Polydnavirus Innexins Disrupt Host Cellular Encapsulation and Larval Maturation

Abstract

Polydnaviruses are dsDNA viruses associated with endoparasitoid wasps. Delivery of the virus during parasitization of a caterpillar and subsequent virus gene expression is required for production of an amenable environment for parasitoid offspring development. Consequently, understanding of Polydnavirus gene function provides insight into mechanisms of host susceptibility and parasitoid wasp host range. Polydnavirus genes predominantly are arranged in multimember gene families, one of which is the vinnexins, which are virus homologues of insect gap junction genes, the innexins. Previous studies of Campoletis sonorensis Ichnovirus Vinnexins using various heterologous systems have suggested the four encoded members may provide different functionality in the infected caterpillar host. Here, we expressed two of the members, vnxG and vnxQ2, using recombinant baculoviruses in susceptible host, the caterpillar Heliothis virescens. Following intrahemocoelic injections, we observed that >90% of hemocytes (blood cells) were infected, producing recombinant protein. Larvae infected with a vinnexin-recombinant baculovirus exhibited significantly reduced molting rates relative to larvae infected with a control recombinant baculovirus and mock-infected larvae. Similarly, larvae infected with vinnexin-recombinant baculoviruses were less likely to survive relative to controls and showed reduced ability to encapsulate chromatography beads in an immune assay. In most assays, the VnxG protein was associated with more severe pathology than VnxQ2. Our findings support a role for Vinnexins in CsIV and more broadly Ichnovirus pathology in infected lepidopteran hosts, particularly in disrupting multicellular developmental and immune physiology.

Genome, host genome integration, and gene expression in Diadegma fenestrale ichnovirus from the perspective of coevolutionary hosts

“…The second most common family, cys-motif, was represented by 10 members in DfIV. The cys-motif family is found in other ichnoviruses (eight members in DsIV) but not in bracoviruses (Zhang and Turnbull, 2021). Two cys-motif genes in CsIV (VHv1.1 and VHv1.4) affect the hemocytes so that the cellular immune system would be suppressed, to the benefit of the hymenopteran insect (Kim, 2005;Ye et al, 2018).…”

“…The fifth gene family, vinnexins, exhibits homology with the insect gap junction innexin genes and was predicted in DfIV with six members and in DsIV with seven. Vinnexin is a highly conserved protein in ichnoviruses and may interfere with host cell-cell communication (Phelan et al, 1998), alteration of cytoskeletal networks (Hasegawa et al, 2020), host cell encapsulation, molting, and larval maturation (Zhang and Turnbull, 2021). Here, the phylogenetic relationships of these five DfIV and DsIV gene families (rep, cys, PRRP, vankyrin, and vinnexin) were compared and found to be closely related.…”

A Polydnavirus Protein Tyrosine Phosphatase Negatively Regulates the Host Phenoloxidase Pathway

“…PDVs persist in a given wasp genome as proviruses with two distinct parts: structural core genes that are critical for the formation of virion particles, and proviral segments that serve as templates for the production of the virulence genes in its secondary host, primarily an insect in the Lepidoptera order [ 3 ]. These virulence genes alter host physiology, growth, and development, facilitating the survival of wasp offspring [ 1 , 4 , 5 , 6 , 7 ]. They are classified into gene families and contribute greatly to host immunosuppression and growth regulation [ 6 , 8 , 9 ].…”