State of the art

In the B2iHP team, we are interested in the interactions between lepidopteran crop pests and their parasitic wasps, also named “parasitoids”. More particularly, we are interested in the factors that allow the parasitoids to develop in their hosts (generally arthropods).

Parasitoid insects are characterized by being free-living in the adult stage and parasitic during their immature stages. There are thousands of species of parasitoids, with very diverse lifestyles. Some develop outside their host (ectoparasitoids), others inside (endoparasitoids); some parasitize insect eggs, others larvae or pupae (oophagous, larval or pupal parasitoids). As a rule, parasitoids lead to the death of their host, which explains why these species are frequently used in biological control programs against crop pests.

In the team, we mainly focus on species from the Ichneumonidae family, which develop inside an insect larva (endoparasitoids). We are particularly interested in the species where females are able, thanks to the presence of endogenous viral sequences in their genome, to produce virus-like particles in their ovaries. When they lay their egg in another insect (usually a lepidopteran larva), the females also inject these particles, which are necessary for the larval development of their offspring (Figure 1). Depending on the parasitoid species, these virus-like particles contain molecules that may be of different nature; they may contain either proteins (e.g. Venturia canescens) or double-stranded DNA molecules, which is the case for the majority of the species studied to date (e.g. Hyposoter didymator). The particles containing DNA molecules belong to the polydnavirus (PDV) family, a family recognized by the International Committee on Taxonomy of Viruses (ICTV) in the 1990s.

Figure 1. Life cycle of a parasitoid wasp. Example of a polydnavirus (PDV) associated species. Virus particles are produced in the ovaries of females during their pupal and adult stages. Production takes place exclusively in a specialized tissue, the calyx. The virus particles produced are released into the oviducts and then injected into the host insect (in this case a caterpillar) when the wasp lays its eggs. Once inside the caterpillar, the PDV particles infect all the tissues of the insect, and the genes encoded by the packaged DNA molecules are expressed. The expression of these genes transferred via the particles leads to physiological alterations in the caterpillar that are beneficial and often necessary for the development of the endoparasitoid (inhibition of the host caterpillar's immune response, modulation of its development, etc.). Once the parasitoid larva (or larvae) has completed its development, it emerges from the caterpillar, which dies soon after. The parasitoid then weaves a cocoon in which pupation takes place, leading to the emergence of a new adult wasp. Figure taken from the team's publication DOI: 10.1016/B978-0-12-809633-8.21556-2.

The first studies on PDVs date back to the 1970s. Their name "polydnavirus" derives from the fact that the particles present in the ovaries of female parasitoids contain several circular dsDNA molecules. PDVs have been identified in parasitoid species belonging to two major Hymenoptera families, the Braconidae and the Ichneumonidae, defining two PDV taxa, the Bracovirus and the Ichnovirus, respectively.

The parasitoid-PDV association represents a unique model of domestication of a virus by a eukaryotic organism for its own benefit. Indeed, current PDVs are derived from the integration of a viral genome during the evolution of parasitoids. It is now known that bracoviruses result from the integration of a nudivirus genome in an ancestor braconid (Bézier et al, 2009), whereas ichnoviruses result from the integration of a viral genome whose identity is not yet determined in an ancestor ichneumonid (Volkoff et al, 2010). Subsequently to this integration event, a large part of the viral genome has been maintained in the chromosomes of the parasitoid wasps. It is the activation of these conserved viral sequences in the wasp genome, which occurs specifically in the ovaries of female parasitoids, that leads to the production of the particles necessary for parasitoid success.

The model mainly studied in the team is the ichneumonid campoplegine wasp Hyposoter didymator, a natural parasitoid of Helicoverpa armigera caterpillars able to also parasitize other crop pests. H. didymator is associated with the Ichnovirus HdIV (Hyposoter didymator Ichnovirus). Sequence analysis of the H. didymator genome showed that it contained tens of endogenous viral elements (EVEs) scattered throughout it (Legeai et al, 2020). EVEs consist either in regions carrying genes deriving from the viral ancestor, that were named “replication genes” because they are involved in particle production, or in sequences that serve as templates for the circular DNA molecules further encapsidated, or 'segments' (Figure 2). Only the segments are incorporated into the particles and thus transferred during parasitism; the replication genes remain resident in the wasp.

The main objectives of the team are:

To understand the molecular mechanisms underlying the two key steps in the life cycle of the parasitoid-PDV complex:

• The particle production, which takes place specifically in the calyx cells of the parasitoid.
• The manipulation by the PDV of the physiology of the parasitized insect, which ultimately allows the larval development of the parasitoid.

To this end, two complementary research areas are addressed:

Research axis 1. Mechanisms involved in the production of PDV particles in the parasitoid.

In this line of research, we are interested in better understanding the stages of viral replication leading to the production of particles specifically in the calyx cells during the pupal and adult stages of the female parasitoid.

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Research axis 2. Molecular mechanisms involved in host-PDV interactions: impact on the immune response.

In this line of research, we are interested in the physiological, cellular and molecular consequences of viral infection for the parasitized caterpillar and the function of viral proteins expressed during parasitism.

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In parallel, we are interested in the diversity of virus-ichneumonid wasp associations.

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Key publications

Legeai, F., Santos, B. F., Robin, S., Bretaudeau, A., Dikow, R. B., Lemaitre, C., Jouan, V., Ravallec, M., Drezen, J.-M., Tagu, D., Baudat, F., Gyapay, G., Zhou, X., Liu, S., Webb, B. A., Brady, S. G., Volkoff, A.-N. 2020. Genomic architecture of endogenous ichnoviruses reveals distinct evolutionary pathways leading to virus domestication in parasitic wasps. BMC Biology, 18. DOI: 89.10.1186/s12915-020-00822-3. 

Lorenzi, A., Ravallec, M., Eychenne, M., Jouan, V., Robin, S., Darboux, I., Legeai, F., Gosselin-Grenet, A.S., Sicard, M., Stoltz, D., Volkoff, A.N. 2019. RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps. PLoS Pathogens, 15 (12), e1008210. DOI: 10.1371/journal.ppat.1008210. 

Pichon, A., Bezier, A., Urbach, S., Aury, J.-M., Jouan, V., Ravallec, M., Guy, J., Cousserans, F., Theze, J., Gauthier, J., Demettre, E., Schmieder, S., Wurmser, F., Sibut, V., Poirie, M., Colinet, D., da Silva, C., Couloux, A., Barbe, V., Drezen, J.-M., Volkoff, A.-N. 2015. Recurrent DNA virus domestication leading to different parasite virulence strategies. Science Advances, 1 (10), 9 p. DOI: 10.1126/sciadv.1501150. 

Visconti, V., Eychenne, M., Darboux, I. 2019. Modulation of antiviral immunity by the ichnovirus HdIV in Spodoptera frugiperda. Molecular Immunology, 108, 89-101. DOI: 10.1016/j.molimm.2019.02.011.

Volkoff AN, Jouan V, Urbach S, Samain S, Bergoin M, Wincker P, Demettre E, Cousserans F, Provost B, Coulibaly F, Legeai F, Beliveau C, Cusson M, Gyapay G, Drezen JM. 2010. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathogens, 6(5), e1000923. DOI: 10.1371/journal.ppat.1000923.

Recent reviews on the subject (produced by the team)

Volkoff, A.-N., Huguet, E. 2021. Polydnaviruses (Polydnaviridae), in: Bamford, D.H., Zuckerman, M. (Eds.), Encyclopedia of Virology (Fourth Edition). Academic Press, Oxford, pp. 849-857. DOI: 10.1016/B978-0-12-809633-8.21556-2.

Cusumano, A., Volkoff, A.N. 2021. Influence of parasitoid-associated viral symbionts on plant-insect interactions and biological control. Current Opinion in Insect Science, 44, 64-71. DOI: 10.1016/j.cois.2021.03.009.

Volkoff, A.-N., Cusson, M. 2020. The unconventional viruses of Ichneumonid parasitoid wasps. Viruses, 12, 1170. DOI: 10.3390/v12101170.

Lorenzi, A., Volkoff, A.-N. 2020. Les Polydnavirus, un exemple unique de machinerie virale domestiquée par des insectes parasitoïdes. Virologie (Montrouge), 24 (2), 113-125. DOI: 10.1684/vir.2020.0835. 

Darboux, I., Cusson, M., Volkoff, A. N. 2019. The dual life of ichnoviruses. Current Opinion in Insect Science, 32, 47-53. DOI: 10.1016/j.cois.2018.10.007.