Polydnaviruses (PDVs) are unique symbiotic viruses associated with parasitic wasps; they replicate only in the calyx cells of a wasp's ovaries and are transferred at oviposition along with the parasitoid egg into the lepidopteran host. The DNA packaged in the viral particles encodes factors that manipulate the host's immune defences and development to benefit the parasitoid. PDVs are found in two subfamilies of ichneumonids (ichnoviruses) and in braconids of the microgastroid complex (bracoviruses). We recently showed that the latter derive from an ancestral nudivirus, as 24 nudivirus-related genes were identified in ovaries of two distantly related braconids at the stage of virion formation. Here, we present a comprehensive analysis of the viral particle proteins of the bracovirus (CiBV). Proteins of purified CiBV particles were analysed by mass spectrometry and amino acid sequences matched to the existing ovarian-cDNA database. In addition, transcript quantities of identified genes were measured by quantitative real-time PCR in female pupae at the onset and peak of virion formation and at corresponding stages in male pupae. This combined approach allowed the identification of 44 CiBV particle proteins: 16 were nudivirus-related, three had similarity to ovarian proteins of another braconid, 11 had similarity to cellular proteins and 14 had no similarity to known proteins. The transcripts of all of them increased in female, but not male, pupae. These data confirm the important contribution of nudivirus genes but also indicate the presence of many lineage- or species-specific proteins possibly involved in the parasitoid–host interaction.


Article metrics loading...

Loading full text...

Full text loading...



  1. Abd-Alla, A. M. M., Cousserans, F., Parker, A. G., Jehle, J. A., Parker, N. J., Vlak, J. M., Robinson, A. S. & Bergoin, M.(2008). Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus reveals a novel, large, double-stranded circular DNA virus. J Virol 82, 4595–4611.[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. J Gen Virol 75, 3353–3363.[CrossRef] [Google Scholar]
  3. Annaheim, M. & Lanzrein, B.(2007). Genome organization of the Chelonus inanitus polydnavirus: excision sites, spacers and abundance of proviral and excised segments. J Gen Virol 88, 450–457.[CrossRef] [Google Scholar]
  4. 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]
  5. Bézier, A., Herbinière, J., Serbielle, C., Lesobre, J., Wincker, P., Huguet, E. & Drezen, J.-M.(2008). Bracovirus gene products are highly divergent from insect proteins. Arch Insect Biochem Physiol 67, 172–187.[CrossRef] [Google Scholar]
  6. Bézier, A., Annaheim, M., Herbinière, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., Wincker, P., Roditi, I., Heller, M. & other authors(2009a). Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926–930.[CrossRef] [Google Scholar]
  7. Bézier, A., Herbinière, J., Lanzrein, B. & Drezen, J.-M.(2009b). Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. J Invertebr Pathol 101, 194–203.[CrossRef] [Google Scholar]
  8. Braunagel, S. C. & Summers, M. D.(2007). Molecular biology of the baculovirus occlusion-derived envelope. Curr Drug Targets 8, 1084–1095.[CrossRef] [Google Scholar]
  9. Braunagel, S. C., Williamson, S. T., Saksena, S., Zhong, Z., Russell, W. K., Russell, D. H. & Summers, M. D.(2004). Trafficking of ODV-E66 is mediated via a sorting motif and other viral proteins: facilitated trafficking to the inner nuclear membrane. Proc Natl Acad Sci U S A 101, 8372–8377.[CrossRef] [Google Scholar]
  10. Braunagel, S. C., Cox, V. & Summers, M. D.(2009). Baculovirus data suggest a common multifaceted pathway for sorting proteins to the inner nuclear membrane. J Virol 83, 1280–1288.[CrossRef] [Google Scholar]
  11. Burand, J. P.(2008). Insect viruses: nonoccluded. In Encyclopedia of Virology, pp. 144–148. Edited by Mahy, B. W. J. & van Regenmortel, M. H. V.. Oxford. : Elsevier. [Google Scholar]
  12. Burand, J. P., Stiles, B. & Wood, H. A.(1983). Structural and intracellular proteins of the nonoccluded baculovirus HZ-1. J Virol 46, 137–142. [Google Scholar]
  13. Chaivisuthangkura, P., Tawilert, C., Tejangkura, T., Rukpratanporn, S., Longyant, S., Sithigorngul, W. & Sithigorngul, P.(2008). Molecular isolation and characterization of a novel occlusion body protein gene from Penaeus monodon nucleopolyhedrovirus. Virology 381, 261–267.[CrossRef] [Google Scholar]
  14. Cheng, C. H., Liu, S. M., Chow, T. Y., Hsiao, Y. Y., Wang, D. P., Huang, J. J. & Chen, H. H.(2002). Analysis of the complete genome sequence of the Hz-1 virus suggests that it is related to members of the Baculoviridae. J Virol 76, 9024–9034.[CrossRef] [Google Scholar]
  15. Cipollone, R., Ascenzi, P. & Visca, P.(2007). Common themes and variations in the rhodanese superfamily. IUBMB Life 59, 51–59.[CrossRef] [Google Scholar]
  16. de Graaf, D. C., Aerts, M., Brunain, M., Desjardins, C. A., Jacobs, F. J., Werren, J. H. & Devreese, B.(2010). Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic study. Insect Mol Biol 19 (Suppl.), 11–26.[CrossRef] [Google Scholar]
  17. Desjardins, C. A., Gundersen-Rindal, D. E., Hostetler, J. B., Tallon, L. J., Fadrosh, D. W., Fuester, R. W., Pedroni, M. J., Haas, B. J., Schatz, M. C. & other authors(2008). Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol 9, R183.[CrossRef] [Google Scholar]
  18. 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]
  19. 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] [Google Scholar]
  20. Garcia-Maruniak, A., Maruniak, J. E., Farmerie, W. & Boucias, D. G.(2008). Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV. Virology 377, 184–196.[CrossRef] [Google Scholar]
  21. 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]
  22. 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]
  23. Huger, A. M. & Krieg, A.(1991).Baculoviridae. Nonoccluded baculoviruses. In Atlas of Invertebrate Viruses, pp. 287–319. Edited by Adams, J. R. & Bonami, J. R.. Boca Raton, FL. : CRC Press. [Google Scholar]
  24. Kaeslin, M., Reinhard, M., Bühler, D., Roth, T., Pfister-Wilhelm, R. & Lanzrein, B.(2010). Venom of the egg-larval parasitoid Chelonus inanitus is a complex mixture and has multiple biological effects. J Insect Physiol 56, 686–694.[CrossRef] [Google Scholar]
  25. Laemmli, U. K.(1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef] [Google Scholar]
  26. Lapointe, R., Tanaka, K., Barney, W., Whitfield, J., Banks, J., Beliveau, C., Stoltz, D., Webb, B. A. & Cusson, M.(2007). Genomic and morphological features of a banchine polydnavirus: comparison with bracoviruses and ichnoviruses. J Virol 81, 6491–6501.[CrossRef] [Google Scholar]
  27. Li, Y., Wang, J., Deng, R., Zhang, Q., Yang, K. & Wang, X.(2005).vlf-1 deletion brought AcMNPV to defect in nucleocapsid formation. Virus Genes 31, 275–284.[CrossRef] [Google Scholar]
  28. Lin, C. L., Lee, J. C., Chen, S. S., Wood, H. A., Li, M. L., Li, C. F. & Chao, Y. C.(1999). Persistent Hz-1 virus infection in insect cells: evidence for insertion of viral DNA into host chromosomes and viral infection in a latent status. J Virol 73, 128–139. [Google Scholar]
  29. Liu, W. & Saint, D. A.(2002). A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal Biochem 302, 52–59.[CrossRef] [Google Scholar]
  30. 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]
  31. Moreau, S., Huguet, E. & Drezen, J.-M.(2009). Polydnaviruses as tools to deliver wasp virulence factors to impair lepidopteran host immunity. In Insect Infection and Immunity: Evolution, Ecology and Mechanisms, pp. 137–158. Edited by Reynolds, S. E. & Rolff, J.. Oxford. : Oxford University Press. [Google Scholar]
  32. Murphy, N., Banks, J. C., Whitfield, J. B. & Austin, A. D.(2008). Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol 47, 378–395.[CrossRef] [Google Scholar]
  33. 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]
  34. Pertea, G., Huang, X., Liang, F., Antonescu, V., Sultana, R., Karamycheva, S., Lee, Y., White, J., Cheung, F. & other authors(2003). TIGR gene indices clustering tools (tgicl): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651–652.[CrossRef] [Google Scholar]
  35. Pfeffer, S. & Aivazian, D.(2004). Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 5, 886–896.[CrossRef] [Google Scholar]
  36. Raina, A. K. & Lupiani, B.(2006). Acquisition, persistence, and species susceptibility of the Hz-2V virus. J Invertebr Pathol 93, 71–74.[CrossRef] [Google Scholar]
  37. Raina, A. K., Adams, J. R., Lupiani, B., Lynn, D. E., Kim, W., Burand, J. P. & Dougherty, E. M.(2000). Further characterization of the gonad-specific virus of corn earworm, Helicoverpa zea. J Invertebr Pathol 76, 6–12.[CrossRef] [Google Scholar]
  38. Rozen, S. & Skaletsky, H. J.(2000). Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols; Methods in Molecular Biology, pp. 365–386. Edited by Krawetz, S. & Misener, S.. Totowa, NJ. : Humana Press. [Google Scholar]
  39. Sklan, E. H., Staschke, K., Oakes, T. M., Elazar, M., Winters, M., Aroeti, B., Danieli, T. & Glenn, J. S.(2007). A Rab-GAP TBC domain protein binds hepatitis C virus NS5A and mediates viral replication. J Virol 81, 11096–11105.[CrossRef] [Google Scholar]
  40. Slack, J. & Arif, B. M.(2007). The baculovirus occlusion-derived virus: virion structure and function. Adv Virus Res 69, 99–165. [Google Scholar]
  41. Stoltz, D. B.(1990). Evidence for chromosomal transmission of polydnavirus DNA. J Gen Virol 71, 1051–1056.[CrossRef] [Google Scholar]
  42. 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]
  43. The Nasonia Genome Working Group(2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343–348.[CrossRef] [Google Scholar]
  44. Vigdorovich, V., Miller, A. D. & Strong, R. K.(2007). Ability of hyaluronidase 2 to degrade extracellular hyaluronan is not required for its function as a receptor for jaagsiekte sheep retrovirus. J Virol 81, 3124–3129.[CrossRef] [Google Scholar]
  45. Wang, Y. & Jehle, J. A.(2009). Nudiviruses and other large double-stranded circular DNA viruses of invertebrates: new insights into an old topic. J Invertebr Pathol 101, 187–193.[CrossRef] [Google Scholar]
  46. Wang, Y., Burand, J. P. & Jehle, J. A.(2007a). Nudivirus genomics: diversity and classification. Virol Sin 22, 128–136.[CrossRef] [Google Scholar]
  47. Wang, Y., Kleespies, R. G., Huger, A. M. & Jehle, J. A.(2007b). The genome of Gryllus bimaculatus nudivirus indicates an ancient diversification of baculovirus-related nonoccluded nudiviruses of insects. J Virol 81, 5395–5406.[CrossRef] [Google Scholar]
  48. Wang, Y., van Oers, M. M., Crawford, A. M., Vlak, J. M. & Jehle, J. A.(2007c). Genomic analysis of Oryctes rhinoceros virus reveals genetic relatedness to Heliothis zea virus 1. Arch Virol 152, 519–531.[CrossRef] [Google Scholar]
  49. 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. Seventh Report of the International Committee on Taxonomy, pp. 253–260. Edited by van Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H., Carstens, E. B., Estes, M. K., Lemon, S. M., Maniloff, J., Mayo, M. A., McGeoch, D. J. & other authors. San Diego, CA. : Academic Press. [Google Scholar]
  50. 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]
  51. Weber, B., Annaheim, M. & Lanzrein, B.(2007). Transcriptional analysis of polydnaviral genes in the course of parasitization reveals segment-specific patterns. Arch Insect Biochem Physiol 66, 9–22.[CrossRef] [Google Scholar]
  52. Wu, W., Lin, T., Pan, L., Yu, M., Li, Z., Pang, Y. & Yang, K.(2006).Autographa californica multiple nucleopolyhedrovirus nucleocapsid assembly is interrupted upon deletion of the 38K gene. J Virol 80, 11475–11485.[CrossRef] [Google Scholar]
  53. 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]
  54. 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]
  55. 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]

Data & Media loading...


vol. , part 10, pp. 2610–2619

Amino acid sequences of nudivirus-related CiBV particle proteins having similarity to nudivirus/baculovirus core gene products or specific nudivirus gene products

Sequences of CiBV particle proteins having no similarity to gene products of nudiviruses or baculoviruses.

Primers used for RT-PCR

[ Single PDF file] (47 kB)


Most cited this month Most Cited RSS feed

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