1887

Abstract

Polydnaviruses (genera and ) have a segmented genome of circular double-stranded DNA molecules, replicate in the ovary of parasitic wasps and are essential for successful parasitism of the host. Here we show the first detailed analysis of various segments of a bracovirus, the virus (CiV). Four segments were sequenced and two of them, CiV12 and CiV14, were found to be closely related while CiV14.5 and CiV16.8 were unrelated. CiV12, CiV14.5 and CiV16.8 are unique while CiV14 occurs also nested in another larger segment. All four segments are predicted to contain genes and predictions could be substantiated in most cases. Comparison with databases revealed no significant similarities at either the nucleotide or amino acid level. Inverted repeats with identities between 77% and 92% and lengths between 26 bp and 100 bp were found on all segments outside of predicted genes. Hybridization experiments indicate that CiV12 and CiV14 are both flanked by other virus segments, suggesting that proviral CiV segments are clustered in the genome of the wasp. The integration/excision site of CiV14 was analysed and compared to that of CiV12. On both termini of proviral CiV12 and CiV14 as well as in the excised circular molecule and the rejoined DNA a very similar repeat of 14 bp was found. A model to illustrate where the terminal repeats might recombine to yield the circular molecule is presented. Excision of CiV12 and CiV14 is restricted to the female and sets in at a very specific time-point in pupal–adult development.

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2002-01-01
2019-12-07
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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.[CrossRef]
    [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. Journal of General Virology 75, 3353-3363.[CrossRef]
    [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 Research 25, 3389-3402.[CrossRef]
    [Google Scholar]
  4. Asgari, S., Hellers, M. & Schmidt, O. ( 1996; ). Host haemocyte inactivation by an insect parasitoid: transient expression of a polydnavirus gene. Journal of General Virology 77, 2653-2662.[CrossRef]
    [Google Scholar]
  5. Béliveau, C., Laforge, M., Cusson, M. & Bellemare, G. ( 2000; ). Expression of a Tranosema rostrale polydnavirus gene in the spruce budworm, Choristoneura fumiferana. Journal of General Virology 81, 1871-1880.
    [Google Scholar]
  6. Burge, C. & Karlin, S. ( 1997; ). Prediction of complete gene structures in human genomic DNA. Journal of Molecular Biology 268, 78-94.[CrossRef]
    [Google Scholar]
  7. Cui, L. & Webb, B. A. ( 1996; ). Isolation and characterization of a member of the cysteine-rich gene family from Campoletis sonorensis polydnavirus. Journal of General Virology 77, 797-809.[CrossRef]
    [Google Scholar]
  8. 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. Journal of Virology 71, 8504-8513.
    [Google Scholar]
  9. Cui, L., Soldevila, A. & Webb, B. A. ( 1997; ). Expression and hemocyte targeting of a Campoletis sonorensis polydnavirus cysteine-rich gene in Heliothis virescens larvae. Archives of Insect Biochemistry and Physiology 36, 251-271.[CrossRef]
    [Google Scholar]
  10. Deng, L. Q. & Webb, B. A. ( 1999; ). Cloning and expression of a gene encoding a Campoletis sonorensis polydnavirus structural protein. Archives of Insect Biochemistry and Physiology 40, 30-40.[CrossRef]
    [Google Scholar]
  11. Dib-Hajj, S. D., Webb, B. A. & Summers, M. D. ( 1993; ). Structure and evolutionary implications of a ‘cysteine-rich’ Campoletis sonorensis polydnavirus gene family. Proceedings of the National Academy of Sciences, USA 90, 3765-3769.[CrossRef]
    [Google Scholar]
  12. Feng, J., Johnson, R. C. & Dickerson, R. E. ( 1994; ). Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science 263, 348-355.[CrossRef]
    [Google Scholar]
  13. Fleming, J. A. G. & Summers, M. D. ( 1986; ). Campoletis sonorensis endoparasitic wasps contain forms of Campoletis sonorensis virus DNA suggestive of integrated and extrachromosomal polydnavirus DNAs. Journal of Virology 57, 552-562.
    [Google Scholar]
  14. Fleming, J. A. G. & Summers, M. D. ( 1991; ). Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proceedings of the National Academy of Sciences, USA 88, 9770-9774.[CrossRef]
    [Google Scholar]
  15. 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). Invertebrate Reproduction and Development 25, 143-158.[CrossRef]
    [Google Scholar]
  16. 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. Journal of General Virology 77, 2873-2879.[CrossRef]
    [Google Scholar]
  17. Hansen, J. E., Lund, O., Tolstrup, N., Gooley, A. A., Williams, K. L. & Brunak, S. ( 1998; ). Prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconjugate Journal 15, 115-130.[CrossRef]
    [Google Scholar]
  18. Harwood, S. H., Grosovsky, A. J., Cowles, E. A., Davis, J. W. & Beckage, N. E. ( 1994; ). An abundantly expressed hemolymph glycoprotein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. Virology 205, 381-392.[CrossRef]
    [Google Scholar]
  19. Henikoff, S. & Henikoff, J. G. ( 1994; ). Protein family classification based on searching a database of blocks. Genomics 19, 97-107.[CrossRef]
    [Google Scholar]
  20. Hoersch, S., Leroy, C., Brown, N. P., Andrade, M. A. & Sander, C. ( 2000; ). The GeneQuiz web server: protein functional analysis through the web. Trends in Biochemical Sciences 25, 33-35.[CrossRef]
    [Google Scholar]
  21. Hofmann, K. & Stoffel, W. ( 1993; ). TMbase – a database of membrane spanning protein segments. Biological Chemistry Hoppe-Seyler 347, 166.
    [Google Scholar]
  22. Hofmann, K., Bucher, P., Falquet, L. & Bairoch, A. ( 1999; ). The PROSITE database, its status in 1999. Nucleic Acids Research 27, 215-219.[CrossRef]
    [Google Scholar]
  23. Johner, A., Stettler, P., Gruber, A. & Lanzrein, B. ( 1999; ). Presence of polydnavirus transcripts in an egg–larval parasitoid and its lepidopterous host. Journal of General Virology 80, 1847-1854.
    [Google Scholar]
  24. Kool, M., Ahrens, C. H., Vlak, J. M. & Rohrmann, G. F. ( 1995; ). Replication of baculovirus DNA. Journal of General Virology 76, 2103-2118.[CrossRef]
    [Google Scholar]
  25. Kulp, D., Haussler, D., Reese, M. G. & Eeckman, F. H. ( 1996; ). A generalized hidden Markov model for the recognition of human genes in DNA. In Proceedings of the Fourth International Conference on Intelligent Systems for Molecular Biology , pp. 134-142. Edited by D. J. States, P. Agarwal, T. Gaasterland, L. Huntern & R. F. Smith. St Louis, MO:AAAI Press.
  26. Lavine, M. D. & Beckage, N. E. ( 1995; ). Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitology Today 11, 368-378.[CrossRef]
    [Google Scholar]
  27. 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.
  28. Nakai, K. & Horton, P. ( 1999; ). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends in Biochemical Sciences 24, 34-36.[CrossRef]
    [Google Scholar]
  29. Nielsen, H., Engelbrecht, J., Brunak, S. & Heijne, G. ( 1997; ). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10, 1-6.[CrossRef]
    [Google Scholar]
  30. Norton, W. N. & Vinson, S. B. ( 1983; ). Correlating the initiation of virus replication with a specific pupal developmental phase of an ichneumonid parasitoid. Cell and Tissue Research 231, 387-398.
    [Google Scholar]
  31. Pearson, M., Bjornson, R., Pearson, G. & Rohrmann, G. ( 1992; ). The Autographa californica baculovirus genome: evidence for multiple replication origins. Science 257, 1382-1384.[CrossRef]
    [Google Scholar]
  32. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbour, NY: Cold Spring Harbour Laboratory.
  33. 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. Journal of General Virology 78, 3125-3134.
    [Google Scholar]
  34. 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 Molecular Biology 8, 319-327.[CrossRef]
    [Google Scholar]
  35. Solovyev, V. V. & Salamov, A. A. ( 1999; ). INFOGENE: a database of known gene structures and predicted genes and proteins in sequences of genome sequencing. Nucleic Acids Research 27, 248-250.[CrossRef]
    [Google Scholar]
  36. 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. Journal of Insect Physiology 44, 817-831.[CrossRef]
    [Google Scholar]
  37. Stoltz, D. B., Guzo, D. & Cook, D. ( 1986; ). Studies on polydnavirus transmission. Virology 155, 120-131.[CrossRef]
    [Google Scholar]
  38. Stoltz, D. B., Beckage, N. E., Blissard, G. W., Fleming, J. G. W., Krell, P. J., Theilmann, D. A., Summers, M. D. & Webb, B. A. ( 1995; ). Polydnaviridae. In Virus Taxonomy. Sixth Report of the International Committee of Viruses , pp. 143-147. Edited by F. A. Murphy, C. M. Fauquet, D. H. L. Bishop, S. A. Ghabrial, A. W. Jarvis, G. P. Martelli, M. A. Mayo & M. D. Summers. Vienna & New York:Springer-Verlag.
  39. Strand, M. R., Witherell, S. A. & Trudeau, D. ( 1997; ). Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. Journal of Virology 71, 2146-2156.
    [Google Scholar]
  40. Tatusova, T. A. & Madden, T. L. ( 1999; ). BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiology Letters 174, 247-250.[CrossRef]
    [Google Scholar]
  41. Taudien, S., Rump, A., Platzer, M., Drescher, B., Schattevoy, R., Gloeckner, G., Dette, M., Baumgart, C., Weber, J., Menzel, U. & Rosenthal, A. ( 2000; ). RUMMAGE – a high-throughput sequence annotation system. Trends in Genetics 16, 519-520.[CrossRef]
    [Google Scholar]
  42. 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. Journal of Virology 61, 2589-2598.
    [Google Scholar]
  43. Trudeau, D., Witherell, R. A. & Strand, M. R. ( 2000; ). Characterization of two novel Microplitis demolitor polydnavirus mRNAs expressed in Pseudoplusia includens haemocytes. Journal of General Virology 81, 3049-3058.
    [Google Scholar]
  44. Varricchio, P., Falabella, P., Sordetti, R., Graziani, F., Malva, C. & Pennacchio, F. ( 1999; ). Cardiochiles nigriceps polydnavirus: molecular characterization and gene expression in parasitized Heliothis virescens larvae. Insect Biochemistry and Molecular Biology 29, 1087-1096.[CrossRef]
    [Google Scholar]
  45. 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 & London:Plenum Press.
  46. Webb, B. A. & Cui, L. ( 1998; ). Relationships between polydnavirus genomes and viral gene expression. Journal of Insect Physiology 44, 785-793.[CrossRef]
    [Google Scholar]
  47. Webb, B. A. & Summers, M. D. ( 1992; ). Stimulation of polydnavirus replication by 20-hydroxyecdysone. Experientia 48, 1018-1022.[CrossRef]
    [Google Scholar]
  48. Whitfield, J. B. ( 1997; ). Molecular and morphological data suggest a single origin of the polydnaviruses among braconid wasps. Naturwissenschaften 84, 502-507.[CrossRef]
    [Google Scholar]
  49. Xu, D. M. & Stoltz, D. ( 1991; ). Evidence for a chromosomal location of polydnavirus DNA in the ichneumonid parasitoid Hyposoter fugitivus. Journal of Virology 65, 6693-6704.
    [Google Scholar]
  50. Xu, D. & Stoltz, D. ( 1993; ). Polydnavirus genome segment families in the ichneumonid parasitoid Hyposoter fugitivus. Journal of Virology 67, 1340-1349.
    [Google Scholar]
  51. Xu, Y. & Uberbacher, E. C. ( 1997; ). Automated gene identification in large-scale genomic sequences. Journal of Computational Biology 4, 325-338.[CrossRef]
    [Google Scholar]
  52. Yamanaka, A., Hayakawa, Y., Noda, H., Nakashina, N. & Watanabe, H. ( 1996; ). Characterization of polydnavirus-encoded mRNA in parasitized armyworm larvae. Insect Biochemistry and Molecular Biology 26, 529-536.[CrossRef]
    [Google Scholar]
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