid parasitoid wasp parasitism success. Indeed, results obtained here show massive integration of bracovirus DNA in somatic immune cells at each parasitism event of a caterpillar host. Given that bracoviruses do not replicate in infected cells, integration of viral sequences in host DNA might allow the production of PTP and VANK virulence proteins within newly dividing cells of caterpillar hosts that continue to develop during parasitism. Furthermore, this integration process could serve as a basis to understand how PDVs mediate the recently identified gene flux between parasitoid wasps and Lepidoptera and the frequency of these horizontal transfer events in nature.
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transcriptomic response of manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata
Insect Biochemistry and Molecular Biology, 2015Co-Authors: Germain Chevignon, Jean-michel Drezen, Elisabeth Huguet, Sebastien Cambier, Julie Poulain, Corinne Da Silva, Sébastien J.m. MoreauAbstract:During oviposition, Cotesia congregata parasitoid wasps inject into their host, Manduca sexta, some biological factors such as venom, ovarian fluid and a symbiotic polydnavirus (PDV) named Cotesia congregata bracovirus (CcBV). During parasitism, complex interactions occur between wasp-derived factors and host targets that lead to important modifications in host physiology. In particular, the immune response leading to wasp egg encapsulation is inhibited allowing wasp survival. To date, the regulation of host genes during the interaction had only been studied for a limited number of genes. In this study, we analysed the global impact of parasitism on host gene regulation 24 h post oviposition by high throughput 454 transcriptomic analyses of two tissues known to be involved in the host immune response (hemocytes and fat body). To identify specific effects of parasitism on host transcription at this time point, transcriptomes were obtained from non-treated and parasitized larvae, and also from larvae injected with heat-killed bacteria and double stimulated larvae that were parasitized prior to bacterial challenge. Results showed that, immune challenge by bacteria leads to induction of certain antimicrobial peptide (AMP) genes in M. sexta larvae whether they were parasitized or not prior to bacterial challenge. These results show that at 24 h post oviposition pathways leading to expression of AMP genes are not all inactivated suggesting wasps are in an antiseptic environment. In contrast, at this time point genes involved in phenoloxidase activation and cellular immune responses were globally down-regulated after parasitism in accordance with the observed inhibition of wasp egg encapsulation.
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functional annotation of Cotesia congregata bracovirus identification of viral genes expressed in parasitized host immune tissues
Journal of Virology, 2014Co-Authors: Germain Chevignon, Annie Bezier, Karine Musset, Sébastien J.m. Moreau, Julien Thézé, Jean-michel Drezen, Sebastien Cambier, Julie Poulain, Corinne Da Silva, Elisabeth HuguetAbstract: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. IMPORTANCE Bracoviruses (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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Functional annotation of Cotesia congregata bracovirus: identification of the viral genes expressed in parasitized host immune tissues.
Journal of Virology, 2014Co-Authors: Chevignon Germain, Karine Musset, Julien Thézé, Jean-michel Drezen, Sebastien Cambier, Julie Poulain, Corinne Da Silva, Bézier Annie, J.m. Sébastien Moreau, Elisabeth HuguetAbstract:Bracoviruses (BV) from 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 in the wasp genome. To date, the expression of only a few selected candidate virulence genes had 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 host allowed detection of expression of 88 CcBV genes expressed 24 h after the onset of parasitism. We could link the expression profile of these genes to several factors, showing that different regulatory mechanisms control viral gene expression in the host. These factors include 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 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.
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the bracovirus genome of the parasitoid wasp Cotesia congregata is amplified within 13 replication units including sequences not packaged in the particles
Journal of Virology, 2013Co-Authors: Faustine Louis, Annie Bezier, Jean-michel Drezen, Georges Periquet, Cristina Ferras, Catherine DupuyAbstract:The relationship between parasitoid wasps and polydnaviruses constitutes one of the few known mutualisms between viruses and eukaryotes. Viral particles are injected with the wasp eggs into parasitized larvae, and the viral genes thus introduced are used to manipulate lepidopteran host physiology. The genome packaged in the particles is composed of 35 double-stranded DNA (dsDNA) circles produced in wasp ovaries by amplification of viral sequences from proviral segments integrated in tandem arrays in the wasp genome. These segments and their flanking regions within the genome of the wasp Cotesia congregata were recently isolated, allowing extensive mapping of amplified sequences. The bracovirus DNAs packaged in the particles were found to be amplified within more than 12 replication units. Strikingly, the nudiviral cluster, the genes of which encode particle structural components, was also amplified, although not encapsidated. Amplification of bracoviral sequences was shown to involve successive head-to-head and tail-to-tail concatemers, which was not expected given the nudiviral origin of bracoviruses.
Elisabeth Huguet - One of the best experts on this subject based on the ideXlab platform.
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Cotesia congregata Bracovirus Circles Encoding PTP and Ankyrin Genes Integrate into the DNA of Parasitized Manduca sexta Hemocytes.
Journal of Virology, 2018Co-Authors: Germain Chevignon, Karine Musset, Jean-michel Drezen, Georges Periquet, Gabor Gyapay, Nathalie Vega-czarny, Elisabeth HuguetAbstract:Polydnaviruses (PDVs) are essential for the parasitism success of tens of thousands of species of parasitoid wasps. PDVs are present in wasp genomes as proviruses, which serve as the template for the production of double-stranded circular viral DNA carrying virulence genes that are injected into lepidopteran hosts. PDV circles do not contain genes coding for particle production, thereby impeding viral replication in caterpillar hosts during parasitism. Here, we investigated the fate of PDV circles of Cotesia congregata bracovirus during parasitism of the tobacco hornworm, Manduca sexta, by the wasp Cotesia congregata Sequences sharing similarities with host integration motifs (HIMs) of Microplitis demolitor bracovirus (MdBV) circles involved in integration into DNA could be identified in 12 CcBV circles, which encode PTP and VANK gene families involved in host immune disruption. A PCR approach performed on a subset of these circles indicated that they persisted in parasitized M. sexta hemocytes as linear forms, possibly integrated in host DNA. Furthermore, by using a primer extension capture method based on these HIMs and high-throughput sequencing, we could show that 8 out of 9 circles tested were integrated in M. sexta hemocyte genomic DNA and that integration had occurred specifically using the HIM, indicating that an HIM-mediated specific mechanism was involved in their integration. Investigation of BV circle insertion sites at the genome scale revealed that certain genomic regions appeared to be enriched in BV insertions, but no specific M. sexta target site could be identified.IMPORTANCE The identification of a specific and efficient integration mechanism shared by several bracovirus species opens the question of its role in braconid parasitoid wasp parasitism success. Indeed, results obtained here show massive integration of bracovirus DNA in somatic immune cells at each parasitism event of a caterpillar host. Given that bracoviruses do not replicate in infected cells, integration of viral sequences in host DNA might allow the production of PTP and VANK virulence proteins within newly dividing cells of caterpillar hosts that continue to develop during parasitism. Furthermore, this integration process could serve as a basis to understand how PDVs mediate the recently identified gene flux between parasitoid wasps and Lepidoptera and the frequency of these horizontal transfer events in nature.
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transcriptomic response of manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata
Insect Biochemistry and Molecular Biology, 2015Co-Authors: Germain Chevignon, Jean-michel Drezen, Elisabeth Huguet, Sebastien Cambier, Julie Poulain, Corinne Da Silva, Sébastien J.m. MoreauAbstract:During oviposition, Cotesia congregata parasitoid wasps inject into their host, Manduca sexta, some biological factors such as venom, ovarian fluid and a symbiotic polydnavirus (PDV) named Cotesia congregata bracovirus (CcBV). During parasitism, complex interactions occur between wasp-derived factors and host targets that lead to important modifications in host physiology. In particular, the immune response leading to wasp egg encapsulation is inhibited allowing wasp survival. To date, the regulation of host genes during the interaction had only been studied for a limited number of genes. In this study, we analysed the global impact of parasitism on host gene regulation 24 h post oviposition by high throughput 454 transcriptomic analyses of two tissues known to be involved in the host immune response (hemocytes and fat body). To identify specific effects of parasitism on host transcription at this time point, transcriptomes were obtained from non-treated and parasitized larvae, and also from larvae injected with heat-killed bacteria and double stimulated larvae that were parasitized prior to bacterial challenge. Results showed that, immune challenge by bacteria leads to induction of certain antimicrobial peptide (AMP) genes in M. sexta larvae whether they were parasitized or not prior to bacterial challenge. These results show that at 24 h post oviposition pathways leading to expression of AMP genes are not all inactivated suggesting wasps are in an antiseptic environment. In contrast, at this time point genes involved in phenoloxidase activation and cellular immune responses were globally down-regulated after parasitism in accordance with the observed inhibition of wasp egg encapsulation.
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Production of bracovirus particles by the parasitoid wasp C. congregata and hypothesis on the process leading to transfer of bracovirus sequences to lepidopteran genomes.
2015Co-Authors: Laila Gasmi, Karine Musset, Elisabeth Huguet, Helene Boulain, Jeremy Gauthier, Aurelie Hua-van, Agata K. Jakubowska, Jean-marc Aury, Anne-nathalie Volkoff, Salvador HerreroAbstract:The BV genome is integrated in the wasp genome (in grey). It is composed of proviral segments (in blue) used to produce dsDNA circles (blue circles) packaged in nucleocapsids (grey cylinders) that encode virulence genes introduced into the host (coloured rectangles) and of BV genes that are involved in particle production (grey rectangles). The latter originate from a nudivirus and encode structural proteins, they are expressed in wasp ovaries where production of bracovirus circles also occurs. Direct Repeat Junctions (DRJ, red triangles) are involved in site-specific recombination allowing circularisation of linear molecules from proviral segments. The circles thus produced are packaged in BV particles that also contain several integrase proteins. The particles are injected in the lepidopteran host during wasp oviposition. Once in the host BV particles infect many lepidopteran cell types but do not replicate. BV circles can integrate into lepidopteran host genomic DNA (in light blue) by a mechanism involving most likely an integrase and mediated by Host Integration Motifs (HIM) indicated by dark blue lines. When injected into a regular host (1) BV virulence gene (coloured squares) expression leads to modifications in lepidopteran host physiology, such as inhibition of wasp egg encapsulation and alteration of developmental programming allowing wasp larvae to complete their development safely in the host body. Hypothesis: when integration of viral circles occurs in the germline the integrated forms are not transmitted because the host dies. When bracoviruses are injected into a caterpillar, which is not a regular host species (2) or is a resistant host (interrupting oviposition, destroying wasp eggs, etc.) the integrated viral form in germline DNA can be transmitted vertically. As bracovirus genes are adapted for expression in lepidopteran cells they can be readily domesticated. Once integrated in lepidopteran genomes the bracovirus sequences undergo rearrangements. Ultimately, after several million years, only the domesticated genes remain from the original integrated circle. We propose that stinging of non-host species could be the main route for bracovirus sequence transfer to Lepidoptera. This is based on the fact that the genome of M. sexta which is the regular host of Cotesia congregata does not contain genes acquired from CcBV, conversely genes found in Spodoptera exigua, which is not a host of Cotesia congregata, are more closely related to CcBV. This figure is mostly based on the life cycle of CcBV associated with C. congregata parasitoid wasp of M. sexta, HIM motifs have been identified in the bracovirus of M. demolitor, the picture of S. exigua is shown as an example of C. congregata non-host species.
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Analysis of BEN 9 encoding insertions in the Danaina subtribe.
2015Co-Authors: Laila Gasmi, Karine Musset, Elisabeth Huguet, Helene Boulain, Jeremy Gauthier, Aurelie Hua-van, Agata K. Jakubowska, Jean-marc Aury, Anne-nathalie Volkoff, Salvador HerreroAbstract:A) Analysis of BEN9 encoding insertions in genomic DNA of individuals from different species of the Danaina subtribe by ben9 gene PCR amplification from Lepidoptera of the species Danaus chrysippus chrysippus (Oman), Danaus genutia (Thailand), Danaus plexippus (Q, caterpillar sampled in Québec, A, adults from Australia), Tirumala septentrionis septentrionis (Malaysia). C1, C2, C3: control PCR (without DNA) performed with primer pairs used respectively for D. plexippus, D. chrysippus/D. genutia and T. septentrionis PCRs B) RT-PCR analysis of Ben9 expression in D. plexippus caterpillars from Québec. Ben9 expression was detected in three individuals. No PCR amplification of Ben9 was observed on RNA samples that were not subjected to RT (No RT). C) PCR fragments obtained from D. plexippus genomic DNA and cDNA and schematic represention of Ben9 gene and D. plexippus Ben9 cDNA organization. The black bar indicates that exon 3 is not to scale. Note that in the amplified fragment corresponding to D. plexippus cDNA, the two Ben9 intron sequences have been excised as observed in Ben9 cDNA obtained from Manduca sexta parasitized by Cotesia congregata [33]. The phylogenetic tree is adapted from [34]. Dating of the common ancestor is reported from [35].
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functional annotation of Cotesia congregata bracovirus identification of viral genes expressed in parasitized host immune tissues
Journal of Virology, 2014Co-Authors: Germain Chevignon, Annie Bezier, Karine Musset, Sébastien J.m. Moreau, Julien Thézé, Jean-michel Drezen, Sebastien Cambier, Julie Poulain, Corinne Da Silva, Elisabeth HuguetAbstract: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. IMPORTANCE Bracoviruses (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.
Karen M. Kester - One of the best experts on this subject based on the ideXlab platform.
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The Parasitic Wasp, Cotesia congregata (Say), Consists of Two Incipient Species Isolated by Asymmetric Reproductive Incompatibility and Hybrid Inability to Overcome Host Defenses
Frontiers in Ecology and Evolution, 2019Co-Authors: Justin P. Bredlau, Daniel Kuhar, Dawn E. Gundersen-rindal, Karen M. KesterAbstract:Parasitic wasps are highly diverse and play a major role in suppression of herbivorous insect pest populations. Several previously identified species of parasitic wasps have been found to be complexes of cryptic species resulting from adaptations to specific hosts or host foodplants. Cotesia congregata (Say) (Hymenoptera: Braconidae), which has long served as a model system for host-parasitoid interactions, can be used for investigating the process of diversification among sympatric populations that differ in host and host foodplant usage. Two incipient species of C. congregata have been identified in the USA mid-Atlantic region, “MsT wasps” originate from Manduca sexta (L.) (Lepidoptera: Sphingidae) on tobacco and “CcC wasps” originate from Ceratomia catalpae (Boisduval) (Lepidoptera: Sphingidae) on catalpa. Both wasp sources can develop in either host species. Hybrids resulting from MsT♂xCcC♀ crosses are fertile, whereas hybrids from CcC♂xMsT♀ crosses are typically sterile. In this study, we compared relative expression in vivo of seven C. congregata bracovirus (CcBV) genes among MsT and CcC parental and hybrid crosses. Also, we established hybrid crosses between MsT and CcC wasps and four additional host foodplant sources of C. congregata. Patterns of relative expression in vivo of MsT and CcC CcBV genes differed; a few were not expressed in hosts parasitized by CcC wasps. Overall, relative expression of CcBV genes from MsT and CcC wasps did not differ with respect to the host species parasitized. Low or absent expression of CcBV genes was found in hosts parasitized by sterile hybrids. For the most part, the other four host-foodplant wasp sources were reproductively compatible with either MsT or CcC wasps and hybrid crosses with the alternative wasp source were asymmetrically sterile. Crosses involving CcC males or MsT females produced sterile hybrids that lacked mature ovaries. Cumulatively, results indicate that C. congregata is composed of two sympatric incipient species that can utilize multiple host species rather than several host-associated races or cryptic species.
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Duration (ms; mean ± SE) of male courtship song elements among species of Cotesia.
2019Co-Authors: Justin P. Bredlau, Karen M. KesterAbstract:Cotesia congregata is divided by host-foodplant complex. N = number of individual wasps analyzed.
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Fundamental frequency (Hz; mean ± SE) of male courtship song elements among species of Cotesia.
2019Co-Authors: Justin P. Bredlau, Karen M. KesterAbstract:Cotesia congregata is divided by host-foodplant complex. N = number of individual wasps analyzed.
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Scatterplots of factors of a principal components analysis of seven Cotesia courtship song elements.
2019Co-Authors: Justin P. Bredlau, Karen M. KesterAbstract:(A) PC1 vs. PC2, (B) PC1 vs PC3, (C) PC3 vs PC2. Each data point represents a single individual coded by species. (D) 3-dimensional plot of the mean PC of each species color-coded by dominant courtship song pattern (red—rapid pulses; green—pulse-buzz; blue—long pauses; orange—long buzz-pulse). Letter codes indicate species name. Cotesia congregata is represented by the MsT host-foodplant complex. Some species are separated from the others by one or more PCs; most species form a close cluster with some overlap.
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Cotesia species collected, host-foodplant complex (for C. congregata), lepidopteran host names, collection locations (county/city, state; lat, long, datum: WGS84), and number of wasp broods collected at each site.
2019Co-Authors: Justin P. Bredlau, Karen M. KesterAbstract:Cotesia congregata is divided into six host-foodplant complexes (H-FPC) abbreviated by host species and plant name (tobacco, catalpa, holly/pawpaw, Virginia creeper, and privet, respectively).
Georges Periquet - One of the best experts on this subject based on the ideXlab platform.
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Cotesia congregata Bracovirus Circles Encoding PTP and Ankyrin Genes Integrate into the DNA of Parasitized Manduca sexta Hemocytes.
Journal of Virology, 2018Co-Authors: Germain Chevignon, Karine Musset, Jean-michel Drezen, Georges Periquet, Gabor Gyapay, Nathalie Vega-czarny, Elisabeth HuguetAbstract:Polydnaviruses (PDVs) are essential for the parasitism success of tens of thousands of species of parasitoid wasps. PDVs are present in wasp genomes as proviruses, which serve as the template for the production of double-stranded circular viral DNA carrying virulence genes that are injected into lepidopteran hosts. PDV circles do not contain genes coding for particle production, thereby impeding viral replication in caterpillar hosts during parasitism. Here, we investigated the fate of PDV circles of Cotesia congregata bracovirus during parasitism of the tobacco hornworm, Manduca sexta, by the wasp Cotesia congregata Sequences sharing similarities with host integration motifs (HIMs) of Microplitis demolitor bracovirus (MdBV) circles involved in integration into DNA could be identified in 12 CcBV circles, which encode PTP and VANK gene families involved in host immune disruption. A PCR approach performed on a subset of these circles indicated that they persisted in parasitized M. sexta hemocytes as linear forms, possibly integrated in host DNA. Furthermore, by using a primer extension capture method based on these HIMs and high-throughput sequencing, we could show that 8 out of 9 circles tested were integrated in M. sexta hemocyte genomic DNA and that integration had occurred specifically using the HIM, indicating that an HIM-mediated specific mechanism was involved in their integration. Investigation of BV circle insertion sites at the genome scale revealed that certain genomic regions appeared to be enriched in BV insertions, but no specific M. sexta target site could be identified.IMPORTANCE The identification of a specific and efficient integration mechanism shared by several bracovirus species opens the question of its role in braconid parasitoid wasp parasitism success. Indeed, results obtained here show massive integration of bracovirus DNA in somatic immune cells at each parasitism event of a caterpillar host. Given that bracoviruses do not replicate in infected cells, integration of viral sequences in host DNA might allow the production of PTP and VANK virulence proteins within newly dividing cells of caterpillar hosts that continue to develop during parasitism. Furthermore, this integration process could serve as a basis to understand how PDVs mediate the recently identified gene flux between parasitoid wasps and Lepidoptera and the frequency of these horizontal transfer events in nature.
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functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata insights into the evolutionary dynamics of bracoviruses
Philosophical Transactions of the Royal Society B, 2013Co-Authors: Annie Bezier, Karine Musset, Julien Thézé, Jérôme Lesobre, Georges Periquet, Gabor Gyapay, Faustine Louis, Severine Jancek, Patricia Lenoble, Catherine DupuyAbstract:Bracoviruses 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 encapsidate multiple dsDNA circles 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 different wasp genomes showed the orthology of the proviral macrolocus across different species. The nudiviral gene odv-e66-like1 is conserved within the macrolocus, 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 bracovirus genome of the parasitoid wasp Cotesia congregata is amplified within 13 replication units including sequences not packaged in the particles
Journal of Virology, 2013Co-Authors: Faustine Louis, Annie Bezier, Jean-michel Drezen, Georges Periquet, Cristina Ferras, Catherine DupuyAbstract:The relationship between parasitoid wasps and polydnaviruses constitutes one of the few known mutualisms between viruses and eukaryotes. Viral particles are injected with the wasp eggs into parasitized larvae, and the viral genes thus introduced are used to manipulate lepidopteran host physiology. The genome packaged in the particles is composed of 35 double-stranded DNA (dsDNA) circles produced in wasp ovaries by amplification of viral sequences from proviral segments integrated in tandem arrays in the wasp genome. These segments and their flanking regions within the genome of the wasp Cotesia congregata were recently isolated, allowing extensive mapping of amplified sequences. The bracovirus DNAs packaged in the particles were found to be amplified within more than 12 replication units. Strikingly, the nudiviral cluster, the genes of which encode particle structural components, was also amplified, although not encapsidated. Amplification of bracoviral sequences was shown to involve successive head-to-head and tail-to-tail concatemers, which was not expected given the nudiviral origin of bracoviruses.
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Journal of General Virology (1997), 78, 3125–3134. Printed in Great Britain
2013Co-Authors: Ste Phane Savary, N Beckage, Georges Periquet, Frances Tan, Jean-michel DrezenAbstract:Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastinae) at potential recombinase binding site
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the few virus like genes of Cotesia congregata bracovirus
Archives of Insect Biochemistry and Physiology, 2006Co-Authors: Jean-michel Drezen, Annie Bezier, Elisabeth Huguet, Jérôme Lesobre, L. Cattolico, Georges Periquet, Catherine DupuyAbstract:The origin of the symbiotic association between parasitoid wasps and bracoviruses is still unknown. From phylogenetic analyses, bracovirus-associated wasp species constitute a monophyletic group, the microgastroid complex. Thus all wasp–bracovirus associations could have originated from the integration of an ancestral virus in the genome of the ancestor of the microgastroids. In an effort to identify a set of virus genes that would give clues on the nature of the ancestral virus, we have recently performed the complete sequencing of the genome of CcBV, the bracovirus of the wasp Cotesia congregata. We describe here the putative proteins encoded by CcBV genome having significant similarities with sequences from known viruses and mobile elements. The analysis of CcBV gene content does not lend support to the hypothesis that bracoviruses originated from a baculovirus. Moreover, no consistent homology was found between CcBV genes and any set of genes constituting the core genome of a known free-living virus. We discuss the significance of the scarce homology found between proteins from CcBV and other viruses or mobile elements. Arch. Insect Biochem. Physiol. 61:110–122, 2006. © 2006 Wiley-Liss, Inc.
