Journal of Asia-Pacific Entomology

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지

Parasitism of Cotesia spp. Enhances Susceptibility of Plutella xylostella to Other Pathogens

  • Jung, Sung-Chae (Department of Agricultural Biology, Andong National University) ;
  • Kwoen, Min (Environment Management Division, National Institute of Highland Agriculture, RDA) ;
  • Choi, Jae-Young (Department of Entomology, School of Agricultural Biotechnology, Seoul National University) ;
  • Je, Yeon-Ho (Department of Entomology, School of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Yong-Gyun (Department of Agricultural Biology, Andong National University)
  • Published : 2006.09.30
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Abstract

Two endoparasitoids, Cotesia plutellae and C. glomerata, parasitize the diamondback moth, Plutella xylostella, and induce significant host immunosuppression. This study analyzed the susceptibility changes of the parasitized P. xylostella against other pathogens using an entomopathogenic bacterium, Xenorhabdus nematophila (Xn), and a viral pathogen, Autographa californica nucleopolyhedrosis virus (AcNPV). The P. xylostella parasitized by either C. plutellae or C. glomerata exhibited higher susceptibilities to both microbial pathogens than the nonparasitized. To determine the parasitism factors inducing the enhanced susceptibility, three polydnaviral genes so far successfully cloned were selected from C. plutellae bracovirus (CpBV). CpBV-lectin and CpBV15${\alpha}/{\beta}$ were inserted into AcNPV under a CpBV promote and analyzed in their pathogenicities against P. xylostella larvae. Two AcNPVs recombined with CpBV15${\alpha}/{\beta}$ were more potent than the control AcNPV recombined with an enhanced green fluorescent protein gene or the AcNPV recombined with CpBV-lectin. These results suggest that the wasp parasitization enhances other pathogen susceptibilities by inducing host immunosuppression, in which the symbiotic polydnavirus can play significant role in the enhanced susceptibility.

Keywords

References

  1. Akhurst, R.J. 1980. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121: 303-309
  2. Amaya, K.E., S. Asgari, R. Jung, M. Hongskula and N.E. Beckage. 2005. Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. J. Insect Physiol. 51: 505-512 https://doi.org/10.1016/j.jinsphys.2004.11.019
  3. Bae, S. and Y. Kim. 2004. Host physiological changes due to parasitism of a braconid wasp, Cotesia plutellae, on diamondback moth, Plutella xylostella. Comp. Biochem. Physiol. 138A: 39-44
  4. Basio, N.A. and Y. Kim. 2005. A short review of teratocytes and their characters in Cotesia plutellae (Bracovirus: Hymenoptera). J. Asia-Pacific Entomol. 8: 211-217 https://doi.org/10.1016/S1226-8615(08)60093-X
  5. Basio, N.A. and Y. Kim. 2006. Additive effect of teratocyte and calyx fluid from Cotesia plutellae on immunosuppression of Plutella xylostella. Physiol. Entomol. (In press)
  6. Choi, J.Y., J.Y. Roh, J.N. Kang, H.J. Shim, S.D. Woo, B.R. Jin, M.S. Li and Y.H. Je. 2005. Genomic segments cloning and analysis of Cotesia plutellae polydnavirus using plasmid capture system. Biochem. Biophys. Res. Comm. 332: 487-493 https://doi.org/10.1016/j.bbrc.2005.04.146
  7. Clem, R.J. 1997. Regulation of programmed cell death by baculoviruses. pp. 237-266, in The baculoviruses, Ed. L.K. Miller. Plenum, NY
  8. Clem, R.J., M. Fechheimer and L.K. Miller. 1991. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388-1390 https://doi.org/10.1126/science.1962198
  9. Clem, R.J. and L.K. Miller. 1993. Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J. Virol. 67: 3730-3738
  10. Clem, R.J., M. Robson and L.K. Miller. 1994. Influence of infection route on the infectivity of baculovirus mutants lacking the apoptosis-inhibiting gene p35 and the adjacent gene p94. J. Virol. 68: 6759-6762
  11. Dahlman, D.L. 1991. Teratocytes and host/parasitoid interactions. Biol. Control 1: 118-126 https://doi.org/10.1016/1049-9644(91)90110-L
  12. Friesen, P.D. and L.K. Miller. 1987. Divergent transcription of early 35- and 94-kildalton protein genes encoded by the HindIII K genome fragment of the baculovirus Autographa californica nuclear polyhedrosis virus. J. Virol. 61: 2264-2272
  13. Glatz, R., O. Schmidt and S. Asgari. 2003. Characterization of a novel protein with homology to C-type lectins expressed by the Cotesia rubecula bracovirus in larvae of the lepidopteran host, Pieris rapae. J. Biol. Chem. 278: 19743-19750 https://doi.org/10.1074/jbc.M301396200
  14. Gu, H., Q. Wang and S. Dorn. 2003. Superparasitism in Cotesia glomerata: response of hosts and consequences for parasitoids. Ecol. Entomol. 28: 422-431 https://doi.org/10.1046/j.1365-2311.2003.00535.x
  15. Hayakawa, Y. 1994. Cellular immunosuppressive protein in the plasma of parasitized insect larvae. J. Biol. Chem. 269: 14536-14540
  16. Hotta, M., T. Okuda and T. Tanaka. 2001. Cotesia kariyai teratocytes: growth and development. J. Insect Physiol. 47: 31-41 https://doi.org/10.1016/S0022-1910(00)00089-5
  17. Ibrahim, A.M.A., J.Y. Choi, Y.H. Je and Y. Kim. 2005. Structure and expression profiles of two putative Cotesia plutellae bracovirus genes (CpBV-H4 and CpBV-E94() in parasitized Plutella xylostella. J. Asia-Pacific Entomol. 8: 359-366 https://doi.org/10.1016/S1226-8615(08)60258-7
  18. Je, Y.H., J.H. Chang, J.Y. Rho and B.R. Jin. 2001. Generation of baculovirus expression vector using defective Autographa californica nuclear polyhedrosis virus genome maintained in Escherichia coli for $Oec^{+}$ virus production. Int. J. Indust. Entomol. 2: 155-160
  19. Ji, D., Y. Yi and Y. Kim. 2004. 16S rDNA sequence and biochemical characters of a Korean isolate of Xenorhabdus nematophila. J. Asia-Pacific Entomol. 7: 105-111 https://doi.org/10.1016/S1226-8615(08)60205-8
  20. Kim, Y. 2005. Identification of host translation inhibitory factor of Campoletis sonorensis ichnovirus on the tobacco budworm, Heliothis virescens. Arch. Insect Biochem. Physiol. 59: 230-244 https://doi.org/10.1002/arch.20074
  21. Kim, Y., S. Bae and S. Lee. 2004. Polydnavirus replication and ovipositional habit of Cotesia plutellae. Korean J. Appl. Entomol. 43: 225-231
  22. Kim, Y., N.A. Basio, A.M.A. Ibrahim and S. Bae. 2006. Gene structure of Cotesia plutellae bracovirus (CpBV)-IkB and its expression pattern in the parasitized diamondback moth, Plutella xylostella. Korean J. Appl. Entomol. 45: 1-10 https://doi.org/10.1111/j.1440-6055.2006.00517.x
  23. Kitano, H., H. Wago and T. Arakawa. 1990. Possible role of teratocytes of the gregarious parasitoid, Cotesia (=Apanteles) glomerata in the suppression of phenoloxidase activity in the larval host, Pieris rapae crucivora. Arch. Insect Biochem. Physiol. 13: 177-185 https://doi.org/10.1002/arch.940130305
  24. Krell, P.J., M.D. Summers and S.D. Vinson. 1982. A virus with a multipartite superhelical DNA genome from the ichneumonid parasitoid, Campoletis sonorensis. J. Virol. 43: 859-870
  25. Laing, J.E. and D.B. Levin. 1982. A review of the biology and a bibliography of Apanteles glomeratus (L.) (Hymenoptera: Braconidae). Biocon. News Inform. 3: 7-23
  26. Lee, S. 2004. Study on polydnavirus-derived genes and their functions related with parasitism by Cotesia plutellae against diamondback moth, Plutella xylostella. 157pp. MS Thesis, Andong National University, Andong, Korea
  27. Lee, K., S. Cho, H. Lee, J.Y. Choi, Y.H. Je and Y. Kim. 2005. Gene expression of Cotesia plutellae bracovirus EP1-like protein (CpBV-ELP1) in parasitized diamondback moth, Plutella xylostella. J. Asia-Pacific Entomol. 8: 249-255 https://doi.org/10.1016/S1226-8615(08)60242-3
  28. Norton, W.N. and S.B. Vinson. 1983. Correlating the initiation of virus replication with a specific pupal developmental phase of an ichneumonid parasitoid. Cell Tissue Res. 231: 387-389
  29. Ockroy, K.S., T.J. Cole, T.E. Trenczek and S. Dorn. 2002. Comparison of parasitism by Cotesia glomerata with bacterial infection and wounding in Pieris brassicae: induction of new haemolymph polypeptides and changes in humoral immune response. J. Invertebr. Pathol. 81: 12-18 https://doi.org/10.1016/S0022-2011(02)00146-5
  30. Ockroy, K., T. Trenczek and S. Dorn. 1997. Parasitism by Cotesia glomerata induces several changes in the hemolymph protein pattern of the host insect Pieris brassicae. Verh. Dtsch. Zool. Ges. 90: 130
  31. O'Reilly, D.R., L.K. Miller and V.A. Luckow. 1992. Baculovirus expression vectors: a laboratory manual. 347p. Oxford University Press, New York
  32. Park, Y., Y. Kim and Y. Lee. 1999. Identification and characterization of a symbiotic bacterium associated with Steinernema carpocapsae in Korea. J. Asia-Pacific Entomol. 2: 105-111 https://doi.org/10.1016/S1226-8615(08)60038-2
  33. Schmidt, O., S. Asgari, M. Beck and U. Theopold. 2000. Host defence manipulation by parasitoid wasps and the problem of assessing host specificity. pp. 29-37, in Hymenoptera: evolution, biodiversity and biological control, Eds. A.D. Austin and M. Dowton. 467pp. CSIRO publishing, Collingwood, Victoria, Australia
  34. Stoltz, D.B. and J.B. Whitfield. 1992. Viruses and virus-like entities in the parasitic hymenoptera. J. Hymenopt. Res. 1: 125-139
  35. Strand, M.R. and L.L. Pech. 1995. Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. J. Gen. Virol. 76: 283-291 https://doi.org/10.1099/0022-1317-76-2-283
  36. Strand, M.R. and E.A. Wong. 1991. The growth and role of Microplitis demolitor teratocytes in parasitism of Pseudoplusia includens. J. Insect Physiol. 37: 503-515 https://doi.org/10.1016/0022-1910(91)90027-W
  37. Tanaka, T. and H. Wago. 1990. Ultrastructural and functional maturation of teratocytes of Apanteles kariyai. Arch. Insect Biochem. Physiol. 13: 187-197 https://doi.org/10.1002/arch.940130306
  38. Vinson, S.B. 1970. Development and possible functions of teratocytes in the host-parasite association. J. Invert. Pathol. 20: 118-123
  39. Washburn, J.O., E. Haas-Stapleton, F.F. Tan, N.E. Beckage and L.E. Volkman. 2000. Co-infection of Manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by Autographa californica M. nucleopolyhedrovirus. J. Insect Physiol. 46: 179-190 https://doi.org/10.1016/S0022-1910(99)00115-8
  40. Washburn, J.O., B.A. Kirkpatrick and L.E. Volkman. 1996. Insect protection against viruses. Nature 383: 767 https://doi.org/10.1038/383767a0
  41. Webb, B.A. 1988. Polydnavirus biology, genome structure and evolution. pp. 105-139, in The insect virus, Eds. L.K. Miller and A. Ball. Plenum Press, New York
  42. Webb, B.A. and M.R. Strand. 2005. The biology and genomics of polydnaviruses. pp. 323-360, in Comprehensive molecular insect science. Vol. 6. Eds. L.I. Gilbert, K. Iatrou and S.S. Gill. Elsevier, Oxford, UK
  43. Webb, B.A. and M.D. Summers. 1992. Stimulation of polydnavirus replication by 20-hydroxyecdysone. Experientia 48: 1018-1022 https://doi.org/10.1007/BF01919157
  44. Whitfield, J.B. and S. Asgari. 2003. Virus or not? Phylogenetics of plydnaviruses and their wasp carriers. J. Insect Physiol. 49: 397-405 https://doi.org/10.1016/S0022-1910(03)00057-X