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Biology subjects

Drezen, J.-M.

Publications and source records attributed to Drezen, J.-M..

4 recordsLinked to original sources

Discovery of new endogenous viral elements in campoplegine wasps (Ichneumonidae, Campopleginae, Campoplex) suggests a widespread nudivirus domestication event

Viral endogenization events in the genomes of parasitoid wasps have led to the production of immunosuppressive particles that are injected into the host and that either contain DNA encoding virulence effectors or virulence proteins, essential for parasitism success. In some Campopleginae (Ichneumonidae) wasps, viral endogenisation involves the production of large dsDNA ichnoviruses encoding several dozens of rep virulence genes, to the exception of Venturia canescens. Instead, V. canescens harbours an endogenous nudivirus producing Virus-Like-Particles (VLPs) in which virulence proteins are wrapped into viral envelopes. Here, we described that this nudiviral domestication event is more ancient and widespread than previously thought as we identified homologous alphanudivirus sequences in the genomes of three Campopleginae species belonging to the genera Campoplex and Rimphoctona. We showed that Campoplex capitator produces morphologically similar VLPs to those of V. canescens with almost the same viral protein content. Strikingly, the virulence proteins are however different, suggesting that VLPs allow a high versatility in the molecular strategies used by the wasps in response to host selection pressures. Furthermore, a marked expansion of serpin and rep genes is present in Campoplex capitator, with one serpin and several REP proteins identified as major VLP components using proteomics. REP proteins are also well-described virulence factors initially shown to be delivered into hosts via the expression of rep genes coded by ichnovirus DNA. In Campoplex capitator, these proteins are packaged into nudivirus-derived VLPs indicating that convergent use of virulence factors can imply endogenous viruses of different origin and with different delivery mechanisms.

evolutionary biology↗

Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps

Animal venoms and other protein-based secretions that perform a variety of functions, from predation to defense, are highly complex cocktails of bioactive compounds. Gene duplication, accompanied by modification of the expression and/or function of one of the duplicates under the action of positive selection, followed by further duplication to produce multigene families of toxins is a well-documented process in venomous animals. This evolutionary model has been less described in parasitoid wasps, which use maternal fluids, including venom, to protect their eggs from encapsulation by the host immune system. Here, we evidence the convergent recruitment and accelerated evolution of two multigene families of RhoGAPs presumably involved in virulence in two unrelated parasitoid wasp species, Leptopilina boulardi (Figitidae) and Venturia canescens (Icheumonidae). In both species, these RhoGAPs are associated with vesicles that act as transport systems to deliver virulence factors, but are produced in different tissues: the venom gland in Leptopilina sp. and the ovarian calyx in V. canescens. We show that the gene encoding the cellular RacGAP1 is at the origin of the virulent RhoGAP families found in Leptopilina sp. and V. canescens. We also show that both RhoGAP families have undergone evolution under positive selection and that almost all of these RhoGAPs lost their GAP activity and GTPase binding ability due to substitutions in key amino acids. These results suggest an accelerated evolution and functional diversification of these vesicle-associated RhoGAPs in the two phylogenetically distant parasitoid species. The potential new function(s) and the exact mechanism of action of these proteins in host cells remain to be elucidated.

evolutionary biology↗

Somatic chromosomal integration of polydnavirus during parasitism triggered their germline infiltration in multiple lepidopteran families

Increasing numbers of horizontal transfer (HT) of genes and transposable elements are reported in insects. Yet the mechanisms underlying these transfers remain unknown. Here we firs t quantify and characterize the patterns of chromosomal integration of the polydnavirus (PDV) encoded by the Campopleginae Hyposoter didymator parasitoid wasp (HdIV) in somatic cells of parasitized fall armyworm (Spodoptera frugiperda). Polydnaviruses are domesticated viruses injected by wasps together with their eggs into their hosts in order to facilitate the development of wasp larvae. We found that six HdIV DNA circles integrate into the genome of host somatic cells. Each host haploid genome suffers between 23 and 40 integration events (IEs) on average 72 hours post parasitism. Almost all IEs are mediated by DNA double strand breaks occurring in the host integration motif (HIM) of HdIV circles. We show that despite their independent evolutionary origins, PDV from both Campopleginae and Braconidae wasps use remarkably similar mechanisms for chromosomal integration. Next, our similarity search performed on 775 genomes reveals that PDVs of both Campopleginae and Braconidae wasps have recurrently colonized the germline of dozens of lepidopteran species through the same mechanisms they use to integrate into somatic host chromosomes during parasitism. We found evidence of HIM-mediated HT of PDV DNA circles in no less than 124 species belonging to 15 lepidopteran families. Thus, this mechanism underlies a major route of HT of genetic material from wasps to lepidopterans with likely important consequences on lepidopterans.

evolutionary biology↗

Conserved and specific genomic features of endogenous polydnaviruses revealed by whole genome sequencing of two ichneumonid wasps

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 didymator and Campoletis 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.

genomics↗