Submitted to: Parasitoid Viruses: Symbionts and Pathogens
Publication Type: Book / Chapter
Publication Acceptance Date: November 20, 2011
Publication Date: January 1, 2012
Citation: Gundersen, D.E. 2012. Integration of Polydnavirus DNA into Host Cellular Genomic DNA. Parasitoid Viruses: Symbionts and Pathogens. In: Beckage, N.E, Drezen, J.M., editors. London, England: Academic Press, p. 99-113. Interpretive Summary: Parasitic wasps have potential for control of moth species that are pests of agricultural crops and forests. The survival of many of these wasps is enhanced by a virus, called a polydnavirus, that is injected along with the wasp egg into the host caterpillar pest. The wasp polydnavirus is different from every other characterized DNA viruses in several ways, including its lifecycle, which takes place between two insect hosts. In the first wasp host, the polydnavirus is present as an integrated part of the wasp genetic material in a form called “provirus”. In certain cells of the female wasp reproductive tract, the provirus is taken out of the genetic material and replicated before individual polydnavirus components are packaged as the second form, the virus. The virus is then injected into the second insect host, the caterpillar, where it has negative effects. In the current paper, the presence in the host cellular genetic material of the provirus form and the virus form is discussed. Long-term persistence of polydnavirus genetic material in infected caterpillar cells after infection with polydnavirus in culture suggests that at least some of the virus genome becomes integrated permanently into the cellular genetic material. This may also happen in living cells of the caterpillar, and we present new evidence for this here. General discussion is made of how the polydnavirus may help the wasp to survive. The information will help explain how the wasp causes the decline of the pest caterpillar and may enable new biocontrol strategies. This information will be of interest to university and industry scientists who are interested in how viruses work and/or in developing new virus-based strategies to control pests.
Technical Abstract: Polydnaviruses are unique insect viruses that are obligately associated with thousands of parasitoid wasp species in intimate mutualistic symbioses. Whereas most cases of virus infection of host cells leads to production of progeny virions, polydnaviruses have evolved by atypical lifecycle and replication strategies requiring two entirely separate insect hosts. In addition, polydnaviruses exist in two distinct forms, both as linear integrated provirus and as double strand circular form of genome segments packaged into virions. The linear integrated provirus form is transferred vertically through the parasitoid germline. The packaged circular form in virions is produced from the integrated proviral form in the parasitoid and is transferred horizontally by injection into the secondary host during oviposition along with egg(s) and parasitization-associated proteins, where upon infection viral genes are expressed and cause immune suppression, developmental arrest, and other negative impacts. Integration, the insertion of viral DNA into host-cell DNA, is a central theme in polydnavirus biology for provirus and packaged virion. In addition to analysis of vertical provirus integration, several studies have examined integration of the packaged form polydnavirus virion DNA in infected lepidopteran host cells, finding some, but not all, of the virus genome became integrated permanently into the secondary host cellular DNA, which potentially may also have occurred in vivo. Analysis of proviral and packaged polydnavirus genomes suggests unique sequence features of polydnaviruses themselves, as well as an association with an abundance of transposable elements. The intimacy in parasitism, unique replication and life strategies, novel structural features and organization of polydnavirus integrated proviral and circular packaged forms, and multiple associations with transposable elements, suggest numerous opportunities for genetic exchange and sequence integration among the primary host parasitoid, polydnavirus, and secondary lepidopteran hosts. These may contribute to observed gene interchanges into and out of proviral and encapsidated viral genomes and both insect host genomes that have shaped their content.