1887

Abstract

ichnovirus (TrIV) is a polydnavirus (PDV) transmitted by the endoparasitic wasp to its host during oviposition. PDV genes are expressed in infected caterpillars, causing physiological disturbances that promote the survival of the developing endoparasite. The previously sequenced genome of TrIV contains ~86 genes organized in multigene families and distributed on multiple segments of circular dsDNA. Among these, the ‘ virus’ () family comprises seven genes that are absent in other PDV genomes examined to date and whose function(s) remain(s) unknown. Here, we initiated a functional analysis of the family using qPCR, transfection and RNAi approaches. family genes were weakly expressed in wasp ovaries, but some displayed high transcript abundance in parasitized caterpillars. Whilst was the most highly transcribed gene in infected caterpillars, transcript levels for and were nearly undetectable, indicating that they may be pseudogenes. Temporal and tissue-specific patterns of transcript abundance were similar for all expressed family genes, indicative of an apparent lack of difference in function or tissue specificity. Infection of Cf-203 and Sf-21 insect cells with TrIV led to a dose-dependent inhibition of cell proliferation with no sign of apoptosis. Whilst similar inhibition was observed following transfection of cells with a cloned genome segment carrying the gene, RNA interference targeting largely restored cell growth in TrIV-infected cells, indicating that expression was responsible for the observed inhibition. We suggest that genes may contribute to host developmental disruption by interfering with host-cell proliferation during parasitism.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.049817-0
2013-05-01
2020-01-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/5/1134.html?itemId=/content/journal/jgv/10.1099/vir.0.049817-0&mimeType=html&fmt=ahah

References

  1. 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] [PubMed]
    [Google Scholar]
  2. 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] [PubMed]
    [Google Scholar]
  3. 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.[PubMed]
    [Google Scholar]
  4. 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] [PubMed]
    [Google Scholar]
  5. Bézier A. , Herbinière J. , Lanzrein B. , Drezen J.-M. . ( 2009; ). Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. . J Invertebr Pathol 101:, 194–203. [CrossRef] [PubMed]
    [Google Scholar]
  6. Clavijo G. , Dorémus T. , Ravallec M. , Mannucci M. A. , Jouan V. , Volkoff A. N. , Darboux I. . ( 2011; ). Multigenic families in ichnovirus: a tissue and host specificity study through expression analysis of vankyrins from Hyposoter didymator ichnovirus. . PLoS ONE 6:, e27522. [CrossRef] [PubMed]
    [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. . J Gen Virol 77:, 797–809. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cusson M. , Lucarotti C. , Stoltz D. , Krell P. , Doucet D. . ( 1998a; ). A polydnavirus from the spruce budworm parasitoid, Tranosema rostrale (Ichneumonidae). . J Invertebr Pathol 72:, 50–56. [CrossRef] [PubMed]
    [Google Scholar]
  9. Cusson M. , Barron J. R. , Goulet H. , Régnière J. , Doucet D. . ( 1998b; ). Biology and status of Tranosema rostrale (Hymenoptera: Ichneumonidae), a parasitoid of the eastern spruce budworm (Lepidoptera: Tortricidae). . Ann Entomol Soc Am 91:, 87–93.[CrossRef]
    [Google Scholar]
  10. Cusson M. , Laforge M. , Miller D. , Cloutier C. , Stoltz D. . ( 2000; ). Functional significance of parasitism-induced suppression of juvenile hormone esterase activity in developmentally delayed Choristoneura fumiferana larvae. . Gen Comp Endocrinol 117:, 343–354. [CrossRef] [PubMed]
    [Google Scholar]
  11. 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]
  12. 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]
  13. Dupuy C. , Huguet E. , Drezen J.-M. . ( 2006; ). Unfolding the evolutionary story of polydnaviruses. . Virus Res 117:, 81–89. [CrossRef] [PubMed]
    [Google Scholar]
  14. Dupuy C. , Gundersen-Rindal D. , Cusson M. . ( 2012; ). Genomics and replication of polydnaviruses. . In Parasitoid Viruses: Symbionts and Pathogens, pp. 47–61. Edited by Beckage N. E. , Drezen J.-M. . . London:: Elsevier;. [CrossRef]
    [Google Scholar]
  15. Etebari K. , Palfreyman R. W. , Schlipalius D. , Nielsen L. K. , Glatz R. V. , Asgari S. . ( 2011; ). Deep sequencing-based transcriptome analysis of Plutella xylostella larvae parasitized by Diadegma semiclausum . . BMC Genomics 12:, 446. [CrossRef] [PubMed]
    [Google Scholar]
  16. Farrell P. J. , Lu M. , Prevost J. , Brown C. , Behie L. , Iatrou K. . ( 1998; ). High-level expression of secreted glycoproteins in transformed lepidopteran insect cells using a novel expression vector. . Biotechnol Bioeng 60:, 656–663. [CrossRef] [PubMed]
    [Google Scholar]
  17. Fath-Goodin A. , Kroemer J. A. , Webb B. A. . ( 2009; ). The Campoletis sonorensis ichnovirus vankyrin protein P-vank-1 inhibits apoptosis in insect Sf9 cells. . Insect Mol Biol 18:, 497–506. [CrossRef] [PubMed]
    [Google Scholar]
  18. Federici B. A. , Bigot Y. . ( 2003; ). Origin and evolution of polydnaviruses by symbiogenesis of insect DNA viruses in endoparasitic wasps. . J Insect Physiol 49:, 419–432. [CrossRef] [PubMed]
    [Google Scholar]
  19. Fleming J. G. , Summers M. D. . ( 1991; ). Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. . Proc Natl Acad Sci U S A 88:, 9770–9774. [CrossRef] [PubMed]
    [Google Scholar]
  20. 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] [PubMed]
    [Google Scholar]
  21. 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] [PubMed]
    [Google Scholar]
  22. Kroemer J. A. , Webb B. A. . ( 2005; ). Ikβ-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] [PubMed]
    [Google Scholar]
  23. Kroemer J. A. , Webb B. A. . ( 2006; ). Divergences in protein activity and cellular localization within the Campoletis sonorensis ichnovirus vankyrin family. . J Virol 80:, 12219–12228. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lapointe R. , Wilson R. , Vilaplana L. , O’Reilly D. R. , Falabella P. , Douris V. , Bernier-Cardou M. , Pennacchio F. , Iatrou K. . & other authors ( 2005; ). Expression of a Toxoneuron nigriceps polydnavirus-encoded protein causes apoptosis-like programmed cell death in lepidopteran insect cells. . J Gen Virol 86:, 963–971. [CrossRef] [PubMed]
    [Google Scholar]
  25. Littell R. C. , Milliken G. A. , Stroup W. W. , Wolfinger R. D. , Schabenberger O. . ( 2006; ). SAS for Mixed Models, , 2nd edn.. Cary, NC:: SAS Institute;.
    [Google Scholar]
  26. McMorran A. R. . ( 1965; ). A synthetic diet for the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). . Can Entomol 97:, 58–62. [CrossRef]
    [Google Scholar]
  27. Pruijssers A. J. , Falabella P. , Eum J. H. , Pennacchio F. , Brown M. R. , Strand M. R. . ( 2009; ). Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the moth Pseudoplusia includens . . J Exp Biol 212:, 2998–3006. [CrossRef] [PubMed]
    [Google Scholar]
  28. Rasoolizadeh A. , Béliveau C. , Stewart D. , Cloutier C. , Cusson M. . ( 2009a; ). Tranosema rostrale ichnovirus repeat element genes display distinct transcriptional patterns in caterpillar and wasp hosts. . J Gen Virol 90:, 1505–1514. [CrossRef] [PubMed]
    [Google Scholar]
  29. Rasoolizadeh A. , Dallaire F. , Stewart D. , Béliveau C. , Lapointe R. , Cusson M. . ( 2009b; ). Global transcriptional profile of Tranosema rostrale ichnovirus genes in infected lepidopteran hosts and wasp ovaries. . Virol Sin 24:, 478–492. [CrossRef]
    [Google Scholar]
  30. 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] [PubMed]
    [Google Scholar]
  31. 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] [PubMed]
    [Google Scholar]
  32. Rutledge R. G. , Stewart D. . ( 2010; ). Assessing the performance capabilities of LRE-based assays for absolute quantitative real-time PCR. . PLoS ONE 5:, e9731. [CrossRef] [PubMed]
    [Google Scholar]
  33. Shorey H. H. , Hale R. L. . ( 1965; ). Mass rearing of the larvae of nine Noctuid species on a simple artificial medium. . J Econ Entomol 58:, 522–524.[CrossRef]
    [Google Scholar]
  34. Sohi S. S. , Lalouette W. , MacDonald J. A. , Gringorten J. L. , Budeau C. B. . ( 1993; ). Establishment of continuous midgut cell lines of spruce budworm (Lepidoptera: Tortricidae). . In Vitro Cell Dev Biol 29A:, 56A.
    [Google Scholar]
  35. Stoltz D. B. . ( 1990; ). Evidence for chromosomal transmission of polydnavirus DNA. . J Gen Virol 71:, 1051–1056. [CrossRef] [PubMed]
    [Google Scholar]
  36. Stoltz D. B. , Guzo D. , Cook D. . ( 1986; ). Studies on polydnavirus transmission. . Virology 155:, 120–131. [CrossRef] [PubMed]
    [Google Scholar]
  37. Suderman R. J. , Pruijssers A. J. , Strand M. R. . ( 2008; ). Protein tyrosine phosphatase-H2 from a polydnavirus induces apoptosis of insect cells. . J Gen Virol 89:, 1411–1420. [CrossRef] [PubMed]
    [Google Scholar]
  38. 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] [PubMed]
    [Google Scholar]
  39. Thézé J. , Bézier A. , Periquet G. , Drezen J.-M. , Herniou E. A. . ( 2011; ). Paleozoic origin of insect large dsDNA viruses. . Proc Natl Acad Sci U S A 108:, 15931–15935. [CrossRef] [PubMed]
    [Google Scholar]
  40. Turnbull M. W. , Webb B. A. . ( 2002; ). Perspectives on polydnavirus origins and evolution. . Adv Virus Res 58:, 203–254. [CrossRef] [PubMed]
    [Google Scholar]
  41. Vaughn J. L. , Goodwin R. H. , Tompkins G. J. , McCawley P. . ( 1977; ). The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). . In Vitro 13:, 213–217. [CrossRef] [PubMed]
    [Google Scholar]
  42. 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] [PubMed]
    [Google Scholar]
  43. Volkoff A. N. , Jouan V. , Urbach S. , Samain S. , Bergoin M. , Wincker P. , Demettre E. , Cousserans F. , Provost B. . & other authors ( 2010; ). Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. . PLoS Pathog 6:, e1000923. [CrossRef] [PubMed]
    [Google Scholar]
  44. 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:: Plenum Press;. [CrossRef]
    [Google Scholar]
  45. Webb B. A. , Strand M. R. . ( 2005; ). The biology and genomics of polydnaviruses. . In Comprehensive Molecular Insect Science, pp. 323–360. Edited by Gilbert L. I. , Iatrou K. , Gill S. S. . . San Diego, CA:: Elsevier;. [CrossRef]
    [Google Scholar]
  46. 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: Classification and Nomenclature of Viruses. 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. . . San Diego, CA:: Academic Press;.
    [Google Scholar]
  47. Whitfield J. B. . ( 2002; ). Estimating the age of the polydnavirus/braconid wasp symbiosis. . Proc Natl Acad Sci U S A 99:, 7508–7513. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.049817-0
Loading
/content/journal/jgv/10.1099/vir.0.049817-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most cited articles

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