Massive Somatic and Germline Chromosomal Integrations of Polydnaviruses in Lepidopterans

Abstract

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.

Microhomology‐mediated repair machinery and its relationship with HPV‐mediated oncogenesis

“…The wildtype virus preferentially integrates into chromosome 19 mediated by the viral replicase and contributes to viral latency; whereas, the derived vectors missing this gene integrate at a lower rate in unstable regions of the host genome. Lastly, other more divergent DNA viruses of invertebrates have been observed to integrate through MHS‐related mechanisms as evidenced by the symbiotic polydnaviruses of parasitoid wasps 118,119 . None of these viruses are associated with cancers of their respective hosts, and integration seems to be part of the virus lifecycle, unlike the previously discussed viruses.…”

Microhomology-mediated repair machinery and its relationship with HPV-mediated oncogenesis

“…Lastly, other more divergent DNA viruses of invertebrates have been observed to integrate through MHS-related mechanisms as evidenced by the symbiotic polydnaviruses of parasitoid wasps. 103,104 None of these viruses are associated with cancers of their respective hosts, and integration seems to be part of the virus lifecycle, unlike the previously discussed viruses. This plus the observation that many endogenized viruses also show evidence of MHS-mediated integration raises the question of whether MHS-mediated repair pathways are useful for the virus or serve as an innate immune response for the host.…”