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Revista Latinoamericana de Microbiología

2006, Número 1

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Microbiología 2006; 48 (1)


Estrategias co-evolutivas de la interacción entre parasitoides y polidnavirus

Rodríguez-Pérez MA, Beckage NE

Idioma: Español
Referencias bibliográficas: 208
Paginas: 31-43
Archivo PDF: 196.43 Kb.


RESUMEN

El polidnavirus es material genético en simbiosis con las avispas endoparasitoides del orden himenóptera, particularmente de las familias Icneumonidae (icnovirus) y Braconidae (bracovirus). Los polidnavirus se encuentran en estado de pro-virus integrados en el genoma cromosómico de las avispas y de ahí se escinden para posteriormente replicarse cuando la avispa está en desarrollo hacia el estado adulto. Durante la oviposición, las partículas virales, ya bien formadas, son depositadas junto con los huevos de la avispa parasitoide dentro del insecto huésped de donde nacen larvas que se desarrollan. La principal función de los polidnavirus es suprimir el sistema inmune del insecto huésped, por consecuencia, las células de defensa (o hemocitos) no pueden encapsular los huevos o larvas del parasitoide. Las proteínas o ARN de los polidnavirus se producen una vez que ocurre la parasitosis alterando las propiedades de adhesión de los hemocitos y, por tanto, no encapsulan al parasitoide; en algunas especies, los productos génicos conducen al proceso de apoptosis de los hemocitos del insecto huésped y, por tanto, su sistema inmune queda deprimido. Este artículo revisa las principales características de los polidnavirus ofreciendo una perspectiva general de su función dentro del lepidóptero hospedador de la avispa parasitoide la cual contiene los polidnavirus integrados en su genoma o en forma libre para regular la fisiología del insecto huésped una vez que es parasitado.


REFERENCIAS (EN ESTE ARTÍCULO)

  1. Adamo, S.A., C.E. Linn & N. E. Beckage. 1997. Correlation between changes in host behavior and octopamine levels in the tobacco hornworm, Manduca sexta, parasitized by the gregarious braconid parasitoid wasp Cotesia congregata. J. Exp. Biol. 200:117-127.

  2. Asgari, S. & O. Schmidt. 1994. Passive protection of eggs from the parasitoid Cotesia rubecula in the host Pieris rapae. J. Insect. Physiol. 40:789-795.

  3. Asgari, S. & O. Schmidt. 2002. A coiled-coil region of an insect immune suppressor protein is involved in binding and uptake by hemocytes. Insect. Biochem. Mol. Biol. 32:497-504.

  4. Asgari S., M. Hellers & O. Schmidt. 1996. Host haemocyte inactivation by an insect parasitoid: transient expression of a polydnavirus gene. J. Gen. Virol. 77:2653-2662. Rodríguez-Pérez et al Co-evolución de parasitoides y polidnavirus

  5. Rev Latinoam Microbiol 2006; 48 (1): 31-43 41

  6. Asgari, S., O. Schmidt & U. Theopold. 1997. A polydnavirusencoded protein of an endoparasitoid wasp is an immune suppressor. J. Gen. Virol. 78:3061-3070.

  7. Beckage, N.E. 1993. Games parasites play: the dynamic roles of peptides and proteins in the host-parasite interaction. En: N.E. Beckage, S.N. Thompson, and B.A. Federici, Eds. Parasites and Pathogens of Insects, Vol 1. Academic Press, N. Y. pp. 25-58.

  8. Beckage, N.E. & D.B. Gelman. 2004. Wasp parasitoid disruption of host development: Implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299-330.

  9. Beckage, N.E., J.S. Metcalf, D.J. Nesbit, K.W. Schliefer, S.R. Zetlan & I. de Buron. 1990. Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by a wasp polydnavirus. Insect. Biochem. 20:285-294.

  10. Beckage, N.E., F.F. Tan, K.W. Schleifer, R.D. Lane & L.L. Cherubin. 1994. Characterization and biological effects of Cotesia congregata polydnavirus on host larvae of the tobacco hornworm, Manduca sexta. Arch. Insect. Biochem. Physiol. 26:165-195.

  11. Beckage, N.E., T.J. Templeton, B.D. Nielsen, D.I. Cook & D.B. Stoltz. 1987. Parasitism-induced hemolymph polypeptides in Manduca sexta (L.) larvae parasitized by the braconid wasp Cotesia congregata (Say). Insect. Biochem. 17:439-455.

  12. Béliveau, C., A. Levasseur, D. Stoltz & M. Cusson. 2003. Three related TrIV genes: comparative sequence analysis and expression in host larvae and Cf-124T cells. J. Insect. Physiol. 49:501-512.

  13. Belle, E., N.E. Beckage, J. Rousselet, M. Poirie, F. Lemeunier & J.M. Drezen. 2002. Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J. Virol. 76:5793-96.

  14. Blissard, G.W., S.B. Vinson & M.D. Summers. 1986. Identification, mapping, and in vitro translation of Campoletis sonorensis virus mRNAs from parasitized Heliothis virescens larvae. J. Virol. 57:318-327.

  15. Bonvin, M., D. Marti, S. Wyder, D. Kojic, M. Annaheim, & B. Lanzrein. 2005. Cloning, characterization and analysis by RNA interference of various genes of the Chelonus inanitus polydnavirus. J. Gen. Virol. 86:973-983.

  16. Buron, de I. & N.E. Beckage. 1992. Characterization of a polydnavirus (PDV) and virus-like filamentous particle (VLFP) in the braconid wasp Cotesia congregata (Hymenoptera: Braconidae). J. Invertebr. Pathol. 59:315-327.

  17. Cui, L. & B.A. Webb. 1996. Isolation and characterization of a new member of the cysteine-rich Campoletis sonorensis polydnavirus gene family. J. Gen. Virol. 77:797-809.

  18. Cui L., Soldevila A. & Webb B.A. 1997. Expression and hemocyte- targeting of a Campoletis sonorensis polydnavirus cysteine-rich gene in Heliothis virescens larvae. Arch. Insect. Biochem. Physiol. 36:251-271.

  19. Cook, D.I., D.B. Stoltz & S.B. Vinson. 1984 Induction of a new haemolymph glycoprotein in larvae of permissive hosts parasitized by Campoletis sonorensis. Insect. Biochem. 14:45-50.

  20. Davies, D.H. & S.B. Vinson. 1986. Passive evasion by eggs of braconid parasitoid Cardiochles nigriceps of encapsulation in vitro by haemocytes of host Heliothis virescens: Possible role

  21. for fibrous layer in immunity. J. Insect. Physiol. 32:1003-1010.

  22. DeBorde, S., W. Rattanadechakul, Y. Kim, J.A. Kroemer, B.A. Webb, L. Thoetkiattial, A. Witherell and M.R. Strand. 2002. Characterization of the Microplitis demolitor bracovirus genome Memorias del 50th Annual Meeting of the Entomological Society of America. November 17-20, Fort Lauderdale, Florida. USA, D0032.

  23. Dib-Hajj, S.D., B.A. Webb & M.D. Summers. 1993. Structure and evolutionary implications of a “cysteine-rich” Campoletis sonorensis polydnavirus gene family. Proc. Natl. Acad. Sci. USA. 90: 3765-3769.

  24. Drezen, J.M., B. Provost, E. Espagne, L. Cattolico, C. Dupuy, M. Poirie, G. Periquet & E. Huguet. 2003. Polydnavirus genome: integrated vs free virus. J. Insect. Physiol. 49:407-417.

  25. Dushay, M.S. & N.E. Beckage. 1993. Dose-dependent separation of Cotesia congregata-associated polydnavirus effects on Manduca sexta larval development and immunity. J. Insect. Physiol. 39:1029-1040.

  26. Dumpit, R., M.A. Rodríguez-Pérez, M. Alleyne & N.E. Beckage. 2004. Cotesia flavipes and Manduca sexta: A model for studying parasitoid encapsulation in refractory hosts. Memorias del 52nd Annual Meeting of the Entomological Society of America. Noviembre 14-17, Salt Lake City, Utah. pág. 43.

  27. Edson, K.M., S.B. Vinson, D.B. Stoltz & M.D. Summers. 1981. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid’s host. Science. 211:582-583.

  28. Espagne, E., C. Dupuy, E. Huguet, L. Cattolico, B. Provost, N. Martins, M. Poirié, G. Periquet & J.M. Drezen. 2004. Genome sequence of a polydnavirus: Insights into symbiotic virus evolution. Science 306:286-289.

  29. Fedderson, I., K. Sander & O. Schmidt. 1986. Virus-like particles with host protein-like antigenic determinants protect an insect parasitoid from encapsulation. Experientia. 42:1278-1281.

  30. Federici, B.A. 1991. Viewing polydnaviruses as gene vectors of endoparasitic Hymenoptera. Redia 74:387-392.

  31. Federici, B.A. & Y. Bigot. 2003. Origin and evolution of polydnaviruses

  32. by symbiognesis of insect DNA viruses in endoparasitic wasps. J. Insect. Physiol. 49:419-432.

  33. Fleming, J.G.W. 1992. Polydnaviruses: mutalists and pathogens. Annu. Rev. Entomol. 37:401-425.

  34. Fleming, J.G.W. & P. Krell. 1993. Polydnavirus genome organization. En: N. E., Beckage, S.N. Thompson, and B.A. Federici, Eds. Parasites and Pathogens of Insects, Vol 1. Academic Press, NY. pp. 189-225.

  35. Fleming, J.G.W. & M.D. Summers. 1991. Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc. Natl. Acad. Sci. 88:9770-9774.

  36. Fleming, J.G.W., G.W. Blissard, M.D. Summers & S.B. Vinson. 1983. Expression of Campoletis sonorensis virus in the parasitized host, Heliothis virescens. J. Virol. 48:74-78.

  37. Galibert L., J. Rocher, M. Ravallec, M. Duonor-Cérutti, B.A. Webb & A.N. Volkoff. 2003. Two Hyposoter didmator ichnovirus genes expressed in the lepidopteran host encode secreted or membrane-associated serine and threonine rich proteins in segments that may be nested. J. Insect. Physiol. 49:441-452.

  38. Godfray, H.C.J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press.

  39. Gruber, A., P. Stettler, P. Heiniger, D. Schumperli & B. Lanzrein. 1996. Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp genome and excised only in later pupal and adult stages of the female. J. Gen. Virol. 77:2873-2879.

  40. Gundersen-Rindal D.E. & Lynn D.E. 2003. Polydnavirus integration in lepidopteran host cells in vitro. J. Insect. Physiol. 49:453-462.

  41. Guzo, D. & D.B. Stoltz. 1987. Observations on cellular immunity and parasitism in the tussock moth. J. Insect. Physiol. 33:19-31.

  42. Harwood, S.H. & N.E. Beckage. 1994 Purification and characterization of an early-expressed polydnavirus-induced protein from the hemolymph of Manduca sexta larvae parasitized by Cotesia congregata. Insect. Biochem. Mol. Biol. 24:685-698.

  43. Harwood, S.H., A.J. Grosovsky, E.A. Cowles, J.W. Davis & N.E. Beckage. 1994. An abundantly expressed hemolymph glycoproRodríguez-Pérez et al Co-evolución de parasitoides y polidnavirus Rev Latinoam Microbiol 2006; 48 (1): 31-43 42 tein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. Virology. 205:381-392.

  44. Hayakaya Y. 1995. Growth-blocking peptide: an insect biogenic peptides that prevents the onset of metamorphosis. J. Insect. Physiol. 44:1-6.

  45. Hayakaya Y, I. Yuazaki, A. Yamanaka & T. Tanaka. 1994. Expression of polydnavirus genes from the parasitoid wasp Cotesia kariyai in two noctuid hosts. Insect. Mol. Biol. 3:97-103.

  46. Hellers, M., M. Beck, U. Theopold, M. Kamei & O. Schmidt. 1996. Multiple alleles encoding a virus-like particle protein in the ichneumonid wasp endoparasitoid Venturia canescens. Insect. Mol. Biol. 5:239-249.

  47. Krell, P. J. 1991. The polydnaviruses: multipartite DNA viruses from parasitic Hymenoptera. In: Viruses of Invertebrates (Ed. Krustak E.) pp. 141-177. Marcel Dekker, New York.

  48. Krell, P.J. & D.B. Stoltz. 1980. Virus-like particles in the ovary of an ichneumonid wasp: purification and preliminary characterization. Virology. 101:408-418.

  49. Kroemer, J.A. & B.A. Webb. 2004. Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu. Rev. Entomol. 49:431-456.

  50. Lapointe, R., R. Wilson, L. Vilaplana, D.R. O’Reilly, P. Falabella, V. Douris, M. Bernier-Cardou, F. Pennacchio, K. Latrou, C. Malva & J.A. Olszewski. 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.

  51. Lavine, M.D. & N.E. Beckage. 1995. Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitol. Today. 11:368-378.

  52. Lavine, M.D. & N.E. Beckage. 1996. Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata. J. Insect. Physiol. 42:39-49.

  53. Lavine, M.D. & M.R. Strand. 2002. Insect hemocytes and their role in immunity. Insect. Biochem. Mol. Biol. 32:1295-1309.

  54. Le, N.T., S. Asgari, K. Amaya, F.F. Tan & N.E. Beckage. 2003. Persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm. J. Insect. Physiol. 49:533-543.

  55. Li, X. & B.A. Webb. 1994. Apparent functional role for a cysteine- rich polydnavirus protein in suppression of the insect cellular immune response. J. Virol. 68:7482-7489.

  56. Luckhart, S. & B.A. Webb. 1996. Interaction of a wasp ovarian protein and polydnavirus in host immune suppression. Dev. Comp. Immunol. 20:1-21.

  57. Noguchi, H., Y. Harakawa & R.G.H. Downer. 1995. Elevation of dopamine levels in parasitized insect larvae. Insect. Biochem. Mol. Biol. 25:197-201.

  58. Richards E.H. & J.P. Edwards. 2000. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 127:289-298.

  59. Rizki, R.M. & T.M. Rizki. 1984. Selective destruction of a host blood cell type by a parasitoid wasp. Proc. Natl. Acad. Sci. USA. 81:6154-6158.

  60. Rizki, R.M. & T.M. Rizki. 1990. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc. Natl. Acad. Sci. USA. 97: 8388-8392.

  61. Rodríguez-Pérez, M.A., R. Dumpit, M. Hongskula & N. Beckage. 2004. Physiological consequences of the encapsulation of the parasitoid Cotesia flavipes in host larvae of the tobacco hornworm Manduca sexta. Memorias del IX European Multicolloquium of Parasitology, Valencia, España, 18-23 Julio. pág. 637.

  62. Rodríguez-Pérez, M.A., R.F. Dumpit, J.M. Lenz, E.N. Powell, S.Y. Tam & N. Beckage. 2005. Host Refractoriness of the Tobacco Hornworm, Manduca sexta, to the Braconid Endoparasitoid Cotesia flavipes. Arch. Insect. Biochem. Physiol. 60:159-171.

  63. Ross, D.R. & P.E. Dunn. 1989. Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta to bacterial infection. Dev. Comp. Immunol. 13:205-216.

  64. Rotheram S. 1973. The surface of the egg of a parasitic insect. I. The surface of the egg and the first instar larva of Nemeritis. Proc. R. Soc. London Ser. B. 183: 179-194.

  65. Russo J., S. Dupas, F. Frey, Y. Carton & M. Brehelin. 1996. Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology. 112:135-142.

  66. Salt, G. 1965. Experimental studies in insect parasitism XIII. The haemocytic reaction of a caterpillar to eggs of its habitual parasite. Proc. R. Soc. London Ser. B. 162:303-318.

  67. Savary, S., N.E. Beckage, F. Tan, G. Periquet & J.M. Drezen. 1997. Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastrinae) at potential recombinase binding sites. J. Gen. Virol. 83:2035.

  68. Schmidt, O., U. Theopold & M.R. Strand. 2001. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays. 23:344-351.

  69. Shelby, K.S. & B.A. Webb. 1994. Polydnavirus infection inhibits synthesis of an insect plasma protein, arylphorin. J. Gen. Virol. 75:2285-2292.

  70. Shelby, K.S. & B.A. Webb. 1997. Polydnavirus infection inhibits translation of specific growth-associated host proteins. Insect. Biochem. Mol. Biol. 27:263-270.

  71. Shelby, K.S. & B.A. Webb. 1999. Polydnavirus-mediated suppression of insect immunity. J. Insect. Physiol. 45:507-514.

  72. Soldevila, A.I. & B.A. Webb. 1996. Expression of polydnavirus genes under polydnavirus-promoter regulation in insect larvae infected with baculovirus recombinants. J. Gen. Virol. 77:1379-1388.

  73. Soldevila, A.I., S. Heuston & B.A. Webb 1997. Purification and analysis of a polydnavirus gene product expressed using a poly-histidine baculovirus vector. Insect. Biochem. Mol. Biol. 27:201-211.

  74. Sroka, P. & S.B. Vinson. 1978. Phenyloxidase activity in the hemolyph of parasitized and unparasitized Heliothis virescens. Insect. Biochem. 8:399-402.

  75. Stoltz, D.B. 1993. The polydnavirus life cycle. In Parasites and Pathogens of Insects. (Eds Beckage N.E., Thompson S.N., and Federici B.A.), Vol 1, pp. 167-189. Academic Press, NY.

  76. Stoltz, D.B. & D. Cook. 1983. Inhibition of host phenoloxidase activity by parasitoid Hymenoptera. Experientia. 39:1022-1024.

  77. Stoltz, D.B. & D. Guzo. 1986. Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. J. Insect. Physiol. 32:377-388.

  78. Stoltz, D.B. & J.B. Whitfield. 1992. Viruses and virus-like entities in the parasitic Hymenoptera. J. Hymenopt. Res. 1:125-139.

  79. Stoltz, D.B. & A. Makkay. 2003. Overt viral diseases induced from apparent latency following parasitization by the ichneumonid wasp, Hyposoter exiguae. J. Insect. Physiol. 49:483-490.

  80. Stoltz, D.B., D. Guzo, E.R. Belland, C.J. Cucarotti & E.A. Mac-Kinnon. 1988. Venom promotes uncoating in vitro and persistence in vivo of DNA from a braconid polydnavirus. J. Gen. Virol. 69:903-907.

  81. Strand, M.R. 1994. Microplitis demolitor polydnavirus infects and expresses in specific morphotypes of Pseudoplusia includens haemocytes. J. Gen. Virol. 75:3007-3020.

  82. Strand, M.R. & B.A. Dover. 1991. Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the Rodríguez-Pérez et al Co-evolución de parasitoides y polidnavirus Rev Latinoam Microbiol 2006; 48 (1): 31-43 43 calyx fluid and venom of Microplitis demolitor. Arch. Insect. Biochem. Physiol. 18:131-145.

  83. Strand, M.R. & L.L. Pech 1995a. Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40:31-56.

  84. Strand, M.R. & L.L. Pech. 1995b. Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. J. Gen. Virol. 76:283-291.

  85. Strand, M.R., D.I. McKenque, V. Grassl, B.A. Dover & J.M. Aiken. 1992. Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens. J. Gen. Virol. 73:1627-1635.

  86. Strand, M.R., A. Witherell & D. Trudeau. 1997. Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. J. Virol. 71:2146-2156.

  87. Summers, M.D. & S.D. Dib-Hajj. 1995. Polydnavirus-facilitated endoparasite protection against host immune defenses. Proc. Natl. Acad. Sci. USA. 96:29-36.

  88. Tanaka K., S. Tsuzuki, H. Matsumoto & Y. Hayakawa. 2003. Expression of Cotesia kariyai polydnavirus genes in lepidopteran hemocytes and Sf9 cells. J. Insect. Physiol. 49:433-440.

  89. Theilmann, D.A. & M.D. Summers. 1986. Molecular analysis of Campoletis sonorensis virus DNA in the lepidopteran host Heliothis virescens. J. Gen. Virol. 67:1961-1969.

  90. Theilmann, D.A. & M.D. Summers. 1987. Physical analysis of the Campoletis sonorensis virus multipartite genome and identification of a family of tandemly repeated elements. J. Virol. 61:2589-2598.

  91. Turnbull, M.W. & B.A. Webb. 2002. Perspectives on polydnavirus origin and evolution. Adv. Virus Res. 58:203-254.

  92. Wago H. & T. Tanaka. 1989. Synergistic effects of calyx fluid and venom of Apanteles kariyai Watanabe (Hymenoptera:Braconidae) on the granular cells of Pseudaletia separata Walker (Lepidoptera:Noctuidae). Zoolog. Sci. 6:691-696.

  93. Washburn, J.O., B.A. Kirkpatrick & L.E. Volkman. 1996. Insect protection against viruses. Nature. 383:767.

  94. Washburn, J.O., E.J. Haas-Stapleton, F.F. Tan, N.E. Beckage & 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.

  95. Weaber R.J., G.C. Marris, H.A. Bell & J.P. Edwards. 2001. Identity and mode of action of the host endocrine disrupters from the venom of parasitoid wasps. In Endocrine Interactions of Insect Parasites and Pathogen. (Eds Edwards J.P.,

  96. Weaver R.J.), pp. 33-58. Bios Scientific Publisher, Ltd, Oxford, UK.

  97. Webb, B.A. 1998. Polydnavirus biology genome structure and evolution. En: A. Ball and L.K. Miller, Eds. The Insect Viruses. Plenum Press, New York. pp. 105-139.

  98. Webb, B.A. y S. Luckhart. 1994. Evidence for an early immunosuppressive role for related Campoletis sonorensis venom and ovarian proteins in Heliothis virescens. Arch. Insect. Biochem. Physiol. 26:147-163.

  99. Webb, B.A. & S. Luckhart. 1996. Factors mediating short- and long-term immune suppression in a parasitized insect. J. Insect. Physiol. 42:33-40.

  100. Webb, B.A. & M.D. Summers. 1990. Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proc. Natl. Acad. Sci. USA. 87:4961-4965.

  101. Whitfield, J.B. 1990. Parasitoids, polydnaviruses, and endosymbiosis. Parasitol. Today. 6:381-384.

  102. Whitfield, J.B. 1994. Mutualistic viruses and the evolution of host ranges in endoparasitoid Hymenoptera. En: B.A. Hawkins and W. Sheehan, Eds. Parasitoid Community Ecology, Oxford University Press, Oxford. pp. 163-176.

  103. Whitfield, J.B. & S. Asgari. 2003. Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J. Insect. Physiol. 49:397-405.

  104. Willott, E., T. Trenczek, L.W. Thrower & M.R. Kanost. 1994. Immunochemical identification of insect hemocyte populations: monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. Eur. J. Cell. Biol. 65:417-423.

  105. Wyder, S., F. Blank & B. Lanzrein. 2003. Fate of polydnavirus DNA of the egg-larval parasitoid Chelonus inanitus in the host Spodoptera littoralis. J. Insect. Physiol. 49:491-500.

  106. Yamanaka, A., Y. Hayakawa, H. Noda, N. Nakashima & H. Watanabe. 1996. Characterization of polydnavirus-encoded mRNA in parasitized armyworm larvae. Insect. Biochem. Mol. Biol. 6:529-536.

  107. Adamo, S.A., C.E. Linn & N. E. Beckage. 1997. Correlation between changes in host behavior and octopamine levels in the tobacco hornworm, Manduca sexta, parasitized by the gregarious braconid parasitoid wasp Cotesia congregata. J. Exp. Biol. 200:117-127.

  108. Asgari, S. & O. Schmidt. 1994. Passive protection of eggs from the parasitoid Cotesia rubecula in the host Pieris rapae. J. Insect. Physiol. 40:789-795.

  109. Asgari, S. & O. Schmidt. 2002. A coiled-coil region of an insect immune suppressor protein is involved in binding and uptake by hemocytes. Insect. Biochem. Mol. Biol. 32:497-504.

  110. Asgari S., M. Hellers & O. Schmidt. 1996. Host haemocyte inactivation by an insect parasitoid: transient expression of a polydnavirus gene. J. Gen. Virol. 77:2653-2662.

  111. Asgari, S., O. Schmidt & U. Theopold. 1997. A polydnavirusencoded protein of an endoparasitoid wasp is an immune suppressor. J. Gen. Virol. 78:3061-3070.

  112. Beckage, N.E. 1993. Games parasites play: the dynamic roles of peptides and proteins in the host-parasite interaction. En: N.E. Beckage, S.N. Thompson, and B.A. Federici, Eds. Parasites and Pathogens of Insects, Vol 1. Academic Press, N. Y. pp. 25-58.

  113. Beckage, N.E. & D.B. Gelman. 2004. Wasp parasitoid disruption of host development: Implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299-330.

  114. Beckage, N.E., J.S. Metcalf, D.J. Nesbit, K.W. Schliefer, S.R. Zetlan & I. de Buron. 1990. Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by a wasp polydnavirus. Insect. Biochem. 20:285-294.

  115. Beckage, N.E., F.F. Tan, K.W. Schleifer, R.D. Lane & L.L. Cherubin. 1994. Characterization and biological effects of Cotesia congregata polydnavirus on host larvae of the tobacco hornworm, Manduca sexta. Arch. Insect. Biochem. Physiol. 26:165-195.

  116. Beckage, N.E., T.J. Templeton, B.D. Nielsen, D.I. Cook & D.B. Stoltz. 1987. Parasitism-induced hemolymph polypeptides in Manduca sexta (L.) larvae parasitized by the braconid wasp Cotesia congregata (Say). Insect. Biochem. 17:439-455.

  117. Béliveau, C., A. Levasseur, D. Stoltz & M. Cusson. 2003. Three related TrIV genes: comparative sequence analysis and expression in host larvae and Cf-124T cells. J. Insect. Physiol. 49:501-512.

  118. Belle, E., N.E. Beckage, J. Rousselet, M. Poirie, F. Lemeunier & J.M. Drezen. 2002. Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J. Virol. 76:5793-96.

  119. Blissard, G.W., S.B. Vinson & M.D. Summers. 1986. Identification, mapping, and in vitro translation of Campoletis sonorensis virus mRNAs from parasitized Heliothis virescens larvae. J. Virol. 57:318-327.

  120. Bonvin, M., D. Marti, S. Wyder, D. Kojic, M. Annaheim, & B. Lanzrein. 2005. Cloning, characterization and analysis by RNA interference of various genes of the Chelonus inanitus polydnavirus. J. Gen. Virol. 86:973-983.

  121. Buron, de I. & N.E. Beckage. 1992. Characterization of a polydnavirus (PDV) and virus-like filamentous particle (VLFP) in the braconid wasp Cotesia congregata (Hymenoptera: Braconidae). J. Invertebr. Pathol. 59:315-327.

  122. Cui, L. & B.A. Webb. 1996. Isolation and characterization of a new member of the cysteine-rich Campoletis sonorensis polydnavirus gene family. J. Gen. Virol. 77:797-809.

  123. Cui L., Soldevila A. & Webb B.A. 1997. Expression and hemocyte- targeting of a Campoletis sonorensis polydnavirus cysteine-rich gene in Heliothis virescens larvae. Arch. Insect. Biochem. Physiol. 36:251-271.

  124. Cook, D.I., D.B. Stoltz & S.B. Vinson. 1984 Induction of a new haemolymph glycoprotein in larvae of permissive hosts parasitized by Campoletis sonorensis. Insect. Biochem. 14:45-50.

  125. Davies, D.H. & S.B. Vinson. 1986. Passive evasion by eggs of braconid parasitoid Cardiochles nigriceps of encapsulation in vitro by haemocytes of host Heliothis virescens: Possible role for fibrous layer in immunity. J. Insect. Physiol. 32:1003-1010.

  126. DeBorde, S., W. Rattanadechakul, Y. Kim, J.A. Kroemer, B.A. Webb, L. Thoetkiattial, A. Witherell and M.R. Strand. 2002. Characterization of the Microplitis demolitor bracovirus genome Memorias del 50th Annual Meeting of the Entomological Society of America. November 17-20, Fort Lauderdale, Florida. USA, D0032.

  127. Dib-Hajj, S.D., B.A. Webb & M.D. Summers. 1993. Structure and evolutionary implications of a “cysteine-rich” Campoletis sonorensis polydnavirus gene family. Proc. Natl. Acad. Sci. USA. 90: 3765-3769.

  128. Drezen, J.M., B. Provost, E. Espagne, L. Cattolico, C. Dupuy, M. Poirie, G. Periquet & E. Huguet. 2003. Polydnavirus genome: integrated vs free virus. J. Insect. Physiol. 49:407-417.

  129. Dushay, M.S. & N.E. Beckage. 1993. Dose-dependent separation of Cotesia congregata-associated polydnavirus effects on Manduca sexta larval development and immunity. J. Insect. Physiol. 39:1029-1040.

  130. Dumpit, R., M.A. Rodríguez-Pérez, M. Alleyne & N.E. Beckage. 2004. Cotesia flavipes and Manduca sexta: A model for studying parasitoid encapsulation in refractory hosts. Memorias del 52nd Annual Meeting of the Entomological Society of America. Noviembre 14-17, Salt Lake City, Utah. pág. 43.

  131. Edson, K.M., S.B. Vinson, D.B. Stoltz & M.D. Summers. 1981. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid’s host. Science. 211:582-583.

  132. Espagne, E., C. Dupuy, E. Huguet, L. Cattolico, B. Provost, N. Martins, M. Poirié, G. Periquet & J.M. Drezen. 2004. Genome sequence of a polydnavirus: Insights into symbiotic virus evolution. Science 306:286-289.

  133. Fedderson, I., K. Sander & O. Schmidt. 1986. Virus-like particles with host protein-like antigenic determinants protect an insect parasitoid from encapsulation. Experientia. 42:1278-1281.

  134. Federici, B.A. 1991. Viewing polydnaviruses as gene vectors of endoparasitic Hymenoptera. Redia 74:387-392.

  135. Federici, B.A. & Y. Bigot. 2003. Origin and evolution of polydnaviruses by symbiognesis of insect DNA viruses in endoparasitic wasps. J. Insect. Physiol. 49:419-432.

  136. Fleming, J.G.W. 1992. Polydnaviruses: mutalists and pathogens. Annu. Rev. Entomol. 37:401-425.

  137. Fleming, J.G.W. & P. Krell. 1993. Polydnavirus genome organization. En: N. E., Beckage, S.N. Thompson, and B.A. Federici, Eds. Parasites and Pathogens of Insects, Vol 1. Academic Press, NY. pp. 189-225.

  138. Fleming, J.G.W. & M.D. Summers. 1991. Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc. Natl. Acad. Sci. 88:9770-9774.

  139. Fleming, J.G.W., G.W. Blissard, M.D. Summers & S.B. Vinson. 1983. Expression of Campoletis sonorensis virus in the parasitized host, Heliothis virescens. J. Virol. 48:74-78.

  140. Galibert L., J. Rocher, M. Ravallec, M. Duonor-Cérutti, B.A. Webb & A.N. Volkoff. 2003. Two Hyposoter didmator ichnovirus genes expressed in the lepidopteran host encode secreted or membrane-associated serine and threonine rich proteins in segments that may be nested. J. Insect. Physiol. 49:441-452.

  141. Godfray, H.C.J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press.

  142. Gruber, A., P. Stettler, P. Heiniger, D. Schumperli & B. Lanzrein. 1996. Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp genome and excised only in later pupal and adult stages of the female. J. Gen. Virol. 77:2873-2879.

  143. Gundersen-Rindal D.E. & Lynn D.E. 2003. Polydnavirus integration in lepidopteran host cells in vitro. J. Insect. Physiol. 49:453-462.

  144. Guzo, D. & D.B. Stoltz. 1987. Observations on cellular immunity and parasitism in the tussock moth. J. Insect. Physiol. 33:19-31.

  145. Harwood, S.H. & N.E. Beckage. 1994 Purification and characterization of an early-expressed polydnavirus-induced protein from the hemolymph of Manduca sexta larvae parasitized by Cotesia congregata. Insect. Biochem. Mol. Biol. 24:685-698.

  146. Harwood, S.H., A.J. Grosovsky, E.A. Cowles, J.W. Davis & N.E. Beckage. 1994. An abundantly expressed hemolymph glycoproRodríguez-Pérez et al Co-evolución de parasitoides y polidnavirus Rev Latinoam Microbiol 2006; 48 (1): 31-43 42 tein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. Virology. 205:381-392.

  147. Hayakaya Y. 1995. Growth-blocking peptide: an insect biogenic peptides that prevents the onset of metamorphosis. J. Insect. Physiol. 44:1-6.

  148. Hayakaya Y, I. Yuazaki, A. Yamanaka & T. Tanaka. 1994. Expression of polydnavirus genes from the parasitoid wasp Cotesia kariyai in two noctuid hosts. Insect. Mol. Biol. 3:97-103.

  149. Hellers, M., M. Beck, U. Theopold, M. Kamei & O. Schmidt. 1996. Multiple alleles encoding a virus-like particle protein in the ichneumonid wasp endoparasitoid Venturia canescens. Insect. Mol. Biol. 5:239-249.

  150. Krell, P. J. 1991. The polydnaviruses: multipartite DNA viruses from parasitic Hymenoptera. In: Viruses of Invertebrates (Ed. Krustak E.) pp. 141-177. Marcel Dekker, New York.

  151. Krell, P.J. & D.B. Stoltz. 1980. Virus-like particles in the ovary of an ichneumonid wasp: purification and preliminary characterization. Virology. 101:408-418.

  152. Kroemer, J.A. & B.A. Webb. 2004. Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu. Rev. Entomol. 49:431-456.

  153. Lapointe, R., R. Wilson, L. Vilaplana, D.R. O’Reilly, P. Falabella, V. Douris, M. Bernier-Cardou, F. Pennacchio, K. Latrou, C. Malva & J.A. Olszewski. 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.

  154. Lavine, M.D. & N.E. Beckage. 1995. Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitol. Today. 11:368-378.

  155. Lavine, M.D. & N.E. Beckage. 1996. Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata. J. Insect. Physiol. 42:39-49.

  156. Lavine, M.D. & M.R. Strand. 2002. Insect hemocytes and their role in immunity. Insect. Biochem. Mol. Biol. 32:1295-1309.

  157. Le, N.T., S. Asgari, K. Amaya, F.F. Tan & N.E. Beckage. 2003. Persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm. J. Insect. Physiol. 49:533-543.

  158. Li, X. & B.A. Webb. 1994. Apparent functional role for a cysteine- rich polydnavirus protein in suppression of the insect cellular immune response. J. Virol. 68:7482-7489.

  159. Luckhart, S. & B.A. Webb. 1996. Interaction of a wasp ovarian protein and polydnavirus in host immune suppression. Dev. Comp. Immunol. 20:1-21.

  160. Noguchi, H., Y. Harakawa & R.G.H. Downer. 1995. Elevation of dopamine levels in parasitized insect larvae. Insect. Biochem. Mol. Biol. 25:197-201.

  161. Richards E.H. & J.P. Edwards. 2000. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 127:289-298.

  162. Rizki, R.M. & T.M. Rizki. 1984. Selective destruction of a host blood cell type by a parasitoid wasp. Proc. Natl. Acad. Sci. USA. 81:6154-6158.

  163. Rizki, R.M. & T.M. Rizki. 1990. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc. Natl. Acad. Sci. USA. 97: 8388-8392.

  164. Rodríguez-Pérez, M.A., R. Dumpit, M. Hongskula & N. Beckage. 2004. Physiological consequences of the encapsulation of the parasitoid Cotesia flavipes in host larvae of the tobacco hornworm Manduca sexta. Memorias del IX European Multicolloquium of Parasitology, Valencia, España, 18-23 Julio. pág. 637.

  165. Rodríguez-Pérez, M.A., R.F. Dumpit, J.M. Lenz, E.N. Powell, S.Y. Tam & N. Beckage. 2005. Host Refractoriness of the Tobacco Hornworm, Manduca sexta, to the Braconid Endoparasitoid Cotesia flavipes. Arch. Insect. Biochem. Physiol. 60:159-171.

  166. Ross, D.R. & P.E. Dunn. 1989. Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta to bacterial infection. Dev. Comp. Immunol. 13:205-216.

  167. Rotheram S. 1973. The surface of the egg of a parasitic insect. I. The surface of the egg and the first instar larva of Nemeritis. Proc. R. Soc. London Ser. B. 183: 179-194.

  168. Russo J., S. Dupas, F. Frey, Y. Carton & M. Brehelin. 1996. Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology. 112:135-142.

  169. Salt, G. 1965. Experimental studies in insect parasitism XIII. The haemocytic reaction of a caterpillar to eggs of its habitual parasite. Proc. R. Soc. London Ser. B. 162:303-318.

  170. Savary, S., N.E. Beckage, F. Tan, G. Periquet & J.M. Drezen. 1997. Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastrinae) at potential recombinase binding sites. J. Gen. Virol. 83:2035.

  171. Schmidt, O., U. Theopold & M.R. Strand. 2001. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays. 23:344-351.

  172. Shelby, K.S. & B.A. Webb. 1994. Polydnavirus infection inhibits synthesis of an insect plasma protein, arylphorin. J. Gen. Virol. 75:2285-2292.

  173. Shelby, K.S. & B.A. Webb. 1997. Polydnavirus infection inhibits translation of specific growth-associated host proteins. Insect. Biochem. Mol. Biol. 27:263-270.

  174. Shelby, K.S. & B.A. Webb. 1999. Polydnavirus-mediated suppression of insect immunity. J. Insect. Physiol. 45:507-514.

  175. Soldevila, A.I. & B.A. Webb. 1996. Expression of polydnavirus genes under polydnavirus-promoter regulation in insect larvae infected with baculovirus recombinants. J. Gen. Virol. 77:1379-1388.

  176. Soldevila, A.I., S. Heuston & B.A. Webb 1997. Purification and analysis of a polydnavirus gene product expressed using a poly-histidine baculovirus vector. Insect. Biochem. Mol. Biol. 27:201-211.

  177. Sroka, P. & S.B. Vinson. 1978. Phenyloxidase activity in the hemolyph of parasitized and unparasitized Heliothis virescens. Insect. Biochem. 8:399-402.

  178. Stoltz, D.B. 1993. The polydnavirus life cycle. In Parasites and Pathogens of Insects. (Eds Beckage N.E., Thompson S.N., and Federici B.A.), Vol 1, pp. 167-189. Academic Press, NY.

  179. Stoltz, D.B. & D. Cook. 1983. Inhibition of host phenoloxidase activity by parasitoid Hymenoptera. Experientia. 39:1022-1024.

  180. Stoltz, D.B. & D. Guzo. 1986. Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. J. Insect. Physiol. 32:377-388.

  181. Stoltz, D.B. & J.B. Whitfield. 1992. Viruses and virus-like entities in the parasitic Hymenoptera. J. Hymenopt. Res. 1:125-139.

  182. Stoltz, D.B. & A. Makkay. 2003. Overt viral diseases induced from apparent latency following parasitization by the ichneumonid wasp, Hyposoter exiguae. J. Insect. Physiol. 49:483-490.

  183. Stoltz, D.B., D. Guzo, E.R. Belland, C.J. Cucarotti & E.A. Mac-Kinnon. 1988. Venom promotes uncoating in vitro and persistence in vivo of DNA from a braconid polydnavirus. J. Gen. Virol. 69:903-907.

  184. Strand, M.R. 1994. Microplitis demolitor polydnavirus infects and expresses in specific morphotypes of Pseudoplusia includens haemocytes. J. Gen. Virol. 75:3007-3020.

  185. Strand, M.R. & B.A. Dover. 1991. Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the Rodríguez-Pérez et al Co-evolución de parasitoides y polidnavirus Rev Latinoam Microbiol 2006; 48 (1): 31-43 43 calyx fluid and venom of Microplitis demolitor. Arch. Insect. Biochem. Physiol. 18:131-145.

  186. Strand, M.R. & L.L. Pech 1995a. Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40:31-56.

  187. Strand, M.R. & L.L. Pech. 1995b. Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. J. Gen. Virol. 76:283-291.

  188. Strand, M.R., D.I. McKenque, V. Grassl, B.A. Dover & J.M. Aiken. 1992. Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens. J. Gen. Virol. 73:1627-1635.

  189. Strand, M.R., A. Witherell & D. Trudeau. 1997. Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. J. Virol. 71:2146-2156.

  190. Summers, M.D. & S.D. Dib-Hajj. 1995. Polydnavirus-facilitated endoparasite protection against host immune defenses. Proc. Natl. Acad. Sci. USA. 96:29-36.

  191. Tanaka K., S. Tsuzuki, H. Matsumoto & Y. Hayakawa. 2003. Expression of Cotesia kariyai polydnavirus genes in lepidopteran hemocytes and Sf9 cells. J. Insect. Physiol. 49:433-440.

  192. Theilmann, D.A. & M.D. Summers. 1986. Molecular analysis of Campoletis sonorensis virus DNA in the lepidopteran host Heliothis virescens. J. Gen. Virol. 67:1961-1969.

  193. Theilmann, D.A. & M.D. Summers. 1987. Physical analysis of the Campoletis sonorensis virus multipartite genome and identification of a family of tandemly repeated elements. J. Virol. 61:2589-2598.

  194. Turnbull, M.W. & B.A. Webb. 2002. Perspectives on polydnavirus origin and evolution. Adv. Virus Res. 58:203-254.

  195. Wago H. & T. Tanaka. 1989. Synergistic effects of calyx fluid and venom of Apanteles kariyai Watanabe (Hymenoptera:Braconidae) on the granular cells of Pseudaletia separata Walker (Lepidoptera:Noctuidae). Zoolog. Sci. 6:691-696.

  196. Washburn, J.O., B.A. Kirkpatrick & L.E. Volkman. 1996. Insect protection against viruses. Nature. 383:767.

  197. Washburn, J.O., E.J. Haas-Stapleton, F.F. Tan, N.E. Beckage & 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.

  198. Weaber R.J., G.C. Marris, H.A. Bell & J.P. Edwards. 2001. Identity and mode of action of the host endocrine disrupters from the venom of parasitoid wasps. In Endocrine Interactions of Insect Parasites and Pathogen. (Eds Edwards J.P., Weaver R.J.), pp. 33-58. Bios Scientific Publisher, Ltd, Oxford, UK.

  199. Webb, B.A. 1998. Polydnavirus biology genome structure and evolution. En: A. Ball and L.K. Miller, Eds. The Insect Viruses. Plenum Press, New York. pp. 105-139.

  200. Webb, B.A. y S. Luckhart. 1994. Evidence for an early immunosuppressive role for related Campoletis sonorensis venom and ovarian proteins in Heliothis virescens. Arch. Insect. Biochem. Physiol. 26:147-163.

  201. Webb, B.A. & S. Luckhart. 1996. Factors mediating short- and long-term immune suppression in a parasitized insect. J. Insect. Physiol. 42:33-40.

  202. Webb, B.A. & M.D. Summers. 1990. Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proc. Natl. Acad. Sci. USA. 87:4961-4965.

  203. Whitfield, J.B. 1990. Parasitoids, polydnaviruses, and endosymbiosis. Parasitol. Today. 6:381-384.

  204. Whitfield, J.B. 1994. Mutualistic viruses and the evolution of host ranges in endoparasitoid Hymenoptera. En: B.A. Hawkins and W. Sheehan, Eds. Parasitoid Community Ecology, Oxford University Press, Oxford. pp. 163-176.

  205. Whitfield, J.B. & S. Asgari. 2003. Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J. Insect. Physiol. 49:397-405.

  206. Willott, E., T. Trenczek, L.W. Thrower & M.R. Kanost. 1994. Immunochemical identification of insect hemocyte populations: monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. Eur. J. Cell. Biol. 65:417-423.

  207. Wyder, S., F. Blank & B. Lanzrein. 2003. Fate of polydnavirus DNA of the egg-larval parasitoid Chelonus inanitus in the host Spodoptera littoralis. J. Insect. Physiol. 49:491-500.

  208. Yamanaka, A., Y. Hayakawa, H. Noda, N. Nakashima & H. Watanabe. 1996. Characterization of polydnavirus-encoded mRNA in parasitized armyworm larvae. Insect. Biochem. Mol. Biol. 6:529-536.




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