Genome-Wide Profiling of Diadegma semiclausum Ichnovirus Integration in Parasitized Plutella xylostella Hemocytes Identifies Host Integration Motifs and Insertion Sites

Ze-Hua Wang,Yue-Nan Zhou,Min Shi,Xue-Xin Chen,Xi-Qian Ye,Jing Yang,Jian-Hua Huang

doi:10.3389/fmicb.2020.608346

Abstract

Polydnaviruses (PDVs), classified into two genera, bracoviruses (BVs) and ichnoviruses (IVs), are large, double-stranded DNA viruses, which are beneficial symbionts of parasitoid wasps. PDVs do not replicate in their infected lepidopteran hosts. BV circles have been demonstrated to be integrated into host genomic DNA after natural parasitization. However, the integrations of IV circles in vivo remain largely unknown. Here, we analyzed the integration of Diadegma semiclausum ichnovirus (DsIV) in the genomic DNA of parasitized Plutella xylostella hemocytes. We found that DsIV circles are present in host hemocytes with non-integrated and integrated forms. Moreover, DsIV integrates its DNA circles into the host genome by two distinct strategies, conservatively, and randomly. We also found that four conserved-broken circles share similar motifs containing two reverse complementary repeats at their breaking sites, which were host integration motifs (HIMs). We also predicted HIMs of eight circles from other ichnoviruses, indicating that a HIM-mediated specific mechanism was conserved in IV integrations. Investigation of DsIV circle insertion sites of the host genome revealed the enrichment of microhomologies between the host genome and the DsIV circles at integration breakpoints. These findings will deepen our understanding of the infections of PDVs, especially IVs.

Highlights

Endoparasitoid wasps, one of the most species-rich animal groups on Earth, have developed various strategies to regulate their host’s physiology and development to ensure successful parasitism (Pennacchio and Strand, 2006; Ye et al, 2018)
Polydnaviruses (PDVs), divided into two genera, bracoviruses, and ichnoviruses, are doublestranded DNA viruses associated with parasitic wasps, which do not replicate in their infected caterpillar hosts
We identified the breaking sites of ichnovirus circles and the integration sites in the host genome

Summary

Introduction

Endoparasitoid wasps, one of the most species-rich animal groups on Earth, have developed various strategies to regulate their host’s physiology and development to ensure successful parasitism (Pennacchio and Strand, 2006; Ye et al, 2018). Polydnaviruses (PDVs) are obligatory symbionts of parasitoid wasps and are essential for the successful parasitism of thousands of species of parasitoid wasps. PDVs are present in the wasp genome as integrated proviruses (Webb, 1998; Strand and Burke, 2014). The assembly and replication of PDV virions that are injected into lepidopteran hosts during parasitoid oviposition occur only in the nuclei of ovarian calyx cells of female wasps (Gruber et al, 1996). PDVs infect most of the host immune cells and many other tissue cells as well after parasitization (Strand, 1994; Beck et al, 2007; Bitra et al, 2011), but they do not propagate themselves in the host cells

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