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1. Identification of a viral gene essential for the genome replication of a domesticated endogenous virus in ichneumonid parasitoid wasps.

Author: Ange Lorenzi, Fabrice Legeai, Véronique Jouan, Pierre-Alain Girard, Michael R Strand, Marc Ravallec, Magali Eychenne, Anthony Bretaudeau, Stéphanie Robin, Jeanne Rochefort, Mathilde Villegas, Gaelen R Burke, Rita Rebollo, Nicolas Nègre, and Anne-Nathalie Volkoff
Subjects: Immunologic diseases. Allergy, RC581-607, Biology (General), QH301-705.5
Abstract: Thousands of endoparasitoid wasp species in the families Braconidae and Ichneumonidae harbor "domesticated endogenous viruses" (DEVs) in their genomes. This study focuses on ichneumonid DEVs, named ichnoviruses (IVs). Large quantities of DNA-containing IV virions are produced in ovary calyx cells during the pupal and adult stages of female wasps. Females parasitize host insects by injecting eggs and virions into the body cavity. After injection, virions rapidly infect host cells which is followed by expression of IV genes that promote the successful development of wasp offspring. IV genomes consist of two components: proviral segment loci that serve as templates for circular dsDNAs that are packaged into capsids, and genes from an ancestral virus that produce virions. In this study, we generated a chromosome-scale genome assembly for Hyposoter didymator that harbors H. didymator ichnovirus (HdIV). We identified a total of 67 HdIV loci that are amplified in calyx cells during the wasp pupal stage. We then focused on an HdIV gene, U16, which is transcribed in calyx cells during the initial stages of replication. Sequence analysis indicated that U16 contains a conserved domain in primases from select other viruses. Knockdown of U16 by RNA interference inhibited virion morphogenesis in calyx cells. Genome-wide analysis indicated U16 knockdown also inhibited amplification of HdIV loci in calyx cells. Altogether, our results identified several previously unknown HdIV loci, demonstrated that all HdIV loci are amplified in calyx cells during the pupal stage, and showed that U16 is required for amplification and virion morphogenesis.
Published: 2024
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2. Progeny fitness determines the performance of the parasitoid Therophilus javanus, a prospective biocontrol agent against the legume pod borer

Author: Djibril Aboubakar Souna, Aimé Hippolyte Bokonon-Ganta, Marc Ravallec, Mesmin Alizannon, Ramasamy Srinivasan, Barry Robert Pittendrigh, Anne-Nathalie Volkoff, and Manuele Tamò
Subjects: Medicine, Science
Abstract: Abstract Therophilus javanus (Bhat & Gupta) is an exotic larval endoparasitoid newly imported from Asia into Africa as a classical biological control agent against the pod borer Maruca vitrata (Fabricius). The parasitoid preference for the five larval instars of M. vitrata and their influence on progeny sex ratio were assessed together with the impact of larval host age at the time of oviposition on development time, mother longevity and offspring production. In a choice situation, female parasitoids preferred to oviposit in the first three larval instars. The development of immature stages of the parasitoid was observed inside three-day-old hosts, whereby the first two larval instars of T. javanus completed their development as endoparasites and the third larval instar as ectoparasite. The development time was faster when first larval instars (two- and three-day-old) of the host caterpillars were parasitized compared to second larval instar (four-day-old). The highest proportion of daughters (0.51) was observed when females were provided with four-day-old hosts. The lowest intrinsic rate of increase (r) (0.21 ± 0.01), the lowest rate of increase (λ) (1.23 ± 0.01), and the lowest net reproductive rate (Ro) (35.93 ± 6.51) were recorded on four-day-old hosts. These results are discussed in the light of optimizing mass rearing and release strategies.
Published: 2021
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3. Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps

Author: Fabrice Legeai, Bernardo F. Santos, Stéphanie Robin, Anthony Bretaudeau, Rebecca B. Dikow, Claire Lemaitre, Véronique Jouan, Marc Ravallec, Jean-Michel Drezen, Denis Tagu, Frédéric Baudat, Gabor Gyapay, Xin Zhou, Shanlin Liu, Bruce A. Webb, Seán G. Brady, and Anne-Nathalie Volkoff
Subjects: Endogenous virus architecture, Polydnavirus, Parasitoid wasp, Koinobiont, Campopleginae, IVSPERs, Biology (General), QH301-705.5
Abstract: Abstract Background Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. PDVs include the ichnoviruses and bracoviruses that originate from independent viral acquisitions in ichneumonid and braconid wasps respectively. PDV genomes are fully incorporated into the wasp genomes and consist of (1) genes involved in viral particle production, which derive from the viral ancestor and are not encapsidated, and (2) proviral segments harboring virulence genes, which are packaged into the viral particle. To help elucidating the mechanisms that have facilitated viral domestication in ichneumonid wasps, we analyzed the structure of the viral insertions by sequencing the whole genome of two ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Results Assemblies with long scaffold sizes allowed us to unravel the organization of the endogenous ichnovirus and revealed considerable dispersion of the viral loci within the wasp genomes. Proviral segments contained species-specific sets of genes and occupied distinct genomic locations in the two ichneumonid wasps. In contrast, viral machinery genes were organized in clusters showing highly conserved gene content and order, with some loci located in collinear wasp genomic regions. This genomic architecture clearly differs from the organization of PDVs in braconid wasps, in which proviral segments are clustered and viral machinery elements are more dispersed. Conclusions The contrasting structures of the two types of ichnovirus genomic elements are consistent with their different functions: proviral segments are vehicles for virulence proteins expected to adapt according to different host defense systems, whereas the genes involved in virus particle production in the wasp are likely more stable and may reflect ancestral viral architecture. The distinct genomic architectures seen in ichnoviruses versus bracoviruses reveal different evolutionary trajectories that have led to virus domestication in the two wasp lineages.
Published: 2020
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4. RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps.

Author: Ange Lorenzi, Marc Ravallec, Magali Eychenne, Véronique Jouan, Stéphanie Robin, Isabelle Darboux, Fabrice Legeai, Anne-Sophie Gosselin-Grenet, Mathieu Sicard, Don Stoltz, and Anne-Nathalie Volkoff
Subjects: Immunologic diseases. Allergy, RC581-607, Biology (General), QH301-705.5
Abstract: There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a 'virulence gene delivery vehicle' that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals.
Published: 2019
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5. Venom Atypical Extracellular Vesicles as Interspecies Vehicles of Virulence Factors Involved in Host Specificity: The Case of a Drosophila Parasitoid Wasp

Author: Bin Wan, Emilie Goguet, Marc Ravallec, Olivier Pierre, Séverine Lemauf, Anne-Nathalie Volkoff, Jean-Luc Gatti, and Marylène Poirié
Subjects: Drosophila, immunity, parasitoid wasp, Leptopilina, venosomes, lamellocyte, Immunologic diseases. Allergy, RC581-607
Abstract: Endoparasitoid wasps, which lay eggs inside the bodies of other insects, use various strategies to protect their offspring from the host immune response. The hymenopteran species of the genus Leptopilina, parasites of Drosophila, rely on the injection of a venom which contains proteins and peculiar vesicles (hereafter venosomes). We show here that the injection of purified L. boulardi venosomes is sufficient to impair the function of the Drosophila melanogaster lamellocytes, a hemocyte type specialized in the defense against wasp eggs, and thus the parasitic success of the wasp. These venosomes seem to have a unique extracellular biogenesis in the wasp venom apparatus where they acquire specific secreted proteins/virulence factors and act as a transport system to deliver these compounds into host lamellocytes. The level of venosomes entry into lamellocytes of different Drosophila species was correlated with the rate of parasitism success of the wasp, suggesting that this venosome-cell interaction may represent a new evolutionary level of host-parasitoid specificity.
Published: 2019
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6. Proteo-Trancriptomic Analyses Reveal a Large Expansion of Metalloprotease-Like Proteins in Atypical Venom Vesicles of the Wasp Meteorus pulchricornis (Braconidae)

Author: Jean-Luc Gatti, Maya Belghazi, Fabrice Legeai, Marc Ravallec, Marie Frayssinet, Stéphanie Robin, Djibril Aboubakar-Souna, Ramasamy Srinivasan, Manuele Tamò, Marylène Poirié, and Anne-Nathalie Volkoff
Subjects: Meteorus pulchricornis, parasitoid wasp, Braconidae, venomics, virus-like particles (VLPs), proteomic, Medicine
Abstract: Meteorus pulchricornis (Ichneumonoidea, Braconidae) is an endoparasitoid wasp of lepidopteran caterpillars. Its parasitic success relies on vesicles (named M. pulchricornis Virus-Like Particles or MpVLPs) that are synthesized in the venom gland and injected into the parasitoid host along with the venom during oviposition. In order to define the content and understand the biogenesis of these atypical vesicles, we performed a transcriptome analysis of the venom gland and a proteomic analysis of the venom and purified MpVLPs. About half of the MpVLPs and soluble venom proteins identified were unknown and no similarity with any known viral sequence was found. However, MpVLPs contained a large number of proteins labelled as metalloproteinases while the most abundant protein family in the soluble venom was that of proteins containing the Domain of Unknown Function DUF-4803. The high number of these proteins identified suggests that a large expansion of these two protein families occurred in M. pulchricornis. Therefore, although the exact mechanism of MpVLPs formation remains to be elucidated, these vesicles appear to be “metalloproteinase bombs” that may have several physiological roles in the host including modifying the functions of its immune cells. The role of DUF4803 proteins, also present in the venom of other braconids, remains to be clarified.
Published: 2021
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7. Interaction of a Densovirus with Glycans of the Peritrophic Matrix Mediates Oral Infection of the Lepidopteran Pest Spodoptera frugiperda

Author: Laetitia Pigeyre, Malvina Schatz, Marc Ravallec, Leila Gasmi, Nicolas Nègre, Cécile Clouet, Martial Seveno, Khadija El Koulali, Mathilde Decourcelle, Yann Guerardel, Didier Cot, Thierry Dupressoir, Anne-Sophie Gosselin-Grenet, and Mylène Ogliastro
Subjects: insect, Lepidoptera, insect parvovirus, chitin, peritrophins, glycans, biocontrol, Microbiology, QR1-502
Abstract: The success of oral infection by viruses depends on their capacity to overcome the gut epithelial barrier of their host to crossing over apical, mucous extracellular matrices. As orally transmitted viruses, densoviruses, are also challenged by the complexity of the insect gut barriers, more specifically by the chitinous peritrophic matrix, that lines and protects the midgut epithelium; how capsids stick to and cross these barriers to reach their final cell destination where replication goes has been poorly studied in insects. Here, we analyzed the early interaction of the Junonia coenia densovirus (JcDV) with the midgut barriers of caterpillars from the pest Spodoptera frugiperda. Using combination of imaging, biochemical, proteomic and transcriptomic analyses, we examined in vitro, ex vivo and in vivo the early interaction of the capsids with the peritrophic matrix and the consequence of early oral infection on the overall gut function. We show that the JcDV particle rapidly adheres to the peritrophic matrix through interaction with different glycans including chitin and glycoproteins, and that these interactions are necessary for oral infection. Proteomic analyses of JcDV binding proteins of the peritrophic matrix revealed mucins and non-mucins proteins including enzymes already known to act as receptors for several insect pathogens. In addition, we show that JcDV early infection results in an arrest of N-Acetylglucosamine secretion and a disruption in the integrity of the peritrophic matrix, which may help viral particles to pass through. Finally, JcDV early infection induces changes in midgut genes expression favoring an increased metabolism including an increased translational activity. These dysregulations probably participate to the overall dysfunction of the gut barrier in the early steps of viral pathogenesis. A better understanding of early steps of densovirus infection process is crucial to build biocontrol strategies against major insect pests.
Published: 2019
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8. An Insight in the Reproductive Biology of Therophilus javanus (Hymenoptera, Braconidae, and Agathidinae), a Potential Biological Control Agent against the Legume Pod Borer (Lepidoptera, Crambidae)

Author: Djibril Aboubakar Souna, Aimé Bokonon-Ganta, Marc Ravallec, Antonino Cusumano, Barry Robert Pittendrigh, Anne-Nathalie Volkoff, and Manuele Tamò
Subjects: Zoology, QL1-991
Abstract: Therophilus javanus is a koinobiont, solitary larval endoparasitoid currently being considered as a biological control agent against the pod borer Maruca vitrata, a devastating cowpea pest causing 20–80% crop losses in West Africa. We investigated ovary morphology and anatomy, oogenesis, potential fecundity, and egg load in T. javanus, as well as the effect of factors such as age of the female and parasitoid/host size at oviposition on egg load. The number of ovarioles was found to be variable and significantly influenced by the age/size of the M. vitrata caterpillar when parasitized. Egg load also was strongly influenced by both the instar of M. vitrata caterpillar at the moment of parasitism and wasp age. The practical implications of these findings for improving mass rearing of the parasitoid toward successful biological control of M. vitrata are discussed.
Published: 2017
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9. The cellular immune response of the pea aphid to foreign intrusion and symbiotic challenge.

Author: Antonin Schmitz, Caroline Anselme, Marc Ravallec, Christian Rebuf, Jean-Christophe Simon, Jean-Luc Gatti, and Marylène Poirié
Subjects: Medicine, Science
Abstract: Recent studies suggest that the pea aphid (Acyrthosiphon pisum) has low immune defenses. However, its immune components are largely undescribed, and notably, extensive characterization of circulating cells has been missing. Here, we report characterization of five cell categories in hemolymph of adults of the LL01 pea aphid clone, devoid of secondary symbionts (SS): prohemocytes, plasmatocytes, granulocytes, spherulocytes and wax cells. Circulating lipid-filed wax cells are rare; they otherwise localize at the basis of the cornicles. Spherulocytes, that are likely sub-cuticular sessile cells, are involved in the coagulation process. Prohemocytes have features of precursor cells. Plasmatocytes and granulocytes, the only adherent cells, can form a layer in vivo around inserted foreign objects and phagocytize latex beads or Escherichia coli bacteria injected into aphid hemolymph. Using digital image analysis, we estimated that the hemolymph from one LL01 aphid contains about 600 adherent cells, 35% being granulocytes. Among aphid YR2 lines differing only in their SS content, similar results to LL01 were observed for YR2-Amp (without SS) and YR2-Ss (with Serratia symbiotica), while YR2-Hd (with Hamiltonella defensa) and YR2(Ri) (with Regiella insecticola) had strikingly lower adherent hemocyte numbers and granulocyte proportions. The effect of the presence of SS on A. pisum cellular immunity is thus symbiont-dependent. Interestingly, Buchnera aphidicola (the aphid primary symbiont) and all SS, whether naturally present, released during hemolymph collection, or artificially injected, were internalized by adherent hemocytes. Inside hemocytes, SS were observed in phagocytic vesicles, most often in phagolysosomes. Our results thus raise the question whether aphid symbionts in hemolymph are taken up and destroyed by hemocytes, or actively promote their own internalization, for instance as a way of being transmitted to the next generation. Altogether, we demonstrate here a strong interaction between aphid symbionts and immune cells, depending upon the symbiont, highlighting the link between immunity and symbiosis.
Published: 2012
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10. Viruses associated with ovarian degeneration in Apis mellifera L. queens.

Author: Laurent Gauthier, Marc Ravallec, Magali Tournaire, François Cousserans, Max Bergoin, Benjamin Dainat, and Joachim R de Miranda
Subjects: Medicine, Science
Abstract: Queen fecundity is a critical issue for the health of honeybee (Apis mellifera L.) colonies, as she is the only reproductive female in the colony and responsible for the constant renewal of the worker bee population. Any factor affecting the queen's fecundity will stagnate colony development, increasing its susceptibility to opportunistic pathogens. We discovered a pathology affecting the ovaries, characterized by a yellow discoloration concentrated in the apex of the ovaries resulting from degenerative lesions in the follicles. In extreme cases, marked by intense discoloration, the majority of the ovarioles were affected and these cases were universally associated with egg-laying deficiencies in the queens. Microscopic examination of the degenerated follicles showed extensive paracrystal lattices of 30 nm icosahedral viral particles. A cDNA library from degenerated ovaries contained a high frequency of deformed wing virus (DWV) and Varroa destructor virus 1 (VDV-1) sequences, two common and closely related honeybee Iflaviruses. These could also be identified by in situ hybridization in various parts of the ovary. A large-scale survey for 10 distinct honeybee viruses showed that DWV and VDV-1 were by far the most prevalent honeybee viruses in queen populations, with distinctly higher prevalence in mated queens (100% and 67%, respectively for DWV and VDV-1) than in virgin queens (37% and 0%, respectively). Since very high viral titres could be recorded in the ovaries and abdomens of both functional and deficient queens, no significant correlation could be made between viral titre and ovarian degeneration or egg-laying deficiency among the wider population of queens. Although our data suggest that DWV and VDV-1 have a role in extreme cases of ovarian degeneration, infection of the ovaries by these viruses does not necessarily result in ovarian degeneration, even at high titres, and additional factors are likely to be involved in this pathology.
Published: 2011
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11. Multigenic families in Ichnovirus: a tissue and host specificity study through expression analysis of vankyrins from Hyposoter didymator Ichnovirus.

Author: Gabriel Clavijo, Tristan Dorémus, Marc Ravallec, Marie-Anne Mannucci, Véronique Jouan, Anne-Nathalie Volkoff, and Isabelle Darboux
Subjects: Medicine, Science
Abstract: The viral ankyrin (vankyrin) gene family is represented in all polydnavirus (PDVs) genomes and encodes proteins homologous to I-kappaBs, inhibitors of NF-kappaB transcription factors. The structural similarities led to the hypothesis that vankyrins mimic eukaryotic factors to subvert important physiological pathways in the infected host. Here, we identified nine vankyrin genes in the genome of the Hyposoter didymator Ichnovirus (HdIV). Time-course gene expression experiments indicate that all members are expressed throughout parasitism of Spodoptera frugiperda, as assessed using RNA extracted from whole larvae. To study tissue and/or species specificity transcriptions, the expression of HdIV vankyrin genes were compared between HdIV-injected larvae of S. frugiperda and S. littoralis. The transcriptional profiles were similar in the two species, including the largely predominant expression of Hd27-vank1 in all tissues examined. However, in various insect cell lines, the expression patterns of HdIV vankyrins differed according to species. No clear relationship between vankyrin expression patterns and abundance of vankyrin-bearing genomic segments were found in the lepidopteran cell lines. Moreover, in these cells, the amount of vankyrin-bearing genomic segments differed substantially between cytosol and nuclei of infected cells, implying the existence of an unexpected step regulating the copy number of HdIV segments in cell nuclei. Our in vitro results reveal a host-specific transcriptional profile of vankyrins that may be related to the success of parasitism in different hosts. In Spodoptera hosts, the predominant expression of Hd27-vank1 suggests that this protein might have pleiotropic functions during parasitism of these insect species.
Published: 2011
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12. Progeny fitness determines the performance of the parasitoid Therophilus javanus, a prospective biocontrol agent against the legume pod borer

Author: Barry R. Pittendrigh, Ramasamy Srinivasan, Manuele Tamò, Aimé H. Bokonon-Ganta, Djibril Aboubakar Souna, Mesmin Alizannon, Anne-Nathalie Volkoff, Marc Ravallec, International Institute of Tropical Agriculture [Nigeria] (IITA), Consultative Group on International Agricultural Research [CGIAR] (CGIAR), Université d’Abomey-Calavi (UAC), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), World Vegetable Center, Michigan State University [East Lansing], Michigan State University System, International Institute of Tropical Agriculture (IITA-Benin), Consultative Group on International Agricultural Research [CGIAR] (CGIAR)-Consultative Group on International Agricultural Research [CGIAR] (CGIAR), Cooperation and Cultural Action Service (SCAC) of the French Embassy in Cotonou N 898392E, CGIAR, and Bill & Melinda Gates Foundation OPP1082463
Subjects: Male, 0106 biological sciences, Behavioural ecology, Ecophysiology, Science, [SDV]Life Sciences [q-bio], Wasps, Biological pest control, Moths, 010603 evolutionary biology, 01 natural sciences, Article, Parasitoid, Toxicology, Animals, Population dynamics, Pest Control, Biological, Larva, Multidisciplinary, biology, Host (biology), Reproduction, fungi, biology.organism_classification, 010602 entomology, Maruca vitrata, Medicine, Instar, Female, Agroecology, Sex ratio
Abstract: Therophilus javanus (Bhat & Gupta) is an exotic larval endoparasitoid newly imported from Asia into Africa as a classical biological control agent against the pod borer Maruca vitrata (Fabricius). The parasitoid preference for the five larval instars of M. vitrata and their influence on progeny sex ratio were assessed together with the impact of larval host age at the time of oviposition on development time, mother longevity and offspring production. In a choice situation, female parasitoids preferred to oviposit in the first three larval instars. The development of immature stages of the parasitoid was observed inside three-day-old hosts, whereby the first two larval instars of T. javanus completed their development as endoparasites and the third larval instar as ectoparasite. The development time was faster when first larval instars (two- and three-day-old) of the host caterpillars were parasitized compared to second larval instar (four-day-old). The highest proportion of daughters (0.51) was observed when females were provided with four-day-old hosts. The lowest intrinsic rate of increase (r) (0.21 ± 0.01), the lowest rate of increase (λ) (1.23 ± 0.01), and the lowest net reproductive rate (Ro) (35.93 ± 6.51) were recorded on four-day-old hosts. These results are discussed in the light of optimizing mass rearing and release strategies.
Published: 2021
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13. Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps

Author: Gabor Gyapay, Claire Lemaitre, Seán G. Brady, Frédéric Baudat, Denis Tagu, Anne-Nathalie Volkoff, Fabrice Legeai, Anthony Bretaudeau, Rebecca B. Dikow, Xin Zhou, Marc Ravallec, Stéphanie Robin, Jean-Michel Drezen, Bernardo F. Santos, Shanlin Liu, Véronique Jouan, Bruce A. Webb, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Smithsonian Institution, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Institut de génétique humaine (IGH), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), School of Earth and Space Sciences, Peking University [Beijing], China Agricultural University Library, Beijing Genomics Institute [Shenzhen] (BGI), University of Kentucky (UK), AIPINRA project (GenomeInsect, AIP BIORESSOURCES 2012), Sackler Institute of Comparative Genomics (AMNH), ANR-12-ADAP-0001,ABC - PaPoGen,Adaptation en lutte biologique - Génomique des populations de parasitoïdes(2012), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, University of Kentucky, and Université de Tours-Centre National de la Recherche Scientifique (CNRS)
Subjects: 0106 biological sciences, food.ingredient, IVSPERs, Physiology, Endogenous virus architecture, Koinobiont, [SDV]Life Sciences [q-bio], Wasps, Plant Science, Genome, Viral, macromolecular substances, 010603 evolutionary biology, 01 natural sciences, Genome, Campopleginae, General Biochemistry, Genetics and Molecular Biology, Parasitoid, Parasitoid wasp, Evolution, Molecular, 03 medical and health sciences, food, Species Specificity, Structural Biology, Polydnavirus, Animals, lcsh:QH301-705.5, Gene, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, 0303 health sciences, biology, Host Microbial Interactions, Whole Genome Sequencing, Host (biology), Cell Biology, biology.organism_classification, lcsh:Biology (General), Evolutionary biology, Polydnaviridae, Ichnovirus, General Agricultural and Biological Sciences, Bracovirus, Developmental Biology, Biotechnology, Research Article
Abstract: Background Polydnaviruses (PDVs) are mutualistic endogenous viruses inoculated by some lineages of parasitoid wasps into their hosts, where they facilitate successful wasp development. PDVs include the ichnoviruses and bracoviruses that originate from independent viral acquisitions in ichneumonid and braconid wasps respectively. PDV genomes are fully incorporated into the wasp genomes and consist of (1) genes involved in viral particle production, which derive from the viral ancestor and are not encapsidated, and (2) proviral segments harboring virulence genes, which are packaged into the viral particle. To help elucidating the mechanisms that have facilitated viral domestication in ichneumonid wasps, we analyzed the structure of the viral insertions by sequencing the whole genome of two ichnovirus-carrying wasp species, Hyposoter didymator and Campoletis sonorensis. Results Assemblies with long scaffold sizes allowed us to unravel the organization of the endogenous ichnovirus and revealed considerable dispersion of the viral loci within the wasp genomes. Proviral segments contained species-specific sets of genes and occupied distinct genomic locations in the two ichneumonid wasps. In contrast, viral machinery genes were organized in clusters showing highly conserved gene content and order, with some loci located in collinear wasp genomic regions. This genomic architecture clearly differs from the organization of PDVs in braconid wasps, in which proviral segments are clustered and viral machinery elements are more dispersed. Conclusions The contrasting structures of the two types of ichnovirus genomic elements are consistent with their different functions: proviral segments are vehicles for virulence proteins expected to adapt according to different host defense systems, whereas the genes involved in virus particle production in the wasp are likely more stable and may reflect ancestral viral architecture. The distinct genomic architectures seen in ichnoviruses versus bracoviruses reveal different evolutionary trajectories that have led to virus domestication in the two wasp lineages.
Published: 2020
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14. A behavior-manipulating virus relative as a source of adaptive genes for Drosophila parasitoids

Author: Benjamin Guinet, David Lepetit, Julien Varaldi, Bastien Bennetot, Yohann Couté, Olivier Bouchez, Deborah Di Giovanni, Matthieu Boulesteix, Marc Ravallec, Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Ecologie Systématique et Evolution (ESE), AgroParisTech-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Eléments transposables, évolution, populations, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Laboratoire de Biologie à Grande Échelle (BGE - UMR S1038), Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Grenoble Alpes (UGA), Etude de la dynamique des protéomes (EDyP ), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Grenoble Alpes (UGA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Génome et Transcriptome - Plateforme Génomique ( GeT-PlaGe), Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Génétique et évolution des interactions hôtes-parasites, ANR-11-LABX-0048,ECOFECT,Dynamiques eco-évolutives des maladies infectieuses(2011), ANR-10-INBS-0006,HIDDEN,Extension de l'infrastructure de recherche dédiée aux maladies hautement infectieuses(2010), ANR-11-JSV7-0011,viromics,Distribution et impact des virus héritables dans une communauté hôtes-parasitoïdes(2011), Couté, Yohann, Dynamiques eco-évolutives des maladies infectieuses - - ECOFECT2011 - ANR-11-LABX-0048 - LABX - VALID, Extension de l'infrastructure de recherche dédiée aux maladies hautement infectieuses - - HIDDEN2010 - ANR-10-INBS-0006 - INBS - VALID, Jeunes Chercheuses et Jeunes Chercheurs - Distribution et impact des virus héritables dans une communauté hôtes-parasitoïdes - - viromics2011 - ANR-11-JSV7-0011 - JCJC - VALID, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), and Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Subjects: 0106 biological sciences, Gene Transfer, Horizontal, Genes, Viral, Genome, Insect, Wasps, Adaptation, Biological, Superparasitism, Hymenoptera, [SDV.GEN.GA] Life Sciences [q-bio]/Genetics/Animal genetics, Leptopilina, 010603 evolutionary biology, 01 natural sciences, Parasitoid, Domestication, 03 medical and health sciences, Genetics, [SDV.BID.EVO] Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Animals, [SDV.MP.PAR]Life Sciences [q-bio]/Microbiology and Parasitology/Parasitology, Selection, Genetic, Clade, Symbiosis, Molecular Biology, Drosophila, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, 0303 health sciences, Behavior, Animal, biology, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Horizontal gene transfer, [SDV.EE.IEO] Life Sciences [q-bio]/Ecology, environment/Symbiosis, biology.organism_classification, Virus, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Ichneumonoidea, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, Evolutionary biology, Larva, [SDV.BA.ZI] Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Female, [SDV.MP.PAR] Life Sciences [q-bio]/Microbiology and Parasitology/Parasitology, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract: Some species of parasitic wasps have domesticated viral machineries to deliver immunosuppressive factors to their hosts. Up to now, all described cases fall into the Ichneumonoidea superfamily, which only represents around 10% of hymenoptera diversity, raising the question of whether such domestication occurred outside this clade. Furthermore, the biology of the ancestral donor viruses is completely unknown. Since the 1980s, we know that Drosophila parasitoids belonging to the Leptopilina genus, which diverged from the Ichneumonoidea superfamily 225 Ma, do produce immunosuppressive virus-like structure in their reproductive apparatus. However, the viral origin of these structures has been the subject of debate. In this article, we provide genomic and experimental evidence that those structures do derive from an ancestral virus endogenization event. Interestingly, its close relatives induce a behavior manipulation in present-day wasps. Thus, we conclude that virus domestication is more prevalent than previously thought and that behavior manipulation may have been instrumental in the birth of such associations.
Published: 2020
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15. Evidence for an ichnovirus machinery in parasitoids of coleopteran larvae

Author: Fabrice Legeai, Marc Ravallec, James B. Whitfield, Stéphanie Robin, Marie Frayssinet, Anne-Nathalie Volkoff, Véronique Jouan, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Plateforme bioinformatique GenOuest [Rennes], Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Plateforme Génomique Santé Biogenouest®-Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Department of Entomology, University of Arkansas [Fayetteville], Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Agence Nationale de la Recherche, 'Département Santé des Plantes et Environnement', Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Rennes (UR)-Plateforme Génomique Santé Biogenouest®-Inria Rennes – Bretagne Atlantique, Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes 1 (UR1), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), and Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA)
Subjects: Cancer Research, food.ingredient, Subfamily, ichnovirus, charancon, Ovary (botany), Zoology, luzerne, Genome, 03 medical and health sciences, food, ichneumonidae, Virology, Animals, genes, Gene, 030304 developmental biology, 0303 health sciences, biology, 030306 microbiology, Gene Expression Profiling, Weevil, gène, Ovary, biology.organism_classification, Hymenoptera, Ichneumonidae, Infectious Diseases, Polydnaviridae, Larva, Weevils, Female, Campopleginae, Ichnovirus, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, alfalfa
Abstract: International audience; Bathyplectes spp. are ichneumonid solitary larval parasitoids of the alfalfa weevil which have been classified in the subfamily Campopleginae and which harbor atypical virus particles. Despite the morphological differences between Bathyplectes spp. particles and the polydnaviruses carried by a number of related campoplegine species, called ichnoviruses, the process by which they are produced is very similar to that of ichnoviruses. To address the question of the nature and origin of these atypical particles, the Bathyplectes anurus ovary transcriptome has been analyzed. We found a number of highly expressed transcripts displaying similarities with genes belonging to the machinery involved in the production of ichnovirus particles. In addition, transcripts with similarities with repeat-element genes, which are characteristic of the packaged campoplegine ichnovirus genome were identified. Altogether, our results provide evidence that Bathyplectes particles are related to ichnoviruses.
Published: 2019
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16. Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps

Author: Claire Lemaitre, Seán G. Brady, Fabrice Legeai, Stéphanie Robin, Denis Tagu, Bernardo F. Santos, Shanlin Liu, Véronique Jouan, Anthony Bretaudeau, Anne-Nathalie Volkoff, Xin Zhou, Marc Ravallec, Rebecca B. Dikow, Gabor Gyapay, Jean-Michel Drezen, Bruce A. Webb, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES), National Museum for Natural History, Smithsonian Institution, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Université de Tours, Institut de Génomique d'Evry (IG), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Department of Entomology, China Agricultural University (CAU), China National GeneBank, University of Kentucky, Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Rennes (UR), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Université de Tours (UT), Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), and University of Kentucky (UK)
Subjects: 0106 biological sciences, food.ingredient, ichnovirus, Virulence, macromolecular substances, Biology, 010603 evolutionary biology, 01 natural sciences, Genome, endogenous virusarchitecture, Parasitoid, 03 medical and health sciences, food, virus domestication, Gene, 030304 developmental biology, Genomic organization, Whole genome sequencing, 0303 health sciences, fungi, biology.organism_classification, Evolutionary biology, Ichnovirus, polydnavirus, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Bracovirus, parasitoid wasp
Abstract: Polydnaviruses (PDVs) are mutualistic endogenous viruses associated with some lineages of parasitoid wasps that allow successful development of the wasps within their hosts. PDVs include two taxa resulting from independent virus acquisitions in braconid (bracoviruses) and ichneumonid wasps (ichnoviruses). PDV genomes are fully incorporated into the wasp genomes and comprise (1) virulence genes located on proviral segments that are packaged into the viral particle, and (2) genes involved in the production of the viral particles, which are not encapsidated. Whereas the genomic organization of bracoviruses within the wasp genome is relatively well known, the architecture of endogenous ichnoviruses remains poorly understood. We sequenced the genome of two ichnovirus-carrying wasp species,Hyposoter didymatorandCampoletis sonorensis. Complete assemblies with long scaffold sizes allowed identification of the integrated ichnovirus, highlighting an extreme dispersion within the wasp genomes of the viral loci,i.e.isolated proviral segments and clusters of replication genes. Comparing the two wasp species, proviral segments harbor distinct gene content and variable genomic environment, whereas viral machinery clusters show conserved gene content and order, and can be inserted in collinear wasp genomic regions. This distinct architecture is consistent with the biological properties of the two viral elements: proviral segments producing virulence proteins allowing parasitism success are fine-tuned to the host physiology, while an ancestral viral architecture was likely maintained for the genes involved in virus particle production. Finding a distinct genomic architecture of ichnoviruses and bracoviruses highlights different evolutionary trajectories leading to virus domestication in the two wasp lineages.
Published: 2019
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17. Venom atypical extracellular vesicles as interspecies vehicles of virulence factors involved in host specificity: the case of a Drosophila Parasitoid Wasp

Author: Olivier Pierre, Séverine Lemauf, Emilie Goguet, Marylène Poirié, Jean Luc Gatti, Anne-Nathalie Volkoff, Bin Wan, Marc Ravallec, Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Department of Plant Health and Environment (SPE) of the French National Institute for Agricultural Research (INRA), Provence, Alpes, Cote d'Azur (PACA) region, ANR-11-LABX-0028,SIGNALIFE,Réseau d'Innovation sur les Voies de Signalisation en Sciences de la Vie(2011), European Project: 613678,EC:FP7:KBBE,FP7-KBBE-2013-7-single-stage,DROPSA(2014), Poirié, Marylène, Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)
Subjects: 0301 basic medicine, lcsh:Immunologic diseases. Allergy, Biodiversité et Ecologie, Immunology, Virulence, Parasitism, Leptopilina, Venom, Biology, Parasitoid wasp, Biodiversity and Ecology, 03 medical and health sciences, 0302 clinical medicine, venosomes, Immunology and Allergy, Drosophila, Host (biology), fungi, biology.organism_classification, immunity, 3. Good health, Cell biology, parasitoid wasp, lamellocyte, virulence, 030104 developmental biology, Drosophila melanogaster, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, lcsh:RC581-607, 030215 immunology
Abstract: International audience; Endoparasitoid wasps, which lay eggs inside the bodies of other insects, use various strategies to protect their offspring from the host immune response. The hymenopteran species of the genus Leptopilina, parasites of Drosophila, rely on the injection of a venom which contains proteins and peculiar vesicles (hereafter venosomes). We show here that the injection of purified L. boulardi venosomes is sufficient to impair the function of the Drosophila melanogaster lamellocytes, a hemocyte type specialized in the defense against wasp eggs, and thus the parasitic success of the wasp. These venosomes seem to have a unique extracellular biogenesis in the wasp venom apparatus where they acquire specific secreted proteins/virulence factors and act as a transport system to deliver these compounds into host lamellocytes. The level of venosomes entry into lamellocytes of different Drosophila species was correlated with the rate of parasitism success of the wasp, suggesting that this venosome-cell interaction may represent a new evolutionary level of host-parasitoid specificity.
Published: 2019
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18. Sharing cells with Wolbachia : the transovarian vertical transmission of Culex pipiens densovirus

Author: Mine Altinli, Anne-Sophie Gosselin-Grenet, Manon Bonneau, Julien Soms, Marc Ravallec, Mathieu Sicard, Mylène Weill, Fabienne Justy, Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), French National Research Agency (ANR) [ANR-10-INBS-04], Campus France, Ministere des affaires étrangères, École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de recherche pour le développement [IRD] : UR226, and Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA)
Subjects: Plasmodium, [SDV]Life Sciences [q-bio], immunomodulation, densovirus, law.invention, law, reproductive and urinary physiology, 0303 health sciences, Transmission (medicine), symbiosis, 3. Good health, Transmission (mechanics), ssDNA virus, Single Stranded DNA Virus, [SDE]Environmental Sciences, Wolbachia, Densovirus, West Nile virus, keratinocytes, Zoology, mosquito, [SDV.BID]Life Sciences [q-bio]/Biodiversity, Biology, Microbiology, Virus, An. funestus, 03 medical and health sciences, interferon-stimulated genes, Culex pipiens, parasitic diseases, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, mosquitoes, saliva, 030306 microbiology, Host (biology), biochemical phenomena, metabolism, and nutrition, biology.organism_classification, Virology, Malaria, wAnfu, Viral replication, Vector (epidemiology), innate immune response, bacteria, viral replication, Biological control Senegal, [SDE.BE]Environmental Sciences/Biodiversity and Ecology
Abstract: Originality-Significance Statement This contribution provides a window into the study of a densovirus called CpDV infecting Culex pipiens mosquitoes. The originality of the study lies in the fact that CpDV, a DNA virus, was to date almost unstudied, its interaction with its hosts and its transmission mode were unknown. Considering that all Cx. pipiens are infected with Wolbachia, we studied the influence of this bacterial endosymbiont on CpDV density and transmission. Although Wolbachia-RNA virus interactions, especially in non-native Wolbachia-host associations have been widely studied, Wolbachia-DNA virus interactions were rarely investigated. In this natural tripartite Cx. pipiens-Wolbachia-CpDV system: We revealed the wide prevalence of CpDV, mostly at low densities, in Cx. pipiens laboratory lines. We monitored CpDV presence in several cell types in ovaries including the oocytes where they co-exist with the bacterial endosymbiont Wolbachia. We demonstrated that CpDV density in ovaries was influenced by Wolbachia presence and strain variations We studied CpDV vertical transmission depending on Wolbachia presence and strain variations We report for the first time the occurrence of widely distributed covert CpDV infections in Cx. pipiens laboratory colonies. CpDV is maintained by both vertical and horizontal transmission and under the influence of the vertically transmitted bacterial endosymbiont Wolbachia. Taken together our results suggest that CpDV could be very prevalent in nature putatively influencing natural Cx. pipiens populations’ dynamics. SUMMARY Culex pipiens densovirus (CpDV), a single stranded DNA virus, has been isolated from Culex pipiens mosquitoes but differs from other mosquito densoviruses in terms of genome structure and sequence identity. Its transmission from host to host, the nature of its interactions with both its host and host’s endosymbiotic bacteria Wolbachia are not known. Here we report the presence of CpDV in the ovaries and eggs of Cx. pipiens mosquitoes in close encounters with Wolbachia. In the ovaries, CpDV quantity significantly differed between mosquito lines harboring different strains of Wolbachia and these differences were not linked to variations in Wolbachia densities. CpDV was vertically transmitted in all laboratory lines to 17%-20% of the offspring. For some females, however, the vertical transmission reached 90%. Antibiotic treatment that cured the host from Wolbachia also significantly affected both CpDV quantity and vertical transmission suggesting an impact of host microbiota, including Wolbachia, on CpDV transmission. Overall our results show that CpDV is transmitted vertically via transovarian path along with Wolbachia with which it shares the same cells. Our results are primordial to understand the dynamics of densovirus infection, their persistence and spread in populations considering their potential use in the regulation of mosquito vector populations.
Published: 2018
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19. A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps

Author: D. Di Giovanni, Julien Varaldi, David Lepetit, Marc Ravallec, Matthieu Boulesteix, Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Eléments transposables, évolution, populations, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), and Génétique et évolution des interactions hôtes-parasites
Subjects: 0303 health sciences, biology, Host (biology), viruses, Lineage (evolution), [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], fungi, 030302 biochemistry & molecular biology, Figitidae, Hymenoptera, Leptopilina, biology.organism_classification, Virus, Parasitoid, 03 medical and health sciences, Evolutionary biology, Drosophila, 030304 developmental biology
Abstract: To circumvent host immune response, numerous hymenopteran endo-parasitoid species produce virus-like structures in their reproductive apparatus that are injected into the host together with the eggs. These viral-like structures are absolutely necessary for the reproduction of these wasps. The viral evolutionary origin of these viral-like particles has been demonstrated in only two cases and for both, the nature of the initial virus-wasp association remains unknown. This is either because no closely related descendant infects the wasps, because it has not been sampled yet, or because the virus lineage went extinct. In this paper, we provide strong evidence that the virus-like particles (VLPs) produced by endoparasitoids of Drosophila belonging to the genus Leptopilina (Hymenoptera Figitidae) have a viral origin, solving the debate on their origin. Furthermore, the ancestral donor virus still has close relatives infecting one of the wasp species, thus giving us insights on the ecological interaction that possibly allowed the domestication process. Intriguingly, this contemporary virus is both vertically and horizontally transmitted and has the particularity to manipulate the superparasitism behavior of the wasp. This raises the possibility that behavior manipulation has been instrumental in the birth of such association between wasps and viruses.
Published: 2018

20. A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps

Author: Deborah Di Giovanni, David Lepetit, Matthieu Boulesteix, Yohann Coute, Marc Ravallec, and Julien Varaldi
Subjects: biology, Host (biology), viruses, Lineage (evolution), fungi, Figitidae, macromolecular substances, Hymenoptera, Leptopilina, biology.organism_classification, Virus, Evolutionary biology, Domestication, Drosophila
Abstract: To circumvent host immune response, some hymenopteran endo-parasitoids produce virus-like structures in their reproductive apparatus that are injected into the host together with the eggs. These viral-like structures are absolutely necessary for the reproduction of these wasps. The viral evolutionary origin of these viral-like particles has been demonstrated in only a few cases of wasp species all belonging to the Ichneumonoidea superfamily. In addition, the nature of the initial virus-wasp association remains unknown for all. This is either because no closely related descendant infects the wasps, because it has not been sampled yet, or because the virus lineage went extinct. In this paper, we show that the virus-like particles (VLPs) produced by endoparasitoids of Drosophila belonging to the Leptopilina genus (superfamily Cynipoidea) do have a viral origin, solving the debate on their origin. Furthermore, the ancestral donor virus still has close relatives infecting one of the wasp species, thus giving us insights on the ecological interaction that possibly allowed the domestication process. Intriguingly, this contemporary virus is both vertically and horizontally transmitted and has the particularity to manipulate the superparasitism behavior of the wasp. This raises the possibility that behavior manipulation has been instrumental in the birth of such association between wasps and viruses.
Published: 2018
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21. First extensive characterization of the venom gland from an egg parasitoid: structure, transcriptome and functional role

Author: Fabrice Legeai, Véronique Jouan, Antonino Cusumano, Marc Ravallec, Ezio Peri, Bernard Duvic, Anne-Nathalie Volkoff, Stefano Colazza, Department of Agricultural, Food and Forest Sciences, Università degli studi di Palermo - University of Palermo, Laboratory of Entomology, School of agriculture, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), BioInformatics Platform for Agroecosystems Arthropods, Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), EMBO [533 - 2012], European Project: 609398,EC:FP7:PEOPLE,FP7-PEOPLE-2013-COFUND,AGREENSKILLSPLUS(2014), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Cusumano, Antonino, Duvic, Bernard, Jouan, Véronique, Ravallec, Marc, Legeai, Fabrice, Peri, Ezio, Colazza, Stefano, Volkoff, Anne-Nathalie, Université de Rennes (UR), and Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST
Subjects: 0106 biological sciences, 0301 basic medicine, Physiology, Glycosylases, Wasps, Venom, Laccases, Hymenoptera, Insect, melanization, 01 natural sciences, virulence factor, Parasitoid, Transcriptome, Physiological suppression, Laboratory of Entomology, Arthropod Venoms, media_common, Larva, biology, Virulence factors, Phenotype, Nezara viridula, laccazes, Insect Proteins, Female, Melanization, media_common.quotation_subject, Zoology, complex mixtures, Host-Parasite Interactions, Heteroptera, 03 medical and health sciences, glycosylases, Exocrine Glands, Microscopy, Electron, Transmission, Animals, Peptidase, Host (biology), Laccase, fungi, biology.organism_classification, Laboratorium voor Entomologie, physiological suppression, 010602 entomology, 030104 developmental biology, Settore AGR/11 - Entomologia Generale E Applicata, peptidases, Insect Science, EPS, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Peptidases, Glycosylase
Abstract: The venom gland is a ubiquitous organ in Hymenoptera. In insect parasitoids, the venom gland has been shown to have multiple functions including regulation of host immune response, host paralysis, host castration and developmental alteration. However, the role played by the venom gland has been mainly studied in parasitoids developing in larval or pupal hosts while little is known for parasitoids developing in insect eggs. We conducted the first extensive characterization of the venom of the endoparasitoid Ooencyrtus telenomicida (Vassiliev), a species that develops in eggs of the stink bug Nezara viridula (L.). In particular we investigated the structure of the venom apparatus, its functional role and conducted a transcriptomic analysis of the venom gland. We found that injection of O. telenomicida venom induces: 1) a melanized-like process in N. viridula host eggs (host-parasitoid interaction), 2) impairment of the larval development of the competitor Trissolcus basalis (Wollaston) (parasitoid-parasitoid interaction). The O. telenomicida venom gland transcriptome reveals a majority of digestive enzymes (peptidases and glycosylases) and oxidoreductases (laccases) among the most expressed genes. The former enzymes are likely to be involved in degradation of the host resources for the specific benefit of the O. telenomicida offspring. In turn, alteration of host resources caused by these enzymes may negatively affect the larval development of the competitor T. basalis. We hypothesize that the melanization process induced by venom injection could be related to the presence of laccases, which are multicopper oxidases that belong to the phenoloxidases group. This work contributed to a better understanding of the venom in insect parasitoids and allowed to identify candidate genes whose functional role can be investigated in future studies.
Published: 2017
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22. An Insight in the Reproductive Biology of Therophilus javanus (Hymenoptera, Braconidae, and Agathidinae), a Potential Biological Control Agent against the Legume Pod Borer (Lepidoptera, Crambidae)

Author: Barry R. Pittendrigh, Manuele Tamò, Djibril Aboubakar Souna, Antonino Cusumano, Aimé H. Bokonon-Ganta, Anne-Nathalie Volkoff, Marc Ravallec, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), International Institute of Tropical Agriculture (IITA), International Institute of Tropical Agriculture, Faculté des Sciences Agronomiques (FSA), University of Abomey Calavi (UAC), Wageningen University and Research Centre [Wageningen] (WUR), Michigan State University [East Lansing], Michigan State University System, Aboubakar Souna D., Bokonon-Ganta A., Ravallec M., Cusumano A., Pittendrigh B.R., Volkoff A.-N., Tamo M., International Institute of Tropical Agriculture (IITA-Benin), International Institute of Tropical Agriculture [Nigeria] (IITA), Consultative Group on International Agricultural Research [CGIAR] (CGIAR)-Consultative Group on International Agricultural Research [CGIAR] (CGIAR), and Wageningen University and Research [Wageningen] (WUR)
Subjects: 0106 biological sciences, [SDV.SA]Life Sciences [q-bio]/Agricultural sciences, Article Subject, Biological pest control, Parasitism, Zoology, 010603 evolutionary biology, 01 natural sciences, follicle, Parasitoid, Lepidoptera genitalia, Crambidae, Maruca vitrata, lcsh:Zoology, lcsh:QL1-991, Laboratory of Entomology, Caterpillar, Ecology, Evolution, Behavior and Systematics, biology, fungi, biology.organism_classification, Laboratorium voor Entomologie, ovariole, 010602 entomology, vitellarium, Settore AGR/11 - Entomologia Generale E Applicata, Agronomy, Insect Science, caterpillar, oogenesi, EPS, 017-4066, Braconidae, Research Article
Abstract: Therophilus javanus is a koinobiont, solitary larval endoparasitoid currently being considered as a biological control agent against the pod borer Maruca vitrata, a devastating cowpea pest causing 20–80% crop losses in West Africa. We investigated ovary morphology and anatomy, oogenesis, potential fecundity, and egg load in T. javanus, as well as the effect of factors such as age of the female and parasitoid/host size at oviposition on egg load. The number of ovarioles was found to be variable and significantly influenced by the age/size of the M. vitrata caterpillar when parasitized. Egg load also was strongly influenced by both the instar of M. vitrata caterpillar at the moment of parasitism and wasp age. The practical implications of these findings for improving mass rearing of the parasitoid toward successful biological control of M. vitrata are discussed.
Published: 2017
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23. Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

Author: Julie Poulain, Maya Belghazi, Dominique Colinet, Carole Dossat, Marc Ravallec, Marylène Poirié, Hugo Mathé-Hubert, Jean-Luc Gatti, Emeline Deleury, Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Centre de recherche en neurobiologie - neurophysiologie de Marseille (CRN2M), Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de Génomique d'Evry (IG), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, ANR-09-BLAN-0243-01, ANR-11-LABX-0028, ANR-09-BLAN-0243,PARATOXOSE(2009), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Physiologie de la reproduction et des comportements [Nouzilly] (PRC), Centre National de la Recherche Scientifique (CNRS)-Université de Tours-Institut Français du Cheval et de l'Equitation [Saumur]-Institut National de la Recherche Agronomique (INRA), Mathé Hubert, Hugo, Colinet, Dominique, Poirié, Marylène, Gatti, Jean-Luc, Enjalbert, Alain, and Blanc - - PARATOXOSE2009 - ANR-09-BLAN-0243 - Blanc - VALID
Subjects: 0301 basic medicine, Proteome, [SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology, media_common.quotation_subject, Olive fruit fly, Wasps, Parasitism, Venom, Wasp Venoms, Insect, Leptopilina, Leucine-Rich Repeat Proteins, Article, Parasitoid, 03 medical and health sciences, South Africa, pachyneuron concolor, Botany, protéine du venin, Animals, media_common, psyttalia lounsburyi, Multidisciplinary, 030102 biochemistry & molecular biology, biology, Host (biology), beta-Glucosidase, fungi, [SDV.NEU.NB] Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology, Proteins, Figitidae, biology.organism_classification, Kenya, 030104 developmental biology, Insect Proteins
Abstract: Venom composition of parasitoid wasps attracts increasing interest – notably molecules ensuring parasitism success on arthropod pests – but its variation within and among taxa is not yet understood. We have identified here the main venom proteins of two braconid wasps, Psyttalia lounsburyi (two strains from South Africa and Kenya) and P. concolor, olive fruit fly parasitoids that differ in host range. Among the shared abundant proteins, we found a GH1 β-glucosidase and a family of leucine-rich repeat (LRR) proteins. Olive is extremely rich in glycoside compounds that are hydrolyzed by β-glucosidases into defensive toxic products in response to phytophagous insect attacks. Assuming that Psyttalia host larvae sequester ingested glycosides, the injected venom GH1 β-glucosidase could induce the release of toxic compounds, thus participating in parasitism success by weakening the host. Venom LRR proteins are similar to truncated Toll-like receptors and may possibly scavenge the host immunity. The abundance of one of these LRR proteins in the venom of only one of the two P. lounsburyi strains evidences intraspecific variation in venom composition. Altogether, venom intra- and inter-specific variation in Psyttalia spp. were much lower than previously reported in the Leptopilina genus (Figitidae), suggesting it might depend upon the parasitoid taxa.
Published: 2016
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24. Mechanisms of transfer of virulence molecules in ichneumonid wasps

Author: Fabrice Legeai, Apolline Pichon, Don Stoltz, Valérie Barbe, Jean-Michel Drezen, Serge Urbach, Magali Eychenne, Antoine Bézier, Véronique Jouan, Matthieu Leobold, Anne-Nathalie Volkoff, Marc Ravallec, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique d'Evry (IG), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Department of Microbiology and Immunology, Rega Institute for Medical Research, Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Faculté des Sciences et Techniques, Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 7261, and Université Francois Rabelais [Tours]
Subjects: Genetics, virulence, Ecology, parasite, Virulence, guêpe, lutte biologique, Biology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, genome
Published: 2016

25. Pathogenesis of Junonia coenia densovirus in Spodoptera frugiperda: A route of infection that leads to hypoxia

Author: Philippe Fournier, Béatrice Chabi, Mylène Ogliastro, Jean-Michel Salmon, Doriane Mutuel, Marc Ravallec, Cecilia Multeau, Biologie Intégrative et Virologie des Insectes [Univ. de Montpellier II] (BIVI), Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Différenciation Cellulaire et Croissance (DCC), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2), Biotop, Sciences Pour l'Oenologie (SPO), Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université Montpellier 1 (UM1)-Université de Montpellier (UM)-Institut National de la Recherche Agronomique (INRA)
Subjects: ANOXIA, [SDV]Life Sciences [q-bio], PATHOGENESIS, Spodoptera, Biology, Virus, Pathogenesis, 03 medical and health sciences, INSECT PARVOVIRUS, Virology, [SDV.IDA]Life Sciences [q-bio]/Food engineering, TISSUE TROPISM, medicine, Animals, [INFO]Computer Science [cs], [SPI.GPROC]Engineering Sciences [physics]/Chemical and Process Engineering, SPODOPTERA FRUGIPERDA, Barrier function, 030304 developmental biology, DENSOVIRUS, 0303 health sciences, 030306 microbiology, HOST RANGE, fungi, ROS, Midgut, RELATION VIRUS-VECTEUR, biology.organism_classification, INSECT TRACHEA, Epithelium, 3. Good health, Oxygen, Trachea, Oxidative Stress, medicine.anatomical_structure, Larva, Tissue tropism, Densovirus, BIOLOGICAL CONTROL
Abstract: International audience; To evaluate densovirus potential against lepidopteran pests and their capacity to invade new hosts, we have characterised in vivo the infection and pathogenesis of the Junonia coenia densovirus (JcDNV) in the noctuid pest Spodoptera frugiperda. Here we show that infection starts with the ingestion of viral particles that cross the midgut epithelium without replicating. By quantitative PCR we established the kinetic and the route of infection, from virus ingestion to replication in visceral tracheae and hemocytes. JcDNV has a high particle-to-infection ratio mostly due to the barrier function of the midgut. Pathology and cytopathology suggested that infection of tracheal cells impairs oxygen delivery to demanding tissues leading to cytopathic effects in all the tissues. Finally, larval death results from several physiological shocks, including molting arrest and anoxia.
Published: 2010
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26. Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects

Author: Frédéric Fleury, Marc Ravallec, David Lepetit, Julien Varaldi, Julien Martinez, Génétique et évolution des interactions hôtes-parasites, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), ANR (11-JSV7-0011 Viromics ), Université de Montpellier (UM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), ANR-11-JSV7-0011,viromics,Distribution et impact des virus héritables dans une communauté hôtes-parasitoïdes(2011), and Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)
Subjects: 0301 basic medicine, Male, viruses, genotype, Wasps, Sequence Homology, transmission horizontale, code génétique, Parasitoid, biodiversité, Prevalence, Cluster Analysis, Phylogeny, Totiviridae, biology, Behavior, Animal, DNA virus, drosophila, larve, 3. Good health, Wills, Coinfection, RNA, Viral, Female, Horizontal transmission, 030106 microbiology, Molecular Sequence Data, Insect Viruses, virus, Virus, Parasitoid wasp, 03 medical and health sciences, arn, Virology, medicine, Animals, guêpe, leptopilina boulardi, genome, fungi, RNA virus, Sequence Analysis, DNA, biology.organism_classification, medicine.disease, Survival Analysis, Infectious Disease Transmission, Vertical, 030104 developmental biology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, vinegar flies
Abstract: Parasitoid wasps can be found in association with heritable viruses. Although some viruses have been shown to profoundly affect the biology and evolution of parasitoid wasps, the genetic and phenotypic diversity of parasitoid-associated viruses remains largely unexplored. We previously discovered a behaviour-manipulating DNA virus in the parasitoid wasp Leptopilina boulardi. In this species, which lays its eggs inside Drosophila larvae, Leptopilina boulardi filamentous virus (LbFV) forces the females to lay their eggs in already parasitized Drosophila larvae. This behavioural manipulation increases the chances for the horizontal transmission of the virus. Here, we describe in the same parasitoid species another virus, which we propose to call Leptopilina boulardi toti-like virus (LbTV). This double-stranded RNA virus is highly prevalent in insect laboratory lines as well as in parasitoids caught in the field. In some cases, LbTV was found in coinfection with LbFV, but did not affect the behaviour of the wasp. Instead we found that the presence of LbTV correlates with an increase in the number of offspring, mostly due to increased survival of parasitoid larvae. LbTV is vertically transmitted mostly through the maternal lineage even if frequent paternal transmission also occurs. Unlike LbFV, LbTV is not horizontally transmitted. Its genome encodes a putative RNA-dependent RNA polymerase (RdRp) showing similarities with RdRps of Totiviridae. These results underline the high incidence and diversity of inherited viruses in parasitoids as well as their potential impact on the phenotype of their hosts.
Published: 2016
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27. Effect of the 5′ non-translated region on self-assembly of hepatitis C virus genotype 1a structural proteins produced in insect cells

Author: Miguel López-Ferber, Martine Duonor-Cérutti, Marc Ravallec, Jean-Pierre Bossy, Annie Cahour, Gérard Devauchelle, Geneviève Inchauspé, Christel Girard, and Marcel Mariller
Subjects: Mutation, Genotype, biology, Viral Core Proteins, Virus Assembly, viruses, Hepacivirus, Hepatitis C virus, Translation (biology), Spodoptera, biology.organism_classification, medicine.disease_cause, Virology, Virus, Flaviviridae, Viral Envelope Proteins, Cytoplasm, Protein Biosynthesis, medicine, Animals, Capsid Proteins, 5' Untranslated Regions, Sequence (medicine)
Abstract: The effect of the 5' non-translated region (5'NTR) on hepatitis C virus (HCV) morphogenesis in insect cells is investigated in this study. Expression in baculovirus-infected cells of a sequence encoding the C and E1 structural proteins under the control of the very late promoter P10 (AcSLP10-C-E1) led to the synthesis of C and C-E1 complexes, essentially found in dense reticular material associated with the ER and sedimenting at a density of 1.24-1.26 g ml(-1). Addition of the 5'NTR upstream of the C-E1 sequence (AcSLP10-5'NTR-E1) prevents translation from the initiating codon, probably because of the presence of five AUG codons in this sequence. When cells were co-infected with these two viruses, virus-like particles (VLPs) were found in the cytoplasm. The size and shape of these VLPs were variable. Concomitantly, a shift in the sedimentation profile from 1.24-1.26 to 1.15-1.18 g ml(-1) was observed, suggesting an association of C/E1 with the ER membrane. A unique vector was then constructed bearing a mutated 5'NTR (mutation of the five AUGs) and the sequence encoding all of the structural proteins and part of NS2 (5'NTRm-C-E1-E2-p7-NS2Delta). Translation of structural proteins was restored and electron microscopic observation of a cytoplasmic extract showed the presence of icosahedral particles with a density of 1.15-1.18 g ml(-1).
Published: 2004
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28. A new nucleopolyhedrovirus from the oil-palm leaf-eater Euprosterna elaeasa (Lepidoptera: Limacodidae): preliminary characterization and field assessment in Peruvian plantation

Author: Marc Ravallec, Juana Luna Rodriguez, Julio Arroyo Cruzado, and Jean-Louis Zeddam
Subjects: Integrated pest management, Larva, Ecology, biology, fungi, Biological pest control, biology.organism_classification, Elaeis guineensis, Limacodidae, Toxicology, Lepidoptera genitalia, Botany, Animal Science and Zoology, PEST analysis, Agronomy and Crop Science, Specific identification
Abstract: A new nucleopolyhedrovirus (NPV), named EuelNPV, periodically affects Euprosterna elaeasa populations, a major lepidopteran defoliator of oil-palm in Peru. EuelNPV belongs to the sub-group of the single-embedded NPV and exhibits irregularly shaped inclusion bodies of a size 13 polyhedra/ha caused larval mortality from 70 to 90% compared to untreated controls. The effects were better than those obtained using pyrethroids and overall application costs were about 2.5 times lower. There is good potential for use of this entomopathogen in place of more toxic products.
Published: 2003
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29. [Untitled]

Author: J. Arroyo Cruzado, Marc Ravallec, Jean-Louis Zeddam, E. Candiotti Subilete, and J. Luna Rodriguez
Subjects: biology, business.industry, fungi, Biological pest control, Pest control, biology.organism_classification, Lepidoptera genitalia, Megalopygidae, Animal ecology, Insect Science, Botany, PEST analysis, business, Cypovirus, Agronomy and Crop Science, Predator
Abstract: Norape argyrrhorea, Hubner (Lep.:Megalopygidae), is becoming the most importantdefoliator for oil-palm plantations in Peru(South America). Apart from direct damage,feeding of the larvae also causes wounds thatprovide sites for entry for a complex ofphytopathogenic fungi. Chemical control of N. argyrrhorea is costly and results in theparallel reduction of the populations ofseveral predator and parasitoid insect speciesthat previously limited proliferation of thispest. For this reason, alternative controlmethods are being investigated. Apreviously undescribed occluded virus has beenfound responsible for fast and massivemortality among wild populations of the pest.Based on morphology, protein analysis andnucleic acids, this virus named NoarCPV,belongs to the family Reoviridae. Results ofthe first applications of NoarCPV in anoil-palm plantation demonstrated rapidmortality to population densities below damagethresholds.
Published: 2003
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30. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation

Author: David Duval, Marc Ravallec, Sabine Nidelet, Anne-Nathalie Volkoff, Guillaume Mitta, Vincent Demolombe, Benjamin Gourbal, Josée Doyon, Nolwenn M. Dheilly, Richard Galinier, Frédéric Thomas, Lucas Léger, Jacques Brodeur, Fanny Maure, Dorothée Missé, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Ecologie et évolution des interactions [2011-2014] (2EI), Université de Perpignan Via Domitia (UPVD)-Centre National de la Recherche Scientifique (CNRS), Département des Sciences Biologiques [Montréal], Université du Québec à Montréal = University of Québec in Montréal (UQAM), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX), Institut de Génomique Fonctionnelle (IGF), Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Fonds de recherche du Québec - Nature et technologies (FRQNT), ANR, Ecologie et évolution des interactions (2EI), Université du Québec à Montréal (UQAM), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-BioCampus (BCM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Modat, Anne, and Génétique et évolution des maladies infectieuses (GEMI)
Subjects: Molecular Sequence Data, Wasps, virus, Oviducts, General Biochemistry, Genetics and Molecular Biology, Virus, Parasitoid, Parasitoid wasp, Host-Parasite Interactions, Immune system, [SDV.BID.EVO] Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Animals, RNA Viruses, Research Articles, General Environmental Science, holobiont, Genetics, General Immunology and Microbiology, biology, Transmission (medicine), Host (biology), host–parasite interaction, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], fungi, RNA virus, General Medicine, biology.organism_classification, Virology, host-parasite interaction, 3. Good health, behaviour, symbiont, Coleoptera, Dinocampus coccinellae, microbiology parasitoid wasp, Larva, Female, ecology, General Agricultural and Biological Sciences, parasitoid wasp, behavioural manipulation
Abstract: Many parasites modify their host behaviour to improve their own transmission and survival, but the proximate mechanisms remain poorly understood. An original model consists of the parasitoidDinocampus coccinellaeand its coccinellid host,Coleomegilla maculata; during the behaviour manipulation, the parasitoid is not in contact with its host anymore. We report herein the discovery and characterization of a new RNA virus of the parasitoid (D. coccinellaeparalysis virus, DcPV). Using a combination of RT-qPCR and transmission electron microscopy, we demonstrate that DcPV is stored in the oviduct of parasitoid females, replicates in parasitoid larvae and is transmitted to the host during larval development. Next, DcPV replication in the host's nervous tissue induces a severe neuropathy and antiviral immune response that correlate with the paralytic symptoms characterizing the behaviour manipulation. Remarkably, virus clearance correlates with recovery of normal coccinellid behaviour. These results provide evidence that changes in ladybeetle behaviour most likely result from DcPV replication in the cerebral ganglia rather than by manipulation by the parasitoid. This offers stimulating prospects for research on parasitic manipulation by suggesting for the first time that behaviour manipulation could be symbiont-mediated.
Published: 2015
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31. Recurrent DNA virus domestication leading to different parasite virulence strategies

Author: Serge Urbach, Annie Bézier, Vonick Sibut, Julien Thézé, Sandra Schmieder, Anne-Nathalie Volkoff, Marylène Poirié, Marc Ravallec, Valérie Barbe, François Cousserans, Apolline Pichon, Edith Demettre, Dominique Colinet, Arnaud Couloux, Jean-Marc Aury, Jérémy Gauthier, Jean-Michel Drezen, Julie Guy, Corinne Da Silva, François Wurmser, Véronique Jouan, Institutions et Dynamiques Historiques de l'Économie et de la Société (IDHES), Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Nanterre (UPN)-Université Paris 8 Vincennes-Saint-Denis (UP8)-Université Paris 1 Panthéon-Sorbonne (UP1), Université d'Évry-Val-d'Essonne (UEVE), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), BioCampus Montpellier (BCM), Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Commissariat à l'Energie Atomique, Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Centre de Recherches sur les Économies, les Sociétés, les Arts et les Techniques (CRESAT), Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA)), Institut de pharmacologie moléculaire et cellulaire (IPMC), Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Evolution, Génomes et Spéciation (LEGS), Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Génomique métabolique (UMR 8030), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Genoscope French National Research Agency (ANR) Appeared in article as French National Research Agency ANR-09-BLAN-0243-01, ANR-09-BLAN-0243,PARATOXOSE(2009), École normale supérieure - Cachan (ENS Cachan)-Université Panthéon-Sorbonne (UP1)-Université Paris 8 Vincennes-Saint-Denis (UP8)-Université Paris Nanterre (UPN)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 1 (UM1)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), UPR9034, Laboratoire Évolution Génomes et Spéciation, Université Paris Sud (Paris 11)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Université Paris 1 Panthéon-Sorbonne (UP1)-Université Paris 8 Vincennes-Saint-Denis (UP8)-Université Paris Nanterre (UPN)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), BioCampus (BCM), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Université Nice Sophia Antipolis (1965 - 2019) (UNS), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), École normale supérieure - Cachan (ENS Cachan)-Université Panthéon-Sorbonne (UP1)-Université Paris 8 Vincennes-Saint-Denis (UP8)-Université Paris Nanterre (UPN)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Belloufi, Aicha, Blanc - - PARATOXOSE2009 - ANR-09-BLAN-0243 - Blanc - VALID, Drezen, Jean-Michel, and Volkoff, Anne Nathalie
Subjects: Microscope Electronique à Transmission, 0106 biological sciences, hôte, Biodiversité et Ecologie, viruses, Virulence, virus, macromolecular substances, 010603 evolutionary biology, 01 natural sciences, Genome, Microbiology, Virus, Biodiversity and Ecology, Nudivirus, 03 medical and health sciences, virus domestication, [SDV.BID.EVO] Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], guêpe, Domestication, Research Articles, 030304 developmental biology, [SDV.MP.VIR] Life Sciences [q-bio]/Microbiology and Parasitology/Virology, Genetics, 0303 health sciences, Multidisciplinary, biology, Host (biology), gène viral, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], fungi, eucaryote, SciAdv r-articles, Life Sciences, DNA virus, venturia canescens, wasps, biology.organism_classification, 3. Good health, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, liposome, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, [SDV.BA.ZI] Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, Eukaryote, séquençage adn, genomes, Research Article
Abstract: Virus domestication is a recurrent and beneficial process in the evolution of parasitic wasps., Relics of ancient infections are abundant in eukaryote genomes, but little is known about how they evolve when they confer a functional benefit on their host. We show here, for the first time, that the virus-like particles shown to protect Venturia canescens eggs against host immunity are derived from a nudivirus genome incorporated by the parasitic wasp into its own genetic material. Nudivirus hijacking was also at the origin of protective particles from braconid wasps. However, we show here that the viral genes produce “liposomes” that wrap and deliver V. canescens virulence proteins, whereas the particles are used as gene transfer agents in braconid wasps. Our findings indicate that virus domestication has occurred repeatedly during parasitic wasp evolution but with different evolutionary trajectories after endogenization, resulting in different virulence molecule delivery strategies.
Published: 2015
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32. Using genomic tools to unravel parasitic wasp genome evolution via acquisition of viral genomes

Author: Anne-Nathalie Volkoff, Jean-Michel Drezen, Serge Urbach, Apolline Pichon, Véronique Jouan, Marc Ravallec, Annie Bezier, Jean-Marc Aury, Julie Guy, Francois Cousserans, Valérie Barbe, Fabrice Legeai, Denis Tagu, Li, L., Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique Fonctionnelle (IGF), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Institut de Génomique d'Evry (IG), Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, China National GeneBank, Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 7261, Université Francois Rabelais [Tours], Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Institut de Biologie François JACOB (JACOB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and Université de Tours-Centre National de la Recherche Scientifique (CNRS)
Subjects: infection virale, lutte biologique, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, genome, biodiversité
Published: 2015

33. A Noda-like Virus Isolated from the Sweetpotato Pest Spodoptera eridania (Cramer) (Lep.; Noctuidae)

Author: Aziz Lagnaoui, Juana Luna Rodriguez, Marc Ravallec, and Jean-Louis Zeddam
Subjects: Nodamura virus, biology, viruses, fungi, RNA virus, Spodoptera, biology.organism_classification, Virology, Virus, Spodoptera eridania, parasitic diseases, Agarose gel electrophoresis, Noctuidae, Nodaviridae, Ecology, Evolution, Behavior and Systematics
Abstract: A small isometric virus has been isolated from larvae of the sweetpotato pest Spodoptera eridania (Cramer) collected near Pariacoto, Ancash province, Peru. It is designated the Pariacoto virus (PaV). In addition to its high pathogenicity on its natural host Spodoptera eridania, PaV was found to replicate in Spodoptera ochrea (Hampson) larvae but not in Spodoptera frugiperda (Smith) larvae. The size of the viral particle was estimated to be about 30 nm in diameter. Polyacrylamide gel electrophoresis showed a protein of approximately 40.5 kDa. After agarose gel electrophoresis, the viral genome appeared to be bipartite RNA. Gel immunodiffusion tests showed no serological relationship between PaV and Nodamura virus, the type species for insect nodaviruses. Electron microscopy confirmed that viral replication occurs in the cytoplasm. These properties are similar to those of other members of family Nodaviridae, to which the virus is currently assigned. Copyright 1999 Academic Press.
Published: 1999
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34. Specificities of ichnoviruses associated with campoplegine wasps: genome, genes and role in host–parasitoid interaction

Author: Michel Cusson, Tristan Dorémus, Isabelle Darboux, Marc Ravallec, Marie Frayssinet, Bruce A. Webb, Don Stoltz, Véronique Jouan, Anne-Nathalie Volkoff, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Laurentian Forestry Centre, Natural Resources Canada (NRCan), Department of Microbiology and Immunology, Rega Institute for Medical Research, Department of Entomology, S-225 Agricultural Science Center N, University of Kentucky, ANR-09-BLAN-0243,PARATOXOSE(2009), Laurentian Forestry Centre, Canadian Forest Service, and Paratoxose project (ANR-09-BLAN-0243-01)
Subjects: food.ingredient, ichnovirus, media_common.quotation_subject, viruses, Parasitism, Insect, lutte biologique, Genome, Virus, Parasitoid, 03 medical and health sciences, food, Gene family, Gene, genome, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, media_common, Genetics, 0303 health sciences, biology, 030302 biochemistry & molecular biology, biology.organism_classification, 3. Good health, Insect Science, Ichnovirus, hymenoptera, [SDE.BE]Environmental Sciences/Biodiversity and Ecology
Abstract: Ichnoviruses (IVs), unique symbiotic viruses carried by ichneumonid campoplegine wasps, derive from integration of a paleo-ichnovirus into an ancestral wasp genome. The modern ‘genome’ is composed of both regions that are amplified, circularized and encapsidated into viral particles and non-encapsidated viral genomic regions involved in particle morphogenesis. Packaged genomes include multiple circular dsDNAs encoding many genes mostly organized in gene families. Virus particles are assembled in specialized ovarian cells from which they exit into the oviduct lumen; mature virions are injected during oviposition into the insect host. Expression of viral proteins in infected cells correlates with physiological alterations of the host enabling success of parasitism.
Published: 2014
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35. The Baculovirus/Insect Cell System as an Alternative to Xenopus Oocytes

Author: Christèle Horeau, Hervé Sentenac, Martine Cerutti, Frédéric Gaymard, Guy Lemaillet, Jean-Baptiste Thibaud, Serge Urbach, Gérard Devauchelle, and Marc Ravallec
Subjects: 0106 biological sciences, 0303 health sciences, Xenopus, Sf9, Cell Biology, Immunogold labelling, Biology, biology.organism_classification, 01 natural sciences, Biochemistry, Molecular biology, Potassium channel, Cell biology, Cell membrane, 03 medical and health sciences, medicine.anatomical_structure, Cell culture, embryonic structures, medicine, Arabidopsis thaliana, Molecular Biology, Ion channel, 030304 developmental biology, 010606 plant biology & botany
Abstract: Two plant (Arabidopsis thaliana) K+ transport systems, KAT1 and AKT1, have been expressed in insect cells (Sf9 cell line) using recombinant baculoviruses. Microscopic observation after immunogold staining revealed that the expressed AKT1 and KAT1 polypeptides were mainly associated with internal membranes, but that a minute fraction was targeted to the cell membrane. KAT1 was known, from earlier electrophysiological characterization in Xenopus oocytes, to be an inwardly rectifying voltage-gated channel highly selective for K+, while similar experiments had failed to characterize AKT1. Insect cells expressing KAT1 displayed an exogenous inwardly rectifying K+ conductance reminiscent of that described previously in Xenopus oocytes expressing KAT1. Under similar conditions, cells expressing AKT1 showed a disturbed cell membrane electrical stability that precluded electrophysiological analysis. Use of a baculovirus transfer vector designed so as to decrease the expression level allowed the first electrophysiological characterization of AKT1. The baculovirus system can thus be used as an alternative method when expression in Xenopus oocytes is unsuccessful for electrophysiological characterization of the ion channel of interest. The plant AKT1 protein has been shown in this way to be an inwardly rectifying voltage-gated channel highly selective for K+ ions and sensitive to cGMP.
Published: 1996
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36. Comparative Study of the Cytological Aspects of the Mode of Action of Destruxins and Other Peptidic Fungal Metabolites on Target Epithelial Cells

Author: A. Vey, Marc Ravallec, Christiane Dumas, Vladimir Matha, Unité mixte de recherche de pathologie comparée, and Centre National de la Recherche Scientifique (CNRS)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA)
Subjects: 0106 biological sciences, 0303 health sciences, Brush border, Efrapeptin, Biological activity, Biology, Cadmium chloride, 01 natural sciences, In vitro, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, 010602 entomology, 03 medical and health sciences, chemistry.chemical_compound, Biochemistry, chemistry, Cyclosporin a, Botany, Mode of action, ComputingMilieux_MISCELLANEOUS, Ecology, Evolution, Behavior and Systematics, Intracellular, 030304 developmental biology
Abstract: The cytopathological effects of cyclic fungal peptides, destruxins (dtxs) A and E, Cyclosporin A, and linear peptaibols efrapeptins (=tolypin), on epithelial cells were studied by in vitro experiments with preparations of insect organs. The treatment of Malpighian tubules and midgut revealed the induction by dtx E of the formation of vesicles on microvilli of Malpighian cells and on the apical surface of midgut cells. This morphological alteration of the brush border was a Ca 2+ -dependent process, very strongly inhibited in Ca 2+ -free medium or when a combined treatment with cadmium chloride + dtx E was applied. However, cadmium chloride did not inhibit all the cytotoxic effects of dtx E. The ability to trigger the formation of vesicular structures is a property of biologically active dtxs, the inducing capacity showing, however, a decreasing intensity from dtx E to dtx A and dtx B. On the contrary, the other peptides, Cyclosporin A and efrapeptins, did not induce the formation of vesicles. The most obvious intracellular alterations consist of a pycnosis of the nucleus, and in changes of mitochondria, the contents of which show a decrease in density and are comparable to those observed in vivo . If mitochondria are target organelles for the three different types of toxins tested, the structural changes induced at this level were specific for dtxs, Cyclosporin A, and efrapeptins, respectively. The cytological data obtained strongly suggested that dtxs have a unique mode of action among fungal peptides and do not act mainly as ionophores, inducing the formation of pores in cellular membranes, or as mitochondrial ATPase inhibitors.
Published: 1996
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37. Venom gland extract is not required for successful parasitism in the polydnavirus-associated endoparasitoid Hyposoter didymator (Hym. Ichneumonidae) despite the presence of numerous novel and conserved venom proteins

Author: Eric Wajnberg, Tristan Dorémus, Jean-Luc Gatti, Serge Urbach, Véronique Jouan, Dominique Colinet, Anne-Nathalie Volkoff, Marylène Poirié, Carole Azéma-Dossat, Julie Poulain, François Cousserans, Edith Demettre, Isabelle Darboux, Marc Ravallec, Jean-Michel Escoubas, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), UMR 7254, Centre National de la Recherche Scientifique (CNRS), IG, Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Genoscope ('Parasitoid venoms' project), French National Research Agency (Paratoxose project) [ANR-09-BLAN-0243-01], Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), ANR-09-BLAN-0243,PARATOXOSE(2009), Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)
Subjects: Male, 0106 biological sciences, Proteomics, Cellular immunity, Proteome, Hydrolases, [SDV]Life Sciences [q-bio], Wasps, Wasp Venoms, Venom, 01 natural sciences, Biochemistry, Polydnavirus, Ichneumonid, Immunity, Cellular, 0303 health sciences, Microscopy, biology, Spodoptera frugiperda, 3. Good health, Larva, Insect immunity, Insect Proteins, Female, Serine Proteinase Inhibitors, Molecular Sequence Data, Hyposoter didymator, Spodoptera, Serpin, 010603 evolutionary biology, complex mixtures, Host-Parasite Interactions, 03 medical and health sciences, Exocrine Glands, Botany, Animals, Amino Acid Sequence, Molecular Biology, 030304 developmental biology, Gene Expression Profiling, Sequence Analysis, DNA, Venom Protein, biology.organism_classification, Hymenoptera, Parasitoid, Insect Science, Campopleginae, Host regulation, Transcriptome, Parasitism success
Abstract: Corrigendum to “Venom gland extract is not required for successful parasitism in the polydnavirus-associated endoparasitoid Hyposoter didymator (Hym. Ichneumonidae) despite the presence of numerous novel and conserved venom proteins” [Insect Biochem. Mol. Biol. 43 (2013), 292–307] http://dx.doi.org/10.1016/j.ibmb.2013.07.001(UT:000329772300006); The venom gland is a conserved organ in Hymenoptera that shows adaptations associated with life-style diversification. Few studies have investigated venom components and function in the highly diverse parasitic wasps and all suggest that the venom regulates host physiology. We explored the venom of the endoparasitoid Hyposoter didymator (Campopleginae), a species with an associated polydnavirus produced in the ovarian tissue. We investigated the effects of the H. didymator venom on two physiological traits of the host Spodoptera frugiperda (Noctuidae): encapsulation response and growth rate. We found that H. didymator venom had no significant effect on host cellular immunity or development, suggesting that it does not contribute to parasitism success. The host physiology seemed to be modified essentially by the ovarian fluid containing the symbiotic polydnaviruses. Proteomic analyses indicated that the H. didymator venom gland produces a large variety of proteins, consistent with the classical hymenopteran venom protein signature, including: reprolysin-like, dipeptidyl peptidase IV, hyaluronidase, arginine kinase or allergen proteins. The venom extracts also contained novel proteins, encoded by venom genes conserved in Campopleginae ichneumonids, and proteins with similarities to active molecules identified in other parasitoid species, such as calreticulin, reprolysin, superoxide dismutase and serpin. However, some of these proteins appear to be produced only in small amounts or to not be secreted. Possibly, in Campopleginae carrying polydnaviruses, the host-modifying activities of venom became. redundant following the acquisition of polydnaviruses by the lineage.
Published: 2013
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38. Hyposoter didymator uses a combination of passive and active strategies to escape from the Spodoptera frugiperda cellular immune response

Author: Serge Urbach, Eric Wajnberg, Anne-Nathalie Volkoff, Véronique Jouan, Marc Ravallec, Tristan Dorémus, Patrick Wincker, François Cousserans, Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Université Montpellier 2 - Sciences et Techniques (UM2), Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Genoscope ('Polydnavirus' projet), ANR-09-BLAN-0243-01, Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), ANR-09-BLAN-0243,PARATOXOSE(2009), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA)
Subjects: 0106 biological sciences, Proteome, oviduct, Physiology, système immunitaire, ichnovirus, Wasps, mass spectrum analysis, Egg protein, venom, parasitisme des oeufs, apolipoprotéine, Polymerase Chain Reaction, 01 natural sciences, follicule ovarien, ichneumonidae, Tandem Mass Spectrometry, spectrométrie de masse, hyposoter didymator, symbiote, fluid, Immunity, Cellular, 0303 health sciences, Polydnavirus, fluide, mode de vie, Cell biology, symbiont, protéine, Larva, Insect Proteins, Female, polydnavirus, hymenoptera, protéine de synthèse, Braconidae, food.ingredient, particule virale, apolipoprotein, venin, Spodoptera, Biology, sepals, Calyx, braconidae, évasion immune, Viral Proteins, 03 medical and health sciences, life styles, Immune system, food, calice, Animals, oviducte, Ovum, 030304 developmental biology, Egg Proteins, Virion, protéines de surface, biology.organism_classification, Virology, 010602 entomology, ovarian follicle, Polydnaviridae, Insect Science, encapsulation, réponse de l'hôte, Ichnovirus, aphidiidae, endoparasite, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, protein
Abstract: An endoparasitic life style is widespread among Hymenoptera, and various different strategies allowing parasitoids to escape from the host encapsulation response have been reported. Species carrying polydnaviruses (PDVs), such as the ichneumonid Hyposoter didymator, generally rely on the viral symbionts to evade host immune responses. In this work, we show that H. didymator eggs can evade encapsulation by the host in the absence of calyx fluid (containing the viral particles), whereas protection of the larvae requires the presence of calyx fluid. This evasion by the eggs depends on proteins associated with the exochorion. This type of local passive strategy has been described for a few species carrying PDVs. Immune evasion by braconid eggs appears to be related to PDVs or proteins synthesized in the oviducts being associated with the egg. We report that in H. didymator, by contrast, proteins already present in the ovarian follicles are responsible for the eggs avoiding encapsulation. Mass spectrometry analysis of the egg surface proteins revealed the presence of host immune-related proteins, including one with similarities with apolipophorin-III, and also the presence of three viral proteins encoded by IVSPERs (Ichnovirus Structural Protein Encoding Regions).
Published: 2013
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39. The replication of Hyposoter didymator polydnavirus: Cytopathology of the calyx cells in the parasitoid

Author: Marc Ravallec, Gérard Devauchelle, Jean-Pierre Bossy, Janick Rocher, Anne-Nathalie Volkoff, Pierre Cérutti, and Martine Cerutti
Subjects: 0303 health sciences, food.ingredient, biology, 030306 microbiology, Polydnavirus, Ovary, Cell Biology, General Medicine, Anatomy, biology.organism_classification, Virus, 3. Good health, Parasitoid, Cell biology, Calyx, 03 medical and health sciences, food, medicine.anatomical_structure, Viral replication, Cytopathology, medicine, Bracovirus, 030304 developmental biology
Abstract: In the ichneumonid wasp Hyposoter didymator, a polydnavirus was detected in the female reproductive tract. With the aim of studying the regulation of polydnavirus replication, the location and the structure of the virus-producing cells were determined, and the virus replication process was followed inside the ovaries of young adult females observed in light and electron microscopy. The examination of ovaries of pupa females revealed that virus replication is initiated within the calyx just prior to adult emergence. This study revealed that the calyx appears to be a specialized virogenic tissue which also has, during late pupal life, a secretory function that alters the function of virus production.
Published: 1995
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40. The cellular immune response of the pea aphid to foreign intrusion and symbiotic challenge

Author: Christian Rebuf, Jean-Christophe Simon, Jean-Luc Gatti, Marc Ravallec, Marylène Poirié, Antonin Schmitz, Caroline Anselme, Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut Sophia Agrobiotech (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and Schmitz, Antonin
Subjects: 0106 biological sciences, puceron du pois, Cellular immunity, Anatomy and Physiology, Hemocytes, cellule immune, lcsh:Medicine, Cell Count, 01 natural sciences, hémocyte, défense immunitaire, Immunologie, Hemolymph, symbiote, lcsh:Science, Immune Response, 0303 health sciences, Aphid, Immunity, Cellular, Multidisciplinary, Microbiology and Parasitology, food and beverages, Foreign Bodies, Microbiologie et Parasitologie, Microspheres, hémolymphe, Host-Pathogen Interaction, medicine.anatomical_structure, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, [SDV.IMM]Life Sciences [q-bio]/Immunology, Female, Research Article, Cell Physiology, Evolutionary Immunology, Histology, animal structures, Immune Cells, réponse immunitaire, Immunology, acyrthosiphon pisum, Biology, Granulocyte, Hamiltonella defensa, 010603 evolutionary biology, Microbiology, 03 medical and health sciences, Immune system, Phagocytosis, Species Specificity, medicine, Cell Adhesion, Escherichia coli, Animal Physiology, Animals, Symbiosis, Blood Coagulation, 030304 developmental biology, Evolutionary Biology, fungi, lcsh:R, Immunity, Immune Defense, légume, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, Acyrthosiphon pisum, Aphids, lcsh:Q, Buchnera, Zoology, Entomology, transmission intergénérationnelle, Granulocytes
Abstract: Publication Inra prise en compte dans l'analyse bibliométrique des publications scientifiques mondiales sur les Fruits, les Légumes et la Pomme de terre. Période 2000-2012. http://prodinra.inra.fr/record/256699; International audience; Recent studies suggest that the pea aphid (Acyrthosiphon pisum) has low immune defenses. However, its immune components are largely undescribed, and notably, extensive characterization of circulating cells has been missing. Here, we report characterization of five cell categories in hemolymph of adults of the LL01 pea aphid clone, devoid of secondary symbionts (SS): prohemocytes, plasmatocytes, granulocytes, spherulocytes and wax cells. Circulating lipid-filed wax cells are rare; they otherwise localize at the basis of the cornicles. Spherulocytes, that are likely sub-cuticular sessile cells, are involved in the coagulation process. Prohemocytes have features of precursor cells. Plasmatocytes and granulocytes, the only adherent cells, can form a layer in vivo around inserted foreign objects and phagocytize latex beads or Escherichia coli bacteria injected into aphid hemolymph. Using digital image analysis, we estimated that the hemolymph from one LL01 aphid contains about 600 adherent cells, 35% being granulocytes. Among aphid YR2 lines differing only in their SS content, similar results to LL01 were observed for YR2-Amp (without SS) and YR2-Ss (with Serratia symbiotica), while YR2-Hd (with Hamiltonella defensa) and YR2(Ri) (with Regiella insecticola) had strikingly lower adherent hemocyte numbers and granulocyte proportions. The effect of the presence of SS on A. pisum cellular immunity is thus symbiont-dependent. Interestingly, Buchnera aphidicola (the aphid primary symbiont) and all SS, whether naturally present, released during hemolymph collection, or artificially injected, were internalized by adherent hemocytes. Inside hemocytes, SS were observed in phagocytic vesicles, most often in phagolysosomes. Our results thus raise the question whether aphid symbionts in hemolymph are taken up and destroyed by hemocytes, or actively promote their own internalization, for instance as a way of being transmitted to the next generation. Altogether, we demonstrate here a strong interaction between aphid symbionts and immune cells, depending upon the symbiont, highlighting the link between immunity and symbiosis.
Published: 2012
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41. Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses

Author: Anne-Nathalie Volkoff, François Cousserans, Pierre Delobel, Véronique Jouan, Philippe Fournier, Eric Wajnberg, Bertille Provost, Pauline Bernardo, Isabelle Darboux, Marc Ravallec, Michael R. Strand, Frédérique Hilliou, Diversité, Génomes et Interactions Microorganismes-Insectes, Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2), Interactions Biotiques et Santé Végétale, Institut National de la Recherche Agronomique (INRA), Sciences Pour l'Oenologie (SPO), Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université Montpellier 1 (UM1)-Université de Montpellier (UM)-Institut National de la Recherche Agronomique (INRA), Biologie et Génétique des interactions Plantes-parasites pour la Protection Intégrée, Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and University of Georgia [USA]
Subjects: food.ingredient, Hemocytes, [SDV]Life Sciences [q-bio], Fat Body, Wasps, Gene Expression, Genome, Viral, Spodoptera, Biochemistry, Genome, Transcriptome, 03 medical and health sciences, Viral Proteins, 0302 clinical medicine, food, [SDV.IDA]Life Sciences [q-bio]/Food engineering, Animals, [SPI.GPROC]Engineering Sciences [physics]/Chemical and Process Engineering, RNA, Messenger, polydnavirus, transcriptome, microarray, spodoptera frugiperda, host-parasitoid interaction, polydnavirus host targets, Symbiosis, Molecular Biology, Gene, 030304 developmental biology, Oligonucleotide Array Sequence Analysis, Genetics, 0303 health sciences, biology, Reverse Transcriptase Polymerase Chain Reaction, Polydnavirus, Gene Expression Profiling, biology.organism_classification, Virology, 3. Good health, Gene expression profiling, Polydnaviridae, Insect Science, Insect Proteins, Ichnovirus, Collagen, Bracovirus, Braconidae, 030217 neurology & neurosurgery
Abstract: International audience; The Polydnaviridae is a family of double-stranded DNA viruses that are symbionts of parasitoid wasps. The family is currently divided into two genera, the Ichnovirus (IV) and Bracovirus (BV), which are associated with wasps in the families Ichneumonidae and Braconidae, respectively. IVs and BVs have similar immunosuppressive and developmental effects on parasitized hosts but their encapsidated genomes largely encode different genes. To assess whether IV and BV infection has similar or disparate effects on the transcriptome of shared hosts, we characterized the effects of Hyposoter didymator Ichnovirus (HdIV) and Microplitis demolitor Bracovirus (MdBV) on the fat body and hemocyte transcriptome of Spodoptera frugiperda (Lepidoptera: Noctuidae). Our results indicated that HdIV and MdBV infection alters the abundance of a relatively low proportion of S. frugiperda transcripts at 24 h post-infection. A majority of the transcripts affected by infection also differed between MdBV and HdIV. However, we did identify some host transcripts that were similarly affected by both viruses. A majority of these genes were transcribed in the fat body and most belonged to functional classes with roles in immunity, detoxiﬁcation, or cell structure. Particularly prominent in this suite of transcripts were genes encoding for predicted motor-related and collagen IV-like proteins. Overall, our data suggest that the broadly similar effects that HdIV and MdBV have on host growth and immunity are not due to these viruses inducing profound changes in host gene expression. Given though that IVs and BVs encode few shared genes, the host transcripts that are similarly affected by HdIV and MdBV could indicate convergence by each virus to target a few processes at the level of transcription that are important for successful parasitism of hosts by H. didymator and M. demolitor.
Published: 2011
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42. Viruses associated with ovarian degeneration in Apis mellifera L. queens

Author: Joachim R. de Miranda, Magali Tournaire, Marc Ravallec, François Cousserans, Laurent Gauthier, Benjamin Dainat, and Max Bergoin
Subjects: 0106 biological sciences, Applied Microbiology, Science, Population, Veterinary Microbiology, Ovary, Insect Viruses, Degeneration (medical), Pathogenesis, 01 natural sciences, Microbiology, 03 medical and health sciences, Ovarian Follicle, Deformed wing virus, Virology, medicine, Animals, Ovarian follicle, education, Biology, 030304 developmental biology, Gene Library, 0303 health sciences, education.field_of_study, Multidisciplinary, biology, Anatomy, Bees, Veterinary Virology, Fecundity, biology.organism_classification, 3. Good health, Worker bee, 010602 entomology, medicine.anatomical_structure, Fertility, Veterinary Diseases, Medicine, Female, Veterinary Science, Viral load, Viral Transmission and Infection, Veterinary Pathology, Research Article
Abstract: Queen fecundity is a critical issue for the health of honeybee (Apis mellifera L.) colonies, as she is the only reproductive female in the colony and responsible for the constant renewal of the worker bee population. Any factor affecting the queen's fecundity will stagnate colony development, increasing its susceptibility to opportunistic pathogens. We discovered a pathology affecting the ovaries, characterized by a yellow discoloration concentrated in the apex of the ovaries resulting from degenerative lesions in the follicles. In extreme cases, marked by intense discoloration, the majority of the ovarioles were affected and these cases were universally associated with egg-laying deficiencies in the queens. Microscopic examination of the degenerated follicles showed extensive paracrystal lattices of 30 nm icosahedral viral particles. A cDNA library from degenerated ovaries contained a high frequency of deformed wing virus (DWV) and Varroa destructor virus 1 (VDV-1) sequences, two common and closely related honeybee Iflaviruses. These could also be identified by in situ hybridization in various parts of the ovary. A large-scale survey for 10 distinct honeybee viruses showed that DWV and VDV-1 were by far the most prevalent honeybee viruses in queen populations, with distinctly higher prevalence in mated queens (100% and 67%, respectively for DWV and VDV-1) than in virgin queens (37% and 0%, respectively). Since very high viral titres could be recorded in the ovaries and abdomens of both functional and deficient queens, no significant correlation could be made between viral titre and ovarian degeneration or egg-laying deficiency among the wider population of queens. Although our data suggest that DWV and VDV-1 have a role in extreme cases of ovarian degeneration, infection of the ovaries by these viruses does not necessarily result in ovarian degeneration, even at high titres, and additional factors are likely to be involved in this pathology.
Published: 2011

43. Structural and functional characterization of pseudopodocyte, a shaggy immune cell produced by two Drosophila species of the obscura group

Author: Michel Brehélin, Marc Ravallec, Géraldine Doury, Geneviève Prévost, Sébastien Havard, Patrice Eslin, Biologie des Plantes et Innovation - UR UPJV 3900 (BIOPI), Université de Picardie Jules Verne (UPJV)-Transfrontalière BioEcoAgro - UMR 1158 (BioEcoAgro), Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA), Université catholique de Lille (UCL)-Université catholique de Lille (UCL)-Université d'Artois (UA)-Université de Liège-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA), Université catholique de Lille (UCL)-Université catholique de Lille (UCL), Ecologie microbienne des insectes et interactions hôte-pathogène (EMIP), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2), Biologie Intégrative et Virologie des Insectes [Univ. de Montpellier II] (BIVI), Centre National de la Recherche Scientifique (CNRS), Université de Picardie Jules Verne (UPJV), and Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA)
Subjects: Hemocytes, hemocyte, Immunology, Hemocyte, Cell, Biology, pseudopodocyte, 03 medical and health sciences, 0302 clinical medicine, Immune system, Microscopy, Electron, Transmission, Botany, Hemolymph, Melanogaster, medicine, Animals, Microscopy, Phase-Contrast, 030304 developmental biology, RELATION HOTE-PARASITE, obscura group, 0303 health sciences, Immunity, Cellular, biology.organism_classification, Hymenoptera, Cell biology, INSECTE, medicine.anatomical_structure, Larva, Ultrastructure, encapsulation, [SDV.IMM]Life Sciences [q-bio]/Immunology, Drosophila, Drosophila melanogaster, 030217 neurology & neurosurgery, Developmental Biology
Abstract: International audience; We recently reported that most of the Drosophila species of the obscure group were unable to mount cellular capsules and no lamellocyte was ever found in the hemolyraph of any of the tested species. Only three species were able to encapsulate, despite lacking lamellocytes. Their encapsulation ability was always associated with the presence of an unpreviously described kind of capsule-forming immunocytes designated as «atypical hemocytes». Here, we describe the ultrastructural and functional characteristics of this type of hemocyte. We show that these cells share many ultrastructural and morphological features with Drosophila melanogaster plasmatocytes, although they are involved in the formation of the external layers of the cellular capsule, a functional property exhibited by lamellocytes in D. melanogaster. Due to the high number of pseudopodes in these cells, we suggest to name them «pseudopodocytes». After structural and functional characterization of these atypical hemocytes, their ambiguous status between plasmatocytes and lamellocytes is discussed.
Published: 2010
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44. Densovirus infectious pathway requires clathrin-mediated endocytosis followed by trafficking to the nucleus

Author: Françoise-Xavière Jousset, Micheline Devise, Miguel López-Ferber, Agnès Vendeville, Mylène Ogliastro, Doriane Mutuel, Marc Ravallec, Thierry Dupressoir, Philippe Fournier, Biologie Intégrative et Virologie des Insectes [Univ. de Montpellier II] (BIVI), Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), IMT - MINES ALES (IMT - MINES ALES), Institut Mines-Télécom [Paris] (IMT), and Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)
Subjects: Time Factors, media_common.quotation_subject, Immunology, Endocytic cycle, Active Transport, Cell Nucleus, Spodoptera, Endocytosis, Microbiology, Clathrin, Virus, Cell Line, 03 medical and health sciences, Virology, Animals, Densovirus, Internalization, Cytoskeleton, 030304 developmental biology, media_common, 0303 health sciences, biology, 030306 microbiology, fungi, Receptor-mediated endocytosis, LEPIDOPTERE, Virus Internalization, 3. Good health, Virus-Cell Interactions, Kinetics, Microscopy, Electron, INSECTE, Insect Science, JUNONIA COENIA, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, biology.protein, Intracellular
Abstract: Junonia coenia densovirus (JcDNV) is an ambisense insect parvovirus highly pathogenic for lepidopteran pests at larval stages. The potential use of DNVs as biological control agents prompted us to reinvestigate the host range and cellular mechanisms of infection. In order to understand the early events of infection, we set up a functional infection assay in a cell line of the pest Lymantria dispar to determine the intracellular pathway undertaken by JcDNV to infect a permissive lepidopteran cell line. Our results show that JcDNV particles are rapidly internalized into clathrin-coated vesicles and slowly traffic within early and late endocytic compartments. Blocking late-endocytic trafficking or neutralizing the pH with drugs inhibited infection. During internalization, disruption of the cytoskeleton, and inhibition of phosphatidylinositol 3-kinase blocked the movement of vesicles containing the virus to the nucleus and impaired infection. In summary, our results define for the first time the early endocytic steps required for a productive DNV infection.
Published: 2009
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45. Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp

Author: Marc Ravallec, Miguel López-Ferber, Frédéric Fleury, Corinne Labrosse, Julien Varaldi, Michel Boulétreau, Génétique et évolution des interactions hôtes-parasites, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), and Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)
Subjects: 0106 biological sciences, Male, [SDV.OT]Life Sciences [q-bio]/Other [q-bio.OT], Physiology, media_common.quotation_subject, Wasps, Zoology, Insect Viruses, Oviducts, Leptopilina, 010603 evolutionary biology, 01 natural sciences, Polymerase Chain Reaction, Virus, Competition (biology), Parasitoid wasp, Parasitoid, Host-Parasite Interactions, 03 medical and health sciences, Microscopy, Electron, Transmission, RNA, Ribosomal, 16S, Animals, 030304 developmental biology, media_common, 0303 health sciences, biology, Behavior, Animal, Host (biology), Ecology, fungi, Virion, Tetracycline, biology.organism_classification, Anti-Bacterial Agents, Drosophila melanogaster, Phenotype, Insect Science, Female, Adaptation, Rifampin
Abstract: In parasitoids, the adaptive significance of superparasitism (laying of egg(s) in already parasitized hosts) has been the subject of strong controversy. The current view is to interpret this behaviour as an adaptation to increased competition for hosts, because the supernumerary egg still has a chance to win possession for the host. However, we recently discovered that in the solitary parasitoid Leptopilina boulardi, superparasitism is rather caused by an unknown infectious element: stable non superparasitizing lineages (NS) are transformed into stable superparasitizing lineages (S) after eggs from both lineages have competed inside the same host (superparasitism). In this report, we investigate the nature and location of the causative agent. Involvement of bacteria is unlikely because antibiotic treatments do not affect wasp phenotype and because bacterial 16S ribosomal DNA was not detected using PCR. We report successful injection experiments showing that the causative agents are located in wasp poison gland and ovaries and are stably inherited. Electron microscopic studies demonstrate that long filamentous virus particles located in wasp oviducts are strongly associated with superparasitism behaviour, leading to reconsider the adaptive significance of this behaviour in parasitoids. Interestingly, parasitoids are often infected with similar viruses for which no phenotypic effect has been documented. This raises the possibility that they could induce the same behavioural manipulation.
Published: 2006

46. Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels

Author: Jousset Fx, Anne-Nathalie Volkoff, Galibert L, Frédérique Hilliou, René Feyereisen, Philippe Fournier, Pierre Delobel, Sofer L, Marc Ravallec, Barat-Houari M, Emeline Deleury, Janick Rocher, Biologie Intégrative et Virologie des Insectes [Univ. de Montpellier II] (BIVI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2), Réponse des Organismes aux Stress Environnementaux (ROSE), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Sciences Pour l'Oenologie (SPO), Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut de Recherche pour le Développement (IRD [Nouvelle-Calédonie])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université Montpellier 1 (UM1)-Université de Montpellier (UM)-Institut National de la Recherche Agronomique (INRA), and Université Montpellier 1 (UM1)-Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)
Subjects: Hemocytes, Fat Body, TRANSCRIPTIONAL VARIATIONS, Autoantigens, SPODOPTERA FRUGIPERDA, cDNA MICROARRAY, GENE EXPRESSION, POLYDNAVIRUS, IMMUNE RESPONSE, LEPIDOPTERA, RELATION HOTE PARASITOIDE, Oligonucleotide Array Sequence Analysis, Genetics, Receptors, Scavenger, 0303 health sciences, Enzyme Precursors, biology, Polydnavirus, 030302 biochemistry & molecular biology, Prophenoloxidase, Insect Proteins, Female, DNA microarray, Catechol Oxidase, Biotechnology, Research Article, expression génique, lcsh:QH426-470, Galectins, lcsh:Biotechnology, réponse immunitaire, Genes, MHC Class II, Down-Regulation, Spodoptera, 03 medical and health sciences, Complementary DNA, lcsh:TP248.13-248.65, Animals, Lectins, C-Type, RNA, Messenger, Selection, Genetic, Gene, 030304 developmental biology, [SDV.GEN]Life Sciences [q-bio]/Genetics, Innate immune system, Gene Expression Profiling, fungi, Genetic Variation, biology.organism_classification, Immunity, Innate, Gene expression profiling, Protein Subunits, lcsh:Genetics, Polydnaviridae, Calreticulin
Abstract: Background Genomic approaches provide unique opportunities to study interactions of insects with their pathogens. We developed a cDNA microarray to analyze the gene transcription profile of the lepidopteran pest Spodoptera frugiperda in response to injection of the polydnavirus HdIV associated with the ichneumonid wasp Hyposoter didymator. Polydnaviruses are associated with parasitic ichneumonoid wasps and are required for their development within the lepidopteran host, in which they act as potent immunosuppressive pathogens. In this study, we analyzed transcriptional variations in the two main effectors of the insect immune response, the hemocytes and the fat body, after injection of filter-purified HdIV. Results Results show that 24 hours post-injection, about 4% of the 1750 arrayed host genes display changes in their transcript levels with a large proportion (76%) showing a decrease. As a comparison, in S. frugiperda fat body, after injection of the pathogenic JcDNV densovirus, 8 genes display significant changes in their transcript level. They differ from the 7 affected by HdIV and, as opposed to HdIV injection, are all up-regulated. Interestingly, several of the genes that are modulated by HdIV injection have been shown to be involved in lepidopteran innate immunity. Levels of transcripts related to calreticulin, prophenoloxidase-activating enzyme, immulectin-2 and a novel lepidopteran scavenger receptor are decreased in hemocytes of HdIV-injected caterpillars. This was confirmed by quantitative RT-PCR analysis but not observed after injection of heat-inactivated HdIV. Conversely, an increased level of transcripts was found for a galactose-binding lectin and, surprisingly, for the prophenoloxidase subunits. The results obtained suggest that HdIV injection affects transcript levels of genes encoding different components of the host immune response (non-self recognition, humoral and cellular responses). Conclusion This analysis of the host-polydnavirus interactions by a microarray approach indicates that the presence of HdIV induces, directly or indirectly, variations in transcript levels of specific host genes, changes that could be responsible in part for the alterations observed in the parasitized host physiology. Development of such global approaches will allow a better understanding of the strategies employed by parasites to manipulate their host physiology, and will permit the identification of potential targets of the immunosuppressive polydnaviruses.
Published: 2006
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47. Establishment of cell lines from the wasp Hyposoter didymator (Hym., Ichneumonidae) containing the symbiotic polydnavirus H. didymator ichnovirus

Author: Dominique Ray, Janick Rocher, Gérard Devauchelle, P. Barry, Marc Ravallec, Martine Duonor-Cérutti, and Anne-Nathalie Volkoff
Subjects: food.ingredient, Molecular Sequence Data, Wasps, Biology, Cell Line, food, Transcription (biology), Virology, Sequence Homology, Nucleic Acid, Botany, Gene expression, Animals, Northern blot, Symbiosis, Gene, Southern blot, Base Sequence, Polydnavirus, biology.organism_classification, Molecular biology, Microscopy, Electron, Viral replication, Polydnaviridae, DNA, Viral, RNA, Viral, Ichnovirus
Abstract: Cell lines derived from polydnavirus-associated wasps should constitute a valuable tool for investigations of polydnavirus replication, but none is yet available. In this work, we describe the first cell lines, named Hd-AA, -AD, -BBA and -K, to have been established from the ichneumonid wasp Hyposoter didymator, associated with the polydnavirus H. didymator ichnovirus (HdIV). Southern blot analysis indicated that the viral DNA was present in all four cell lines and co-localized with high molecular mass DNA, probably the wasp chromosomes. Northern blot analysis of mRNAs extracted from the AA cell line showed transcription of some HdIV-encoded genes, although at low level. The effects of ecdysone treatment, HdIV re-infection and 42 °C heat-shock were analysed in the AA cell line. No effect was detected at the DNA (virus replication) or RNA (gene expression) levels, which may be due to the limitation of the present available tools.
Published: 2004

48. Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

Author: Marc Ravallec, Pascal Esperandieu, Françoise Roquet, Stéphane Blanc, Martin Drucker, Alberto Fereres, Eugénie Hébrard, Jean-Claude Mani, Rémy Froissart, Martine Pugnière, Marilyne Uzest, Biologie Intégrative et Virologie des Insectes [Univ. de Montpellier II] (BIVI), and Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)
Subjects: 0106 biological sciences, Baculoviridae, Time Factors, Viral protein, viruses, Blotting, Western, Genetic Vectors, Plasma protein binding, virus, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, medicine.disease_cause, 01 natural sciences, Models, Biological, 03 medical and health sciences, Plasmid, Caulimovirus, medicine, Animals, 030304 developmental biology, 0303 health sciences, Aphid, Multidisciplinary, biology, fungi, transmission virale, food and beverages, Immunogold labelling, séquence nucléotidique, biochemical phenomena, metabolism, and nutrition, Biological Sciences, biology.organism_classification, système hétérologue, Virology, Immunohistochemistry, infection, Recombinant Proteins, 3. Good health, Microscopy, Electron, INSECTE, Aphids, DNA, Viral, Cauliflower mosaic virus, cellule, accumulation, 010606 plant biology & botany, Plasmids, Protein Binding
Abstract: Interactions between Cauliflower mosaic virus (CaMV) and its aphid vector are regulated by the viral protein P2, which binds to the aphid stylets, and protein P3, which bridges P2 and virions. By using baculovirus expression of P2 and P3, electron microscopy, surface plasmon resonance, affinity chromatography, and transmission assays, we demonstrate that P3 must be previously bound to virions in order that attachment to P2 will allow aphid transmission of CaMV. We also show that a P2:P3 complex exists in the absence of virions but is nonfunctional in transmission. Hence, unlike P2, P3 and virions cannot be sequentially acquired by the vector. Immunogold labeling revealed the predominance of spatially separated P2:P3 and P3:virion complexes in infected plant cells. This specific distribution indicates that the transmissible complex, P2:P3:virion, does not form primarily in infected plants but in aphids. A model, describing the regulating role of P3 in the formation of the transmissible CaMV complex in planta and during acquisition by aphids, is presented, and its consequences are discussed.
Published: 2002

49. Temporal expression of the AcMNPV lef-4 gene and subcellular localization of the protein

Author: David Durantel, Miguel López-Ferber, Guy Croizier, and Marc Ravallec
Subjects: Transcription, Genetic, Blotting, Western, Molecular Sequence Data, Gene Expression, Biology, Moths, Spodoptera, Polymerase Chain Reaction, Primer extension, Cell Line, Viral Proteins, Start codon, Virogenic stroma, Virology, Animals, Amino Acid Sequence, RNA, Messenger, Microscopy, Immunoelectron, Gene, Antiserum, Messenger RNA, Base Sequence, fungi, Chromosome Mapping, biology.organism_classification, Blotting, Northern, Molecular biology, Stop codon, Nucleopolyhedroviruses, Autographa californica, DNA, Viral, RNA, Viral, Rabbits, Subcellular Fractions
Abstract: Autographa californica nucleopolyhedrovirus (AcMNPV) lef-4 gene [ORF 90; Ayres et al. (1994) Virology 202, 586–605] is involved in both late and very late gene expression [Passarelli and Miller (1993) Virology 197, 704–714]. The transcriptional properties of this gene have been analyzed. It is transcribed as a single 1.6-kb mRNA and transcripts were first detected 3 h postinfection (pi). The extremities of the transcript have been mapped by primer extension and 3′ RACE–PCR to positions −56 from the translation start codon and +96 downstream of the stop codon. A rabbit polyclonal antiserum has been raised against an internal polypeptide of LEF-4. A 55-kDa protein was observed by Western blot analysis from 5 h pi. LEF-4 localizes preferentially in the nucleus of infected cells and is associated with the virogenic stroma.
Published: 1998

50. Corrigendum to 'Venom gland extract is not required for successful parasitism in the polydnavirus-associated endoparasitoid Hyposoter didymator (Hym. Ichneumonidae) despite the presence of numerous novel and conserved venom proteins' [Insect Biochem. Mol. Biol. 43 (2013), 292–307]

Author: Tristan Dorémus, Dominique Colinet, Marylène Poirié, Eric Wajnberg, Julie Poulain, Véronique Jouan, Carole Azéma-Dossat, Serge Urbach, Edith Demettre, François Cousserans, Anne-Nathalie Volkoff, Jean-Luc Gatti, Isabelle Darboux, Marc Ravallec, and Jean-Michel Escoubas
Subjects: biology, Polydnavirus, media_common.quotation_subject, Parasitism, Venom, Insect, Venom gland, biology.organism_classification, Biochemistry, Hyposoter didymator, Ichneumonidae, Insect Science, Botany, Mole, Molecular Biology, media_common
Published: 2014
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