Biology subjects

Volkoff, A.-N.

Publications and source records attributed to Volkoff, A.-N..

4 recordsLinked to original sources

bioRxiv2024

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

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), which derive from an unknown virus and produce virions in ovary calyx cells during the pupal and adult stages of female wasps. Females inject IV virions into host insects when laying eggs. Virions infect cells which express IV genes with functions required for wasp progeny development. IVs have a dispersed genome consisting of two genetic components: proviral segment loci that serve as templates for circular dsDNAs that are packaged into capsids, and genes from an ancestral virus controlling virion production. Because of the lack of homology with known viral genes, the molecular control mechanisms of IV genome are largely uncharacterized. We generated a chromosome-scale genome assembly for Hyposoter didymator and identified a total of 67 H. didymator ichnovirus (HdIV) loci distributed across the 12 wasp chromosomes. By analyzing genomic DNA levels, we found that all HdIV loci were locally amplified in calyx cells during the wasp pupal stage, suggesting the implication of viral proteins in DNA replication. We tested a candidate HdIV gene, U16, encoding a protein with a conserved domain found in primases and which is transcribed in calyx cells during the initial stages of replication. Knockdown of U16 by RNA interference inhibited amplification of all HdIV loci, as well as HdIV gene transcription, circular molecule production and virion morphogenesis in calyx cells. Altogether, our results showed that viral DNA amplification is an early step of IV replication essential for virions production, and demonstrated the implication of the viral gene U16 in this process. Author SummaryParasitoid "domesticated endogenous viruses" (DEVs) provide a fascinating example of eukaryotes acquiring new functions through integration of a virus genome. DEVs consist of multiple loci in the genomes of wasps. Upon activation, these elements collectively orchestrate the production of virions or virus-like particles that are crucial for successful parasitism of host insects. Despite the significance of DEVs for parasitoid biology, the mechanisms regulating key steps in virion morphogenesis are largely unknown. In this study, we focused on the ichneumonid parasitoid Hyposoter didymator, which harbors an ichnovirus consisting of 67 proviral loci. Our findings reveal that all proviral loci are simultaneously amplified in ovary calyx cells of female wasps during the early pupal stage suggesting a hijacking of cellular replication complexes by viral proteins. We tested the implication of such a candidate, U16, encoding a protein with a weakly conserved primase C-terminal domain. Silencing U16 resulted in inhibited viral DNA amplification and virion production, underscoring the key role of this gene for ichnovirus replication. This study provides evidence that genes involved in viral DNA replication have been conserved during the domestication of viruses in the genomes of ichneumonid wasps.

microbiology↗

bioRxiv2023

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↗

bioRxiv2022

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↗

bioRxiv2019

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↗