1887

Abstract

Polydnaviruses are only found in symbiotic association with parasitic wasps within the families Ichneumonidae and Braconidae (ichnoviruses and bracoviruses). They have a segmented genome consisting of circular double-stranded DNA. In the proviral linear form they are integrated in the wasp's genome; in two bracoviruses, segments were found to be clustered. Proviral segments have direct terminal repeats. Segment excision has been proposed to occur through juxtaposition of these repeats by formation of a loop and recombination; one copy of the repeat then ends up in the circular segment and one in the rejoined DNA. Here we analysed the excision/circularization site of four segments of the bracovirus (CiV) and found that they are similar to the two already known sites; on the basis of the combined data an extended excision site motif was found. Analyses of segment flanking sequences led to the first identification of one complete and several partial spacers between proviral segments in a polydnavirus. The spacer between the proviral segments CiV14 and CiV22.5 has a length of 2065 bp; the terminal repeats of CiV14 and CiV22.5 were seen to have an opposite orientation and from this a model on the spacial organization of the loops of the proviral cluster is proposed. Through various approaches it was shown that spacers are not excised or injected into the host. Measurement of relative abundances of various segments in proviral and excised form indicates for the first time that abundant segments are present in multiple copies in the proviral form.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82396-0
2007-02-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/2/450.html?itemId=/content/journal/jgv/10.1099/vir.0.82396-0&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. Bailey, T. L. & Elkan, C. ( 1994; ). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2, 28–36.
    [Google Scholar]
  3. 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.[CrossRef]
    [Google Scholar]
  4. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. ( 2004; ). WebLogo: a sequence logo generator. Genome Res 14, 1188–1190.[CrossRef]
    [Google Scholar]
  5. D'Haeseleer, P. ( 2006; ). What are DNA sequence motifs? Nat Biotechnol 24, 423–425.[CrossRef]
    [Google Scholar]
  6. Espagne, E., Dupuy, C., Huguet, E., Cattolico, L., Provost, B., Martins, N., Poirie, M., Periquet, G. & Drezen, J. M. ( 2004; ). Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306, 286–289.[CrossRef]
    [Google Scholar]
  7. 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.[CrossRef]
    [Google Scholar]
  8. 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.[CrossRef]
    [Google Scholar]
  9. 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.[CrossRef]
    [Google Scholar]
  10. Kaeslin, M., Pfister-Wilhelm, R. & Lanzrein, B. ( 2005; ). Influence of the parasitoid Chelonus inanitus and its polydnavirus on host nutritional physiology and implications for parasitoid development. J Insect Physiol 51, 1330–1339.[CrossRef]
    [Google Scholar]
  11. 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.
  12. Marti, D., Grossniklaus-Bürgin, C., Wyder, S., Wyler, T. & Lanzrein, B. ( 2003; ). Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres. J Gen Virol 84, 1141–1150.[CrossRef]
    [Google Scholar]
  13. Ochman, H., Gerber, A. S. & Hartl, D. L. ( 1988; ). Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621–623.
    [Google Scholar]
  14. Pasquier-Barre, F., Dupuy, C. H., 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]
  15. Rattanadechakul, W. & Webb, B. A. ( 2003; ). Characterization of Campoletis sonorensis ichnovirus unique segment B and excision locus structure. J Insect Physiol 49, 523–532.[CrossRef]
    [Google Scholar]
  16. 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]
  17. Schmidt, O., Theopold, M. & Strand, M. R. ( 2001; ). Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. Bioessays 23, 344–351.[CrossRef]
    [Google Scholar]
  18. 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.[CrossRef]
    [Google Scholar]
  19. Stettler, P., Trenczek, T., Wyler, T., Pfister-Wilhelm, R. & Lanzrein, B. ( 1998; ). Overview of parasitism associated effects on host haemocytes in larval parasitoids and comparison with effects of the egg-larval parasitoid Chelonus inanitus on its host Spodoptera littoralis. J Insect Physiol 44, 817–831.[CrossRef]
    [Google Scholar]
  20. Volkoff, A. N., Ravallec, M., Bossy, J. P., Cerutti, P., Rocher, J., Cerutti, M. & Devauchelle, G. ( 1995; ). The replication of Hyposoter didymator polydnavirus: cytopathology of the calyx cells in the parasitoid. Biol Cell 83, 1–13.[CrossRef]
    [Google Scholar]
  21. Webb, B. A. ( 1998; ). Polydnavirus biology, genome structure, and evolution. In The Insect Viruses, pp. 105–139. Edited by L. K. Miller & L. A. Ball. New York and London: Plenum Press.
  22. 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: The Classification and Nomenclature of Viruses. The Seventh Report of the International Committee on Taxonomy, pp. 253–260. Edited by M. H. V. van Regenmortel, C. M. Fauquet, D. H. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle & R. B. Wickner. San Diego: Academic Press.
  23. Webb, B. A., Strand, M. R., Dickey, S. E., Beck, M. H., Hilgarth, R. S., Barney, W. E., Kadash, K., Kroemer, J. A., Lindstrom, K. G. & Rattanadechakul, W. ( 2006; ). Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347, 160–174.[CrossRef]
    [Google Scholar]
  24. Whitfield, J. B. ( 2002; ). Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 99, 7508–7513.[CrossRef]
    [Google Scholar]
  25. Whitfield, J. B. & Asgari, S. ( 2003; ). Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J Insect Physiol 49, 397–405.[CrossRef]
    [Google Scholar]
  26. 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]
  27. 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.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82396-0
Loading
/content/journal/jgv/10.1099/vir.0.82396-0
Loading

Data & Media loading...

Supplements

vol. , part 2, pp. 450–457

Primers used in this study [ PDF] (66 KB)



PDF

Most Cited This Month

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