ichnovirus repeat element genes display distinct transcriptional patterns in caterpillar and wasp hosts Free

Abstract

The endoparasitic wasp transmits an ichnovirus to its lepidopteran host, , during parasitization. As shown for other ichnoviruses, the segmented dsDNA genome of the ichnovirus (TrIV) features several multi-gene families, including the repeat element () family, whose products display no known similarity to non-ichnovirus proteins, except for a homologue encoded by the genome of the granulovirus; their functions remain unknown. This study applied linear regression of efficiency analysis to real-time PCR quantification of transcript abundance for all 17 TrIV open reading frames (ORFs) in parasitized and virus-injected larvae, as well as in ovaries and head–thorax complexes. Although transcripts were detected for most ORFs in infected caterpillars, two of them clearly outnumbered the others in whole larvae, with a tendency for levels to drop over time after infection. The genome segments bearing the three most highly expressed genes in parasitized caterpillars were present in higher proportions than other -bearing genome segments in TrIV DNA, suggesting a possible role for gene dosage in the regulation of transcription level. TrIV genes also showed important differences in the relative abundance of their transcripts in specific tissues (cuticular epithelium, the fat body, haemocytes and the midgut), implying tissue-specific roles for individual members of this gene family. Significantly, no transcripts were detected in head–thorax complexes, whereas some were abundant in ovaries. There, the transcription pattern was completely different from that observed in infected caterpillars, suggesting that some genes have wasp-specific functions.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.008664-0
2009-06-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/6/1505.html?itemId=/content/journal/jgv/10.1099/vir.0.008664-0&mimeType=html&fmt=ahah

References

  1. Beck M. H., Inman R. B., Strand M. R. 2007; Microplitis demolitor bracovirus genome segments vary in abundance and are individually packaged in virions. Virology 359:179–189 [CrossRef]
    [Google Scholar]
  2. Béliveau C., Laforge M., Cusson M., Bellemare G. 2000; Expression of a Tranosema rostrale polydnavirus gene in the spruce budworm, Choristoneura fumiferana . J Gen Virol 81:1871–1880
    [Google Scholar]
  3. Béliveau C., Levasseur A., Stoltz D., Cusson M. 2003; Three related TrIV genes: comparative sequence analysis and expression in host larvae and Cf-124T cells. J Insect Physiol 49:501–511 [CrossRef]
    [Google Scholar]
  4. Cusson M., Barron J. R., Goulet H., Régnière J., Doucet D. 1998; Biology and status of Tranosema rostrale rostrale ( Hymenoptera : Ichneumonidae ),a parasitoid of the eastern spruce budworm ( Lepidoptera : Tortricidae ). Ann Entomol Soc Am 91:87–93 [CrossRef]
    [Google Scholar]
  5. Doucet D., Cusson M. 1996a; Alteration of developmental rate and growth of Choristoneura fumiferana parasitized by Tranosema rostrale : role of the calyx fluid. Entomol Exp Appl 81:21–30 [CrossRef]
    [Google Scholar]
  6. Doucet D., Cusson M. 1996b; Role of calyx fluid in alterations of immunity in Choristoneura fumiferana larvae parasitized by Tranosema rostrale . Comp Biochem Physiol 114:311–317 [CrossRef]
    [Google Scholar]
  7. Doucet D., Levasseur A., Béliveau C., Lapointe R., Stoltz D., Cusson M. 2007; In vitro integration of an ichnovirus genome segment into the genomic DNA of lepidopteran cells. J Gen Virol 88:105–113 [CrossRef]
    [Google Scholar]
  8. Eggleton P., Belshaw B. 1993; Comparisons of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biol J Linn Soc Lond 48:213–226 [CrossRef]
    [Google Scholar]
  9. Falabella P., Varricchio P., Provost B., Espagne E., Ferrarese R., Grimaldi A., Eguileor M., Fimiani G., Ursini M. V. other authors 2007; Characterization of the I κ B-like gene family in polydnaviruses associated with wasps belonging to different braconid subfamilies. J Gen Virol 88:92–104 [CrossRef]
    [Google Scholar]
  10. Fath-Goodin A., Kroemer J., Martin S., Reeves K., Webb B. A. 2006; Polydnavirus genes that enhance the baculovirus expression vector system. Adv Virus Res 68:75–90
    [Google Scholar]
  11. Galibert L., Devauchelle G., Cousserans F., Rocher J., Cérutti P., Barat-Houari M., Fournier P., Volkoff A. N. 2006; Members of the Hyposoter didymator ichnovirus repeat element gene family are differentially expressed in Spodoptera frugiperda . Virol J 3:48 [CrossRef]
    [Google Scholar]
  12. Gundersen-Rindal D. E., Pedroni M. J. 2006; Characterization and transcriptional analysis of protein tyrosine phosphatase genes and an ankyrin repeat gene of the parasitoid Glyptapanteles indiensis polydnavirus in the parasitized host. J Gen Virol 87:311–322 [CrossRef]
    [Google Scholar]
  13. Harrison R. L., Popham H. J. R. 2008; Genomic sequence analysis of a granulovirus isolated from the Old World bollworm, Helicoverpa armigera . Virus Genes 36:565–581 [CrossRef]
    [Google Scholar]
  14. Ibrahim A. M., Choi J. Y., Je Y. H., Kim Y. 2007; Protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus: sequence analysis, expression profile, and a possible biological role in host immunosuppression. Dev Comp Immunol 31:978–990 [CrossRef]
    [Google Scholar]
  15. Kroemer J. A., Webb B. A. 2004; Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu Rev Entomol 49:431–456 [CrossRef]
    [Google Scholar]
  16. Kroemer J. A., Webb B. A. 2005; I κ B-related vankyrin genes in the Campoletis sonorensis ichnovirus: temporal and tissue-specific patterns of expression in parasitized Heliothis virescens lepidopteran hosts. J Virol 79:7617–7628 [CrossRef]
    [Google Scholar]
  17. 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]
  18. Provost B., Varricchio P., Arana E., Espagne E., Falabella P., Huguet E., La Scaleia R., Cattolico L., Poirié M. other authors 2004; Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J Virol 78:13090–13103 [CrossRef]
    [Google Scholar]
  19. Rutledge R. G., Stewart D. 2008a; A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biotechnol 8:47 [CrossRef]
    [Google Scholar]
  20. Rutledge R. G., Stewart D. 2008b; Critical evaluation of methods used to determine amplification efficiency refutes the exponential character of real-time PCR. BMC Mol Biol 9:96 [CrossRef]
    [Google Scholar]
  21. Stoltz D. B. 1993; The polydnavirus life cycle. In Parasites and pathogens of insects . vol 1 pp 80–101Edited by Beckage N. E., Thompson S. N., Federici B. A. San Diego, CA: Academic Press;
  22. Stoltz D. B., Guzo D., Cook D. 1986; Studies on polydnavirus transmission. Virology 155:120–131 [CrossRef]
    [Google Scholar]
  23. Tanaka K., Lapointe R., Barney W. E., Makkay A. M., Stoltz D., Cusson M., Webb B. A. 2007; Shared and species-specific features among ichnovirus genomes. Virology 363:26–35 [CrossRef]
    [Google Scholar]
  24. 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]
  25. 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]
  26. Thoetkiattikul H., Beck M. H., Strand M. R. 2005; Inhibitor κ B-like proteins from a polydnavirus inhibit NF- κ B activation and suppress the insect immune response. Proc Natl Acad Sci U S A 102:11426–11431 [CrossRef]
    [Google Scholar]
  27. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  28. Volkoff A. N., Béliveau C., Rocher J., Hilgarth R., Levasseur A., Duonor-Cérutti M., Cusson M., Webb B. A. 2002; Evidence for a conserved polydnavirus gene family: ichnovirus homologs of the CsIV repeat element genes. Virology 300:316–331 [CrossRef]
    [Google Scholar]
  29. Wang Z., Spadoro J. 1998; Determination of target copy number of quantitative standards used in PCR-based diagnostic assays. In Gene quantification pp 31–43Edited by Ferré. Boston: Birkhäuser;
    [Google Scholar]
  30. Webb B. A., Summers M. D. 1992; Stimulation of polydnavirus replication by 20-hydroxyecdysone. Experientia 48:1018–1022 [CrossRef]
    [Google Scholar]
  31. 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., & other authors F. 2006; Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347:160–174 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.008664-0
Loading
/content/journal/jgv/10.1099/vir.0.008664-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed