1887

Abstract

Polydnaviruses are unique symbiotic viruses that are replicated in the calyx cells of the ovary of some parasitic wasps. They have a segmented genome of circular double-stranded DNA and are injected along with the wasp's egg into the host, where they are essential for successful parasitism. Polydnaviruses replicate from integrated proviral DNA, and after excision of viral segments, flanking DNA is rejoined. Little is known about ovarian morphogenesis, the mode of amplification of the viral DNA and the involvement of ecdysteroids. Here we have analysed these parameters in the course of pupal–adult development in the braconid wasp . Immediately after pupation, ovarian cells proliferated and calyx cells began to differentiate; at this stage ecdysteroids, in particular 20-hydroxyecdysone, were highest. Thereafter, calyx cells began to increase in size and DNA content and eventually became gigantic. Amplification of non-viral DNA (actin) and viral DNA in its integrated and excised form and of corresponding rejoined flanking regions was measured by quantitative real-time PCR. In the early phase of calyx cell differentiation, copy numbers of actin and integrated viral DNA increased to a similar extent. This, along with the increase in nuclear volume and DNA content in the absence of extensive cell proliferation, suggested polyploidization of the early stage calyx cells. In the following phase, integrated viral DNA was selectively and intensively amplified and eventually excised and circularized. As copy numbers of excised circular viral DNA and rejoined flanking DNA reached similarly high levels, excised viral DNA appeared not to replicate. After adult eclosion, amplification of viral DNA declined.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18832-0
2003-05-01
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/5/vir841141.html?itemId=/content/journal/jgv/10.1099/vir.0.18832-0&mimeType=html&fmt=ahah

References

  1. Ahrens C. H., Pearson M. N., Rohrmann G. 1995; Identification and characterization of a second putative origin of DNA replication in a baculovirus of Orgyia pseudotsugata . Virology 207:572–576
    [Google Scholar]
  2. 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
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
    [Google Scholar]
  4. Audit-Lamour C., Busson D. 1981; Oögenesis defects in the ecd -1 mutant of Drosophila melanogaster , deficient in ecdysteroid at high temperature. J Insect Physiol 27:829–837
    [Google Scholar]
  5. Belle E., Beckage N. E., Rousselet J., Poirié M., Lemeunier F., Drezen J. M. 2002; Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J Virol 76:5793–5796
    [Google Scholar]
  6. Brodsky W. Y., Uryvaeva I. V. 1977; Cell polyploidy: its relation to tissue growth and function. Int Rev Cytol 50:275–332
    [Google Scholar]
  7. Calvi B. R., Lilly M. A., Spradling A. C. 1998; Cell cycle control of chorion gene amplification. Genes Dev 12:734–744
    [Google Scholar]
  8. Edgar B. A., Orr-Weaver T. L. 2001; Endoreplication cell cycles: more for less. Cell 105:297–306
    [Google Scholar]
  9. Gelman D., Carpenter J. E., Greany P. 2000; Ecdysteroid levels/profiles of the parasitoid wasp, Diapetimorpha introita , reared on its host, Spodoptera frugiperda and on an artificial diet. J Insect Physiol 46:457–465
    [Google Scholar]
  10. Grossniklaus-Bürgin C., Lanzrein B. 1990a; Qualitative and quantitative analysis of juvenile hormone and ecdysteroids from the egg to the pupal molt in Trichoplusia ni . Arch Insect Biochem Physiol 14:13–30
    [Google Scholar]
  11. Grossniklaus-Bürgin C., Lanzrein B. 1990b; Endocrine interrelationship between the parasitoid Chelonus sp. and its host Trichoplusia ni . Arch Insect Biochem Physiol 14:201–216
    [Google Scholar]
  12. Grossniklaus-Bürgin C., Wyler T., Pfister-Wilhelm R., Lanzrein B. 1994; Biology and morphology of the parasitoid Chelonus inanitus (Braconidae, Hymenoptera) and effects on the development of its host Spodoptera littoralis (Noctuidae, Lepidoptera). Invertebr Reprod Dev 25:143–158
    [Google Scholar]
  13. Grossniklaus-Bürgin C., Pfister-Wilhelm R., Meyer V., Treiblmayr K., Lanzrein B. 1998; Physiological and endocrine changes associated with polydnavirus/venom in the parasitoid–host system Chelonus inanitus–Spodoptera littoralis . J Insect Physiol 44:305–321
    [Google Scholar]
  14. Gruber A., Stettler P., Heiniger P., Schümperli D., Lanzrein B. 1996; Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp's genome and excised only in later pupal and adult stages of the female. J Gen Virol 77:2873–2879
    [Google Scholar]
  15. Hodin J., Riddiford L. M. 1998; The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Development Genes Evol 208:304–317
    [Google Scholar]
  16. Hotta M., Okuda T., Tanaka T. 2001; Cotesia kariyai teratocytes: growth and development. J Insect Physiol 47:31–41
    [Google Scholar]
  17. Kool M., Ahrens C. H., Vlak J. M., Rohrmann G. 1995; Replication of baculovirus DNA. J Gen Virol 76:2103–2118
    [Google Scholar]
  18. Lafont R., Koolman J., Rees H. 1993; Standardized abbreviations for common ecdysteroids. Insect Biochem Mol Biol 23:207–209
    [Google Scholar]
  19. Lanzrein B., Pfister-Wilhelm R., von Niederhäusern F. 2001; Effects of an egg–larval parasitoid and its polydnavirus on development and the endocrine system of the host. In Endocrine Interactions of Insect Parasites and Pathogens pp  95–109 Edited by Edwards J. P., Weaver R. Oxford: BIOS Scientific Publishers;
    [Google Scholar]
  20. Lavine M. D., Beckage N. E. 1995; Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitol Today 11:368–378
    [Google Scholar]
  21. 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 Beckage N. E., Thompson S. N., Federici B. A. San Diego: Academic Press;
    [Google Scholar]
  22. 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]
  23. Osheim Y. N., Miller O. L., Beyer A. L. 1988; Visualization of Drosophila melanogaster chorion genes undergoing amplification. Mol Cell Biol 8:2811–2821
    [Google Scholar]
  24. Pasquier-Barre F., Dupuy C., Huguet E., Monteiro F., Moreau A., Poirié M., Drezen J.-M. 2002; Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. J Gen Virol 83:2035–2045
    [Google Scholar]
  25. Pearson M., Bjornson R., Pearson G., Rohrmann G. 1992; The Autographa californica baculovirus genome: evidence for multiple replication origins. Science 257:1382–1384
    [Google Scholar]
  26. Savary S., Beckage N., Tan F., Periquet G., Drezen J. M. 1997; Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastrinae) at potential recombinase binding sites. J Gen Virol 78:3125–3134
    [Google Scholar]
  27. Savary S., Drezen J. M., Tan F., Beckage N. E., Periquet G. 1999; The excision of polydnavirus sequences from the genome of the wasp Cotesia congregata (Braconidae, Microgastrinae) is developmentally regulated but not strictly restricted to the ovaries in the adult. Insect Mol Biol 8:319–327
    [Google Scholar]
  28. Schmidt O., Theopold M., Strand M. R. 2001; Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 23:344–351
    [Google Scholar]
  29. Soller M., Lanzrein B. 1996; Polydnavirus and venom of the egg–larval parasitoid Chelonus inanitus (Braconidae) induce developmental arrest in the prepupa of its host Spodoptera littoralis (Noctuidae). J Insect Physiol 42:471–481
    [Google Scholar]
  30. Stoltz D. B. 1993; The polydnavirus life cycle. In Parasites and Pathogens of Insects pp  167–187 Edited by Beckage N. E., Thompson S. N., Federici B. A. San Diego: Academic Press;
    [Google Scholar]
  31. Strand M. R., Wong E. A. 1991; The growth and role of Microplitis demolitor teratocytes in parasitism of Pseudoplusia includens . J Insect Physiol 37:503–516
    [Google Scholar]
  32. Warren J. T., Gilbert L. I. 1986; Ecdysone metabolism and distribution during the pupal–adult development of Manduca sexta . Insect Biochem 16:65–82
    [Google Scholar]
  33. Webb B. A. 1998; Polydnavirus biology, genome structure, and evolution. In The Insect Viruses pp  105–139 Edited by Miller L. K., Ball L. A. New York & London: Plenum;
    [Google Scholar]
  34. Webb B. A., Summers M. D. 1992; Stimulation of polydnavirus replication by 20-hydroxyecdysone. Experientia 48:1018–1022
    [Google Scholar]
  35. Webb B. A., Beckage N. E., Hayakawa Y., Krell P. J., Lanzrein B., Stoltz D. B., Strand M. R., Summers M. D. 2000; Polydnaviridae. In Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses pp  253–260 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. San Diego: Academic Press;
    [Google Scholar]
  36. 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]
  37. Wyler T., Lanzrein B. 2003; Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus . II. Ultrastructural analysis of calyx cell development, virion formation and release. J Gen Virol 84:1151–1163
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.18832-0
Loading
/content/journal/jgv/10.1099/vir.0.18832-0
Loading

Data & Media loading...

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