BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Exogenous JH and ecdysteroid applications alter initiation of polydnaviral replication in an endoparasitoid wasp, Cotesia plutellae (Braconidae: Hymenoptera)

  • Park, Bok-Ri (Department of Bioresource Sciences, Andong National University) ;
  • Kim, Yong-Gyun (Department of Bioresource Sciences, Andong National University)
  • Received : 2011.01.03
  • Accepted : 2011.04.11
  • Published : 2011.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Polydnaviruses are a group of double-stranded DNA viruses and are symbiotically associated with some ichneumonoid wasps. As proviruses, the replication of polydnaviruses occurs in the female reproductive organ at the pupal stage. This study analyzed the effects of two developmental hormones, juvenile hormone (JH) and ecdysteroid, on the viral replication of Cotesia plutellae bracovirus (CpBV). All 23 CpBV segments identified contained a conserved excision/rejoining site ('AGCTTT') from their proviral segments. Using quantitative real-time PCR based on this excision/rejoining site marker, initiation of CpBV replication was determined to have occurred on day 4 on the pupal stage. Pyriproxyfen, a JH agonist, significantly inhibited adult emergence of C. plutellae, whereas RH5992, an ecdysteroid agonist, had no inhibitory effect. Although RH5992 had no effect dose on adult development, it significantly accelerated viral replication. The results of immunoblotting assays against viral coat proteins support the effects of the hormone agonists on viral replication.

Keywords

References

  1. Webb, B. A. (1998) Polydnavirus biology, genome structure and evolution; in The Insect Viruses, (Miller, L. K. and Ball, A., eds.), pp. 105-139, Plenum Press, New York, USA.
  2. Webb, B. A., Beckage, N. E., Hayakawa, Y., Krell, P. J., Lanzrein, B., Stoltz, D. B., Strand, M. R. and Summers, M. D. (2000) Polydnaviridae; in Virus Taxonomy, (Van Regenmortel, M. H. B., Faquet, C. M., Bishop, D. H. L., Carstens, E. B., Estes, M. K., Lennon, S. M., Maniloff, J., Mayo, M. A., McGeoch, D. J., Pringle, C. R. and Wickner, R. B., eds.), pp. 253-260, Academic Press, New York, USA.
  3. Whitfield, J. B. and Asgari, S. (2003) Virus or not: phylogenetics of polydnaviruses and their wasp carriers. J. Insect Physiol. 49, 397-405. https://doi.org/10.1016/S0022-1910(03)00057-X
  4. Webb, B. A. and Strand, M. R. (2005) The biology and genomics of polydnaviruses; in Comprehensive Insect Molecular Sciences, Vol. 6. (Gilbert, L. I., Iatrou, K. and Gill, S. S., eds.), pp. 323-360, Elsevier, San Diego, USA.
  5. Wyler, T. and 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. https://doi.org/10.1099/vir.0.18830-0
  6. Blissard, G. W., Smith, O. P. and Summers, M. D. (1987) Two related viral genes are located on a single superhelical DNA segment of the multipartite Campoletis sonorensis virus genome. Virology 160, 120-134. https://doi.org/10.1016/0042-6822(87)90052-3
  7. Webb, B. A. and Summers, M. D. (1992) Stimulation of polydnavirus replication by 20-hydroxyecdysone. Experientia 10, 1018-1022.
  8. Wyder, S., Tschannen, A., Hochuli, A., Gruber, A., Saladin, V., Zumbach, S. and Lanzrein, B. (2002) Characterization of Chelonus inanitus polydnavirus segments: sequences and analysis, excision site and demonstration of clustering. J. Gen. Virol. 83, 247-256. https://doi.org/10.1099/0022-1317-83-1-247
  9. Bae, S. and Kim, Y. (2004) Host physiological changes due to parasitism of a braconid wasp Cotesia plutellae on diamondback moth Plutella xylostella. Comp. Biochem. Physiol. A 138, 39-44. https://doi.org/10.1016/j.cbpb.2004.02.018
  10. Kim, Y., Bae, S. and Lee, S. (2004) Polydnavirus replication and ovipositional habit of Cotesia plutellae. Korean J. Appl. Entomol. 43, 225-231.
  11. Basio, N. and Kim, Y. (2006) Additive effect of teratocyte and calyx fluid from Cotesia plutellae on immunosuppression of Plutella xylostella. Physiol. Entomol. 31, 1-7. https://doi.org/10.1111/j.1365-3032.2005.00487.x
  12. Ibrahim, A. M. and Kim, Y. (2006) Parasitism by Cotesia plutellae alters the hemocyte population and immunological function of the diamondback moth, Plutella xylostella. J. Insect Physiol. 52, 943-950. https://doi.org/10.1016/j.jinsphys.2006.06.001
  13. Madanagopal, N. and Kim, Y. (2007a) An evidence for host translation inhibitory factor encoded in a polydnavirus, Cotesia glomerata bracovirus, genome and its expression in parasitized cabbage white butterfly, Pieris rapae. J. Asia Pac. Entomol. 10, 351-356. https://doi.org/10.1016/S1226-8615(08)60375-1
  14. Madanagopal, N. and Kim, Y. (2006) Parasitization by Cotesia glomerata induces immunosuppression of Pieris rapae: effects of ovarian protein and polydnavirus. J. Asia Pac. Entomol. 9, 339-346. https://doi.org/10.1016/S1226-8615(08)60312-X
  15. Madanagopal, N. and Kim, Y. (2007b). A putative protein translation inhibitory factor encoded in Cotesia plutellae bracovirus suppresses host hemocyte spreading behavior. J. Insect Physiol. 53, 1283-1292. https://doi.org/10.1016/j.jinsphys.2007.07.004
  16. Ibrahim, A. M., Choi, J. Y., Je, Y. H. and Kim, Y. (2007) Protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus: sequence encoded in Cotesia plutellae bracovirus: sequence analysis, expression profile, and a possible biological role in host immunosuppression. Dev. Comp. Immunol. 31, 978-990. https://doi.org/10.1016/j.dci.2006.11.005
  17. Ibrahim, A. M. and Kim, Y. (2008) Transient expression of protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus inhibits insect cellular immune responses. Naturwissenschaften 95, 25-32.
  18. Ibrahim, A. M., Choi, J. Y., Je, Y. H. and Kim, Y. (2005) Structure and expression profiles of two putative Cotesia plutellae bracovirus genes (CpBV-H4 and $CpBV-E94{\alpha}$) in parasitized Plutellae xylostella. J. Asia Pac. Entomol. 8, 359-366. https://doi.org/10.1016/S1226-8615(08)60258-7
  19. Lee, K., Cho, S., Lee, H., Choi, J. Y., Je, Y. H. and Kim, Y. (2005) Gene expression of Cotesia plutellae bracovirus and their expression profiles in parasitized Plutella xylostella. Arch. Insect Biochem. Physiol. 67, 157-171
  20. Park, B. and Kim, Y. (2010) Transient transcription of a putative RNase containing BEN domain encoded in Cotesia plutellae bracovirus induces an immunosuppression of the diamondback moth, Plutella xylostella. J. Invertebr. Pathol. 105, 156-163. https://doi.org/10.1016/j.jip.2010.06.003
  21. Riddiford, L. M., Hiruma, K., Zhou, X. and Nelson, C. A. (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem. Mol. Biol. 33, 1327-1338. https://doi.org/10.1016/j.ibmb.2003.06.001
  22. Marti, D., Grossniklaus-Buragin, C., Wyder, S., Wyler, T. and 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. https://doi.org/10.1099/vir.0.18832-0
  23. Desjardins, C. A., Gundersen-Rindal, D. E., Hostetler, J. B., Tallon, L. J., Fuester, R. W., Schatz, M. C., Pedroni, M. J., Fadtosh, D. W., Haas, B. J., Toms, B. S., Chen, D. and Nene, V. (2007) Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol. 26, 7-61.
  24. Blissard, G. W., Vinson, S. B. and Summers, M. D. (1986) Identification, mapping, and in vitro translation of Campoletis sonorensis virus mRNAs from parasitized Heliothis virescens larvae. J. Virol. 57, 318-327.
  25. Bezier, A., Herbiniere, J., Lanzrein, B. and Drezen, J.M. (2009) Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. J. Invertebr. Pathol. 101, 194-203. https://doi.org/10.1016/j.jip.2009.04.006
  26. Stoltz, D. B. (1990) Evidence for chromosomal transmission of polydnavirus DNA. J. Gen. Virol. 71, 1051-1056. https://doi.org/10.1099/0022-1317-71-5-1051
  27. Bezier, A., Annaheim, M., Herbiniere, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., Wincker, P., Roditi, I., Heller, M., Belghazi, M., Pfister-Wilhem, R., Periquet, G., Dupuy, C., Huguet, E., Volkoff, A. N., Lanzrein, B. and Drezen, J. M., (2009) Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926-930. https://doi.org/10.1126/science.1166788
  28. Norton, W. N. and Vinson, S. B. (1983) Correlating the initiation of virus replication with a specific pupal developmental phase of an ichneumonid parasitoid. Cell Tissue Res. 231, 387-398.
  29. Savary, S., Beckage, M., Tan, F., Periquet, G. and Drezen, J. M. (1997) Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregate (Braconidae, Microgastrinae) is developmentally regulated but not strictly restricted to the ovaries in the adult. Insect Mol. Biol. 8, 319-327.
  30. Chen, Y. P., Taylor, P. B., Shapiro, M. and 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. https://doi.org/10.1046/j.1365-2583.2003.00411.x
  31. Beck, J. L., Urathamakul, T., Watt, S. J., Sheil, M. M., Schaeffer, P. M. and Dixon, N. E. (2006) Proteomic dissection of DNA polymerization. Expert Rev. Proteomics 3, 197-211. https://doi.org/10.1586/14789450.3.2.197
  32. Webb, B., Strand, M., Dickey, S., Beck, M., Hilgarth, R., Barney, W., Kadash, K., Kroemer, J., Lindstrom, G., Rattanadechakul, W., Shelby, K., Thoetkiattikul, H., Turnbull, M. and Witherell, R. (2006) Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347, 160-174. https://doi.org/10.1016/j.virol.2005.11.010
  33. Bezier, A., Herbiniere, J., Serbielle, C., Lesobre, J., Wincker, P., Huguet, E. and Drezen, J. M. (2008) Bracovirus gene products are highly divergent from insect proteins. Arch. Insect Biochem. Physiol. 67, 172-187. https://doi.org/10.1002/arch.20219
  34. Volkoff, A. N., Jouan, V., Urbach, S., Samain, S., Bergoin, M., Wincker, P., Demettre, E., Cousserans, F., Provost, B., Coulibaly, F., Legeai, F., Beliveau, C., Cusson, M., Gyapay, G. and Drezen, J. M. (2010) Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLos Pathog. 6, e1000923.
  35. Spradling, A. C. (1981) The organization and amplification of two chromosomal domains Drosophila chorion genes. Cell 27, 193-201. https://doi.org/10.1016/0092-8674(81)90373-1
  36. Calvi, B. R., Lilly, M. A. and Spradling, A. C. (1998) Cell cycle control of chorion gene amplification. Genes Dev. 12, 734-744. https://doi.org/10.1101/gad.12.5.734
  37. Tzolovsky, G., Deng, W. M., Schlitt, T. and Bownes, M. (1999) The function of the Broad-Complex during Drosophila melanogaster oogenesis. Genetics 153, 1371-1383.
  38. Sun, J., Smith, L., Armento, A. and Deng, W. M. (2008) Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J. Cell Biol. 182, 885-896. https://doi.org/10.1083/jcb.200802084
  39. Wu, Y., Parthasarathy, R., Bai, H. and Palli, S. R. (2006) Mechanisms of midgut remodeling: juvenile hormone analog methoprene blocks midgut metamorphosis by modulating ecdysone action. Mech. Dev. 123, 530-547. https://doi.org/10.1016/j.mod.2006.05.005
  40. Livak, K. J. and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. https://doi.org/10.1006/meth.2001.1262
  41. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685. https://doi.org/10.1038/227680a0
  42. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some application. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354. https://doi.org/10.1073/pnas.76.9.4350
  43. Kim, Y. and Kim, J. (2004) Inhibitory effect of Cotesia plutellae bracovirus (CpBV) on development of a non-natural host, Spodoptera exigua. Korean J. Appl. Entomol. 43, 217- 223.
  44. Annaheim, M. and 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. https://doi.org/10.1099/vir.0.82396-0
  45. SAS Institute, Inc. (1989) SAS/STAT User's Guide, release 6.03, ed., SAS Institute, Cary, NC.

Cited by

  1. Roles of Peroxinectin in PGE2-Mediated Cellular Immunity in Spodoptera exigua vol.9, pp.9, 2014, https://doi.org/10.1371/journal.pone.0105717
  2. Translational Control of Host Gene Expression by a Cys-Motif Protein Encoded in a Bracovirus vol.11, pp.9, 2016, https://doi.org/10.1371/journal.pone.0161661
  3. Juvenile hormone regulates an expression of a late gene encoded in a polydnavirus, Cotesia plutellae bracovirus vol.165, pp.2, 2013, https://doi.org/10.1016/j.cbpa.2013.03.012