1887

Abstract

Successful parasitism of some endoparasitic wasps depends on an obligately symbiotic association with polydnaviruses. These unique viruses have a segmented genome consisting of circles of double-stranded (ds) DNA and do not replicate in the parasitized host. They are produced in the wasp's ovary and injected into the host along with the egg. is an egg–larval parasitoid; its polydnavirus (CiV) has been shown to protect the parasitoid larva from the host's immune system and to induce developmental arrest in the prepupal stage. The genome of CiV consists of at least 10–12 segments and five have been sequenced up to now. Here, the complete (CiV12g2) or partial (CiV12g1, CiV16.8g1) cloning of three new CiV genes is reported. All three occur only on one viral segment and have no similarity to other known polydnavirus genes, with the exception of a high similarity of CiV12g1 to CiV14g1 and CiV12g2 to CiV14g2. Furthermore, the first attempt of application of RNA interference to study the function of polydnavirus genes is shown. Injection of dsRNA of two late- and one early- and late-expressed CiV genes into CiV/venom-containing host eggs partially rescued last-instar larvae from developmental arrest. Injection of the same dsRNAs into parasitized eggs partially reduced parasitoid survival, mainly by preventing the successful emergence of the parasitoid from the host. These viral genes thus seem to be involved in inducing developmental arrest and in keeping the cuticle soft, which appears to be necessary for parasitoid emergence and host feeding.

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2005-04-01
2024-04-20
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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. Beck M., Strand M. R. 2003; RNA interference silences Microplitis demolitor bracovirus genes and implicates glc1.8 in disruption of adhesion in infected host cells. Virology 314:521–535 [CrossRef]
    [Google Scholar]
  3. Bettencourt R., Terenius O., Faye I. 2002; Hemolin gene silencing by ds-RNA injected into Cecropia pupae is lethal to next generation embryos. Insect Mol Biol 11:267–271 [CrossRef]
    [Google Scholar]
  4. Blandin S., Shiao S.-H., Moita L. F., Janse C. J., Waters A. P., Kafatos F. C., Levashina E. A. 2004; Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae . Cell 116:661–670 [CrossRef]
    [Google Scholar]
  5. Bonvin M., Kojic D., Blank F., Annaheim M., Wehrle I., Wyder S., Kaeslin M., Lanzrein B. 2004; Stage-dependent expression of Chelonus inanitus polydnavirus genes in the host and the parasitoid. J Insect Physiol 50:1015–1026 [CrossRef]
    [Google Scholar]
  6. Boulétreau M. 1986; The genetic and coevolutionary interactions between parasitoids and their hosts. In Insect Parasitoids pp  169–200 Edited by Waage J., Greathead D. London: Academic Press;
    [Google Scholar]
  7. Brown S. J., Mahaffey J. P., Lorenzen M. D., Denell R. E., Mahaffey J. W. 1999; Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol Dev 1:11–15 [CrossRef]
    [Google Scholar]
  8. Chen Y. P., Gundersen-Rindal D. E. 2003; Morphological and genomic characterization of the polydnavirus associated with the parasitoid wasp Glyptapanteles indiensis (Hymenoptera: Braconidae. J Gen Virol 84:2051–2060 [CrossRef]
    [Google Scholar]
  9. Chen Y. P., Taylor P. B., Shapiro M., Gundersen-Rindal D. E. 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]
  10. Dover B. A., Vinson S. B. 1990; Stage-specific effects of Campoletis sonorensis parasitism on Heliothis virescens development and prothoracic glands. Physiol Entomol 15:405–414
    [Google Scholar]
  11. Dover B. A., Davies D. H., Vinson S. B. 1988; Degeneration of last instar Heliothis virescens prothoracic glands by Campoletis sonorensis polydnavirus. J Invertebr Pathol 51:80–91 [CrossRef]
    [Google Scholar]
  12. Falabella P., Varricchio P., Gigliotti S., Tranfaglia A., Pennacchio F., Malva C. 2003; Toxoneuron nigriceps polydnavirus encodes a putative aspartyl protease highly expressed in parasitized host larvae. Insect Mol Biol 12:9–17 [CrossRef]
    [Google Scholar]
  13. Flores-Jasso C. F., Valdes V. J., Sampieri A., Valadez-Graham V., Recillas-Targa F., Vaca L. 2004; Silencing structural and nonstructural genes in baculovirus by RNA interference. Virus Res 102:75–84 [CrossRef]
    [Google Scholar]
  14. Goto A., Blandin S., Royet J., Reichhart J.-M., Levashina E. A. 2003; Silencing of Toll pathway components by direct injection of double-stranded RNA into Drosophila adult flies. Nucleic Acids Res 31:6619–6623 [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. Invertebr Reprod Dev 25:143–158 [CrossRef]
    [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Lanzrein B., Pfister-Wihelm 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. J. Oxford: BIOS Scientific Publishers;
    [Google Scholar]
  20. Lawrence P. O., Lanzrein B. 1993; Hormonal interactions between insect endoparasites and their host insects. In Parasites and Pathogens of Insects vol. 1 pp  59–86 Edited by Beckage N. E., Thompson S. N., Federici B. A. San Diego: Academic Press;
    [Google Scholar]
  21. Lewis B. P., Green R. E., Brenner S. E. 2003; Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci U S A 100:189–192 [CrossRef]
    [Google Scholar]
  22. Malva C., Varricchio P., Falabella P., La Scaleia R., Graziani F., Pennacchio F. 2004; Physiological and molecular interaction in the host–parasitoid system Heliothis virescens Toxoneuron nigriceps : current status and future perspectives. Insect Biochem Mol Biol 34:177–183 [CrossRef]
    [Google Scholar]
  23. Miyawaki K., Mito T., Sarashina I., Zhang H., Shinmyo Y., Ohuchi H., Noji S. 2004; Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech Dev 121:119–130 [CrossRef]
    [Google Scholar]
  24. Pfister-Wilhelm R., Lanzrein B. 1996; Precocious induction of metamorphosis in Spodoptera littoralis (Noctuidae) by the parasitic wasp Chelonus inanitus (Braconidae): identification of the parasitoid larva as the key element and the host corpora allata as a main target. Arch Insect Biochem Physiol 32:511–525 [CrossRef]
    [Google Scholar]
  25. Quan G. X., Kanda T., Tamura T. 2002; Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Mol Biol 11:217–222 [CrossRef]
    [Google Scholar]
  26. Rosén M., Castillejo-López C., Edström J.-E. 2002; Telomere terminating with centromere-specific repeats is closely associated with a transposon derived gene in Chironomus pallidivitatus . Chromosoma 110:532–541 [CrossRef]
    [Google Scholar]
  27. Sánchez Alvarado A., Newmark P. A. 1999; Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci U S A 96:5049–5054 [CrossRef]
    [Google Scholar]
  28. Schmidt O., Theopold U., Strand M. 2001; Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. Bioessays 23:344–351 [CrossRef]
    [Google Scholar]
  29. Schoppmeier M., Damen W. G. M. 2001; Double-stranded RNA interference in the spider Cupiennus salei : the role of Distal-less is evolutionarily conserved in arthropod appendage formation. Dev Genes Evol 211:76–82 [CrossRef]
    [Google Scholar]
  30. 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]
  31. 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]
  32. Tillinger N. A., Hoch G., Schopf A. 2004; Effects of parasitoid associated factors of the endoparasitoid Glyptapanteles liparidis (Hymenoptera: Braconidae). Eur J Entomol 101:243–249 [CrossRef]
    [Google Scholar]
  33. Turnbull M., Webb B. A. 2002; Perspectives on polydnavirus origins and evolution. Adv Virus Res 58:203–254
    [Google Scholar]
  34. Valdes V. J., Sampieri A., Sepulveda J., Vaca L. 2003; Using double-stranded RNA to prevent in vitro and in vivo viral infections by recombinant baculovirus. J Biol Chem 278:19317–19324 [CrossRef]
    [Google Scholar]
  35. 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]
  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. Wyder S., Blank F., Lanzrein B. 2003; Fate of polydnavirus DNA of the egg–larval parasitoid Chelonus inanitus in the host Spodoptera littoralis . J Insect Physiol 49:491–500 [CrossRef]
    [Google Scholar]
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