Evidence for an ichnovirus machinery in parasitoids of coleopteran larvae

Robin, Stéphanie; Ravallec, Marc; Frayssinet, Marie; Whitfield, James B.; Jouan, Véronique; Legeai, Fabrice; Volkoff, Anne Nathalie

doi:10.1016/j.virusres.2019.02.001

“…Another limitation of this study is that it is focused only on lepidopterans, the major hosts of PDV-encoding braconid and campoplegine parasitoid wasps ( Gauld 1988 ). Yet, some wasps within the two families are known to parasitize non-lepidopteran hosts ( Robin et al 2019 ) and it will be interesting to extend the search for HIM-mediated HT of PDV circles to a larger diversity of hosts. Extending the search to species not known to be hosts of parasitoid wasps may also reveal unexpected wasp–host interactions.…”

Section: Discussionmentioning

confidence: 99%

Massive Somatic and Germline Chromosomal Integrations of Polydnaviruses in Lepidopterans

Heisserer

¹

,

Muller

²

,

Jouan

³

et al. 2023

Molecular Biology and Evolution

Self Cite

View full text Add to dashboard Cite

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 first 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.

show abstract

“…Another limitation of this study is that it is focused only on lepidopterans, the major hosts of PDVencoding braconid and campoplegine parasitoid wasps (Gauld 1988). Yet, some wasps within the two families are known to parasitize non-lepidopteran hosts (Robin et al 2019) and it will be interesting to extend the search for HIM-mediated HT of PDV circles to a larger diversity of hosts. Extending the search to species not known to be hosts of parasitoid wasps may also reveal unexpected wasp-host interactions.…”

Section: Limitations Of the Current Study And Perspectivesmentioning

confidence: 99%

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

Gilbert

¹

,

Heisserer

²

,

Muller

³

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

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 first 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.

show abstract

“…Banchine IV virions typically harbor several nucleocapsids [ 22 , 23 ] whereas most virions of campoplegine IVs contain a single nucleocapsid ( Figure 2 ). However, virions with multiple nucleocapsids have recently been described for the campoplegine wasp Bathyplectes sp., which parasitizes coleopteran larvae [ 24 ]; the other campoplegine wasps that have been shown to carry IVs develop in lepidopteran larvae. Banchine and campoplegine IVs also differ with respect to their packaged genomes: the former have far more segments than the latter, and the genes they contain are strikingly different ( Table 1 ).…”

Section: Diversity Of Ichneumonid Virus Particlesmentioning

confidence: 99%

“…Furthermore, homologs to HdIV structural genes were identified in the calyx transcriptome of other IV-associated campoplegine wasps, namely Tranosema rostrale [ 19 ] and Bathyplectes sp. [ 24 ], or in the genome of C. sonorensis [ 30 ]. This clearly indicated that the set of virion structural genes was conserved among campoplegine wasps known to produce IVs.…”

Section: Evidence For a Viral Origin Of Ichnovirusesmentioning

confidence: 99%

The Unconventional Viruses of Ichneumonid Parasitoid Wasps

Volkoff

¹

,

Cusson

²

2020

Viruses

Self Cite

View full text Add to dashboard Cite

To ensure their own immature development as parasites, ichneumonid parasitoid wasps use endogenous viruses that they acquired through ancient events of viral genome integration. Thousands of species from the campoplegine and banchine wasp subfamilies rely, for their survival, on their association with these viruses, hijacked from a yet undetermined viral taxon. Here, we give an update of recent findings on the nature of the viral genes retained from the progenitor viruses and how they are organized in the wasp genome.

show abstract

Evidence for an ichnovirus machinery in parasitoids of coleopteran larvae

Cited by 9 publications

References 24 publications

Massive Somatic and Germline Chromosomal Integrations of Polydnaviruses in Lepidopterans

Massive Somatic and Germline Chromosomal Integrations of Polydnaviruses in Lepidopterans

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

The Unconventional Viruses of Ichneumonid Parasitoid Wasps

Contact Info

Product

Resources

About