1887

Abstract

polydnavirus (GiPDV) is essential for successful parasitization of the larval stage of the lepidopteran (gypsy moth) by the endoparasitic wasp . This virus has not been characterized previously. Ultrastructural studies of GiPDV showed that virions had a rod-like or rectangular form and each contained as many as ten nucleocapsids enclosed by a single unit membrane envelope. Field inversion gel electrophoresis (FIGE) analysis of the virus genomic DNA revealed that GiPDV had a segmented genome composed of 13 dsDNA segments, ranging in size from approximately 11 kb to more than 30 kb. Four genomic segments were present in higher molar concentration than the others. Further characterization of the GiPDV genome yielded several cDNA clones which derived from GiPDV-specific mRNAs, and Northern blot analysis confirmed expression of isolated cDNA clones in the parasitized host. Each was present on more than one GiPDV genomic DNA segment, suggesting the existence of related sequences among DNA segments. It has been proposed previously that in polydnavirus systems, genome segmentation, hypermolar ratio segments and segment nesting may function to increase the copy number of essential genes and to increase the levels of gene expression in the absence of virus replication. The present data support this notion and suggest that GiPDV morphology and genomic organization may be intrinsically linked to the function and evolutionary strategies of the virus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19234-0
2003-08-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/8/vir842051.html?itemId=/content/journal/jgv/10.1099/vir.0.19234-0&mimeType=html&fmt=ahah

References

  1. Albrecht, U., Wyler, T., Pfister-Wilhelm, R., Gruber, A., Stettler, P., Heiniger, P., Kurt, E., Schümperli, D. & Lanzrein, B. ( 1994; ). Polydnavirus of the parasitic wasp Chelonus inanitus (Braconidae): characterization, genome organization and time point of replication. J Gen Virol 75, 3353–3363.[CrossRef]
    [Google Scholar]
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  3. Beckage, N. E., Tan, F. F., Schleifer, K. W., Lane, R. D. & Cherubin, L. L. ( 1994; ). Characterization and biological effects of Cotesia congregata polydnavirus on host larvae of the tobacco hornworm, Manduca sexta. Arch Insect Biochem Physiol 26, 165–195.[CrossRef]
    [Google Scholar]
  4. Bell, R. A., Owens, C. D., Shapiro, M. & Tardif, J. R. ( 1981; ). Development of mass-rearing technology. In The Gypsy Moth: Research Toward Integrated Pest Management, pp. 599–633. Edited by C. C. Doane & M. L. McManus. USDA Technical Bulletin 1584.
  5. Chen, Y.-P., Taylor, P., Shapiro, M. & Gundersen-Rindal, D. ( 2003; ). Quantitative expression analysis of a Glyptapanteles indiensis polydnavirus protein tyrosine phosphatase gene in its natural lepidopteran host, Lymantria dispar. Insect Mol Biol 12, 271–280.[CrossRef]
    [Google Scholar]
  6. Cui, L. & Webb, B. A. ( 1997; ). Homologous sequences in the Campoletis sonorensis polydnavirus genome are implicated in replication and nesting of the W segment family. J Virol 71, 8504–8513.
    [Google Scholar]
  7. Fleming, J. G. W. ( 1992; ). Polydnaviruses: mutualists and pathogens. Annu Rev Entomol 37, 401–425.[CrossRef]
    [Google Scholar]
  8. Fleming, J. G. W. & Krell, P. J. ( 1993; ). Polydnavirus genome organization. In Parasites and Pathogens of Insects, pp. 189–225. Edited by N. E. Beckage, S. N. Thompson & B. A. Federici. San Diego: Academic Press.
  9. Fleming, J. G. W. & Summers, M. D. ( 1986; ). Campoletis sonorensis endoparasitic wasps contain forms of Campoletis sonorensis virus-DNA suggestive of integrated and extrachromosomal polydnavirus DNAs. J Virol 57, 552–562.
    [Google Scholar]
  10. Fleming, J. G. W. & Summers, M. D. ( 1991; ). Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc Natl Acad Sci U S A 88, 9770–9774.[CrossRef]
    [Google Scholar]
  11. Gundersen-Rindal, D. & Dougherty, E. M. ( 2000; ). Evidence for integration of Glyptapanteles indiensis PDV DNA into the chromosome of Lymantria dispar in vitro. Virus Res 66, 27–37.[CrossRef]
    [Google Scholar]
  12. Johner, A. & Lanzrein, B. ( 2002; ). Characterization of two genes of the polydnavirus of Chelonus inanitus and their stage-specific expression in the host Spodoptera littoralis. J Gen Virol 83, 1075–1085.
    [Google Scholar]
  13. Krell, P. J. ( 1987; ). Polydnavirus replication and tissue organization of infected cells in the parasitic wasp Diadegma terebrans. Can J Microbiol 33, 176–190.[CrossRef]
    [Google Scholar]
  14. Krell, P. J. ( 1991; ). The polydnaviruses, multipartite DNA viruses from parasitic hymenoptera. In Viruses of Invertebrates, pp. 141–177. Edited by E. Kurstak. New York: Marcel Dekker.
  15. Krell, P. J. & Stoltz, D. B. ( 1980; ). Virus-like particles in the ovary of an ichneumonid wasp. Purification and preliminary characterization. Virology 101, 408–418.[CrossRef]
    [Google Scholar]
  16. Krell, P. J., Summers, M. D. & Vinson, S. B. ( 1982; ). Virus with multipartite superhelical DNA genome from the ichneumonid parasitoid Campoletis sonorensis. J Virol 43, 859–870.
    [Google Scholar]
  17. Lavine, M. D. & Beckage, N. E. ( 1995; ). Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitol Today 11, 368–378.[CrossRef]
    [Google Scholar]
  18. Lawrence, P. O. & Lanzrein, B. ( 1993; ). Hormonal interactions between insect endoparasites and their host insects. In Parasites and Pathogens of Insects, pp. 59–86. Edited by N. E. Beckage, S. N. Thompson & B. A. Federici. San Diego: Academic Press.
  19. Norton, W. N. & Vinson, S. B. ( 1983; ). Correlating the initiation of virus replication with a specific pupal developmental phase of an ichneumonid parasitoid. Cell Tissue Res 231, 387–398.
    [Google Scholar]
  20. Stoltz, D. B. ( 1993; ). The polydnavirus life cycle. In Parasites and Pathogens of Insects, pp. 167–187. Edited by N. E. Beckage, S. N. Thompson & B. A. Federici. San Diego: Academic Press.
  21. Stoltz, D. B. & Vinson, S. B. ( 1979; ). Viruses and parasitism in insects. Adv Virus Res 24, 125–171.
    [Google Scholar]
  22. Stoltz, D. B. & Whitfield, J. B. ( 1992; ). Viruses and virus-like entities in the parasitic hymenoptera. J Hymenopt Res 1, 125–139.
    [Google Scholar]
  23. Stoltz, D. B., Krell, P., Summers, M. D. & Vinson, S. B. ( 1984; ). Polydnaviridae – a proposed family of insect viruses with segmented, double stranded, circular DNA genome. Intervirology 21, 1–4.[CrossRef]
    [Google Scholar]
  24. Stoltz, D. B., Guzo, D. & Cook, D. ( 1986; ). Studies on polydnavirus transmission. Virology 155, 120–131.[CrossRef]
    [Google Scholar]
  25. Strand, M. R. & Pech, L. L. ( 1995; ). Immunological basis for compatibility in parasitoid-host relationships. Annu Rev Entomol 40, 31–56.[CrossRef]
    [Google Scholar]
  26. Strand, M. R., McKenzie, D. I., Grassl, V., Dover, B. A. & Aiken, M. ( 1992; ). Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens. J Gen Virol 73, 1627–1635.[CrossRef]
    [Google Scholar]
  27. Strand, M. R., Witherell, R. A. & Trudeau, D. ( 1997; ). Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. J Virol 71, 2146–2165.
    [Google Scholar]
  28. Summers, M. D. & Dib-Hajj, S. D. ( 1995; ). Polydnavirus-facilitated endoparasite protection against host immune defense. Proc Natl Acad Sci U S A 92, 29–36.[CrossRef]
    [Google Scholar]
  29. Theilmann, D. A. & Summers, M. D. ( 1986; ). Molecular analysis of Campoletis sonorensis virus DNA in the lepidopteran host Heliothis virescens. J Gen Virol 67, 1961–1969.[CrossRef]
    [Google Scholar]
  30. Theilmann, D. A. & Summers, M. D. ( 1987; ). Physical analysis of the Campoletis sonorensis virus multipartite genome and identification of a family of tandemly repeated elements. J Virol 61, 2589–2598.
    [Google Scholar]
  31. Theilmann, D. A. & Summers, M. D. ( 1988; ). Identification and comparison of Campoletis sonorensis virus transcripts expressed from four genomic segments in the insect hosts Campoletis sonorensis and Heliothis virescens. Virology 167, 329–341.
    [Google Scholar]
  32. Varricchio, P., Falabella, P., Sordetti, R., Craziani, F., Malva, C. & Pennacchio, F. ( 1999; ). Cardiochiles nigriceps polydnavirus: molecular characterization and gene expression in parasitized Heliothis virescens larvae. Insect Biochem Mol Biol 29, 1087–1096.[CrossRef]
    [Google Scholar]
  33. Volkoff, A., Cérutti, P., Rocher, J., Ohresser, M. C. P., Devauchelle, G. & Duonor-Cérutti, M. ( 1999; ). Related RNAs in lepidopteran cells after in vitro infection with Hyposoter didymator virus define a new polydnavirus gene family. Virology 263, 349–363.[CrossRef]
    [Google Scholar]
  34. Webb, B. A. & Cui, L. ( 1998; ). Relationships between polydnavirus genomes and viral gene expression. J Insect Physiol 44, 785–793.[CrossRef]
    [Google Scholar]
  35. Wyder, S., Tschannen, A., Hochuli, A., Gruber, A., Saladin, V., Zumbach, S. & Lanzrein, B. ( 2002; ). Characterization of Chelonus inanitus polydnavirus segments: sequences and analysis, excision site and demonstration of clustering. J Gen Virol 83, 247–256.
    [Google Scholar]
  36. Xu, D. & Stoltz, D. B. ( 1993; ). Polydnavirus genome segment families in the ichneumonid parasitoid Hyposoter fugitivus. J Virol 67, 1340–1349.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19234-0
Loading
/content/journal/jgv/10.1099/vir.0.19234-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error