Characterization and biological effects of cotesia congregata polydnavirus on host larvae of the tobacco hornworm, manduca sexta

The ovaries of endoparasitic species of braconid and ichneumonid wasps contain large numbers of polydnavirus (PDV) virions that replicate in specialized calyx cells of the ovaries and are injected into the host larva during parasitization. In the braconid wasp Cotesia congregata that parasitizes the tobacco hornworm, Manduca sexta, the total amount of viral DNA present in the ovaries was determined to be 25–75 ng. Analysis of viral DNA on 0.4% agarose gels showed that the genome was comprised of 15–20 circles of double-stranded DNA. SDS-PAGE analyses showed that a large number (>30) of structural polypeptides were present in the virions, and analysis of the venom likewise showed that multiple components were present. The major size classes of venom proteins differed from those present in the PDV. However, Western blots using polyclonal PDV antibodies showed that some cross-reacting PDV-like proteins were present in the venom, perhaps explaining the mild PDV-enhancing effect of the venom. Injection of PDV into unparasitized larvae provoked pronounced alterations in their growth, development, pigmentation, and hemolymph proteins. A densely staining band of hemolymph proteins of approximately 18–20 kD appeared in large amounts relative to other hemolymph proteins several days following injection of PDV; this band was undetectable in naturally parasitized larvae. Eggs which had been washed extensively to remove PDVs were encapsulated following injection, but development of the host still was disrupted, usually in the post-wandering prepupal stage. Thus, neither the parasites nor their host survived, despite mobilization of an “effective” host response.© 1994 WiIey-Liss, Inc.

[1]  N. Beckage,et al.  Purification and characterization of an early-expressed polydnavirus-induced protein from the hemolymph of Manduca sexta larvae parasitized by Cotesia congregata , 1994 .

[2]  M. Dushay,et al.  Dose-dependent separation of Cotesia congregata-associated polydnavirus effects on Manduca sexta larval development and immunity , 1993 .

[3]  M. Kanost,et al.  Effects of parasitism by the braconid wasp Cotesia congregata on host hemolymph proteins of the tobacco hornworm, Manduca sexta. , 1993, Insect biochemistry and molecular biology.

[4]  S. Dib-Hajj,et al.  Structure and evolutionary implications of a "cysteine-rich" Campoletis sonorensis polydnavirus gene family. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[5]  I. Buron,et al.  Lack of Prothoracic Gland Degeneration in Developmentally Arrested Host Larvae of Manduca sexta Parasitized by the Braconid Wasp Cotesia congregata , 1993 .

[6]  D. Jones,et al.  Chapter 10 – Venoms of Parasitic Hymenoptera as Investigatory Tools , 1993 .

[7]  D. Stoltz.  Chapter 8 – The Polydnavirus Life Cycle , 1993 .

[8]  N. Beckage.  Chapter 2 – Games Parasites Play: The Dynamic Roles of Proteins and Peptides in the Relationship between Parasite and Host , 1993 .

[9]  B. Lanzrein,et al.  Chapter 3 – Hormonal Interactions between Insect Endoparasites and Their Host Insects , 1993 .

[10]  J. Aiken,et al.  Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens. , 1992, The Journal of general virology.

[11]  I. Buron,et al.  Characterization of a polydnavirus (PDV) and virus-like filamentous particle (VLFP) in the braconid wasp Cotesia congregata (Hymenoptera: Braconidae) , 1992 .

[12]  J. A. Fleming.  Polydnaviruses: mutualists and pathogens. , 1992, Annual review of entomology.

[13]  M. Summers,et al.  Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Soldevila,et al.  Immunoanalysis of unique protein in Trichoplusia ni larvae parasitized by the braconid wasp Chelonus near curvimaculatus , 1991 .

[15]  M. Strand,et al.  Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor , 1991 .

[16]  M. Strand,et al.  Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the calyx fluid and venom of Microplitis demolitor. , 1991, Archives of insect biochemistry and physiology.

[17]  J. W. Smith,et al.  Inheritance of the White Larval Trait in a Laboratory Colony of Manduca sexta (L.) , 1990 .

[18]  Toshiharu Tanaka,et al.  Synergistic effect of venom, calyx and teratocytes of Apanteles kariyai on the inhibition of larval pupal ecdysis of the host, Pseudaletia separata , 1990 .

[19]  M. Summers,et al.  Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W. J. Lewis,et al.  Comparative virogenesis of filamentous virus and polydnavirus in the female reproductive tract of Cotesia marginibentris (Hymenoptera: Braconidae) , 1990 .

[21]  S. Vinson.  How parasitoids deal with the immune system of their host: An overview , 1990 .

[22]  P. Lawrence.  Serosal cells of biosteres longicaudatus (Hymenoptera: Braconidae): ultrastructure and release of polypeptides , 1990 .

[23]  I. Buron,et al.  Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by wasp polydnavirus , 1990 .

[24]  J. H. Law,et al.  Insect Haemolymph Proteins , 1990 .

[25]  L. Riddiford,et al.  Developmental expression, synthesis, and secretion of insecticyanin by the epidermis of the tobacco hornworm, Manduca sexta. , 1990, Archives of insect biochemistry and physiology.

[26]  N. Beckage,et al.  Alteration of hemolymph polypeptides in Manduca sexta larvae parasitized by Cotesia congregata: A two-dimensional electrophoretic analysis and comparison with major bacteria-induced proteins , 1989 .

[27]  D. Theilmann,et al.  Identification and comparison of Campoletis sonorensis virus transcripts expressed from four genomic segments in the insect hosts Campoletis sonorensis and Heliothis virescens. , 1988, Virology.

[28]  D. Stoltz,et al.  Venom Promotes Uncoating in vitro and Persistence in vivo of DNA from a Braconid Polydnavirus , 1988 .

[29]  D. Davies,et al.  Degeneration of last instar Heliothis virescens prothoracic glands by Campoletis sonorensis polydnavirus , 1988 .

[30]  D. Davies,et al.  Dose-dependent influence of Campoletis sonorensis polydnavirus on the development and ecdysteroid titers of last-instar Heliothis virescens larvae , 1988 .

[31]  E. Harlow,et al.  Antibodies: A Laboratory Manual , 1988 .

[32]  H. Schägger,et al.  Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. , 1987, Analytical biochemistry.

[33]  P. Matsudaira,et al.  Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. , 1987, The Journal of biological chemistry.

[34]  Toshiharu Tanaka.  Calyx and Venom Fluids of Apanteles kariyai (Hymenoptera: Braconidae) as Factors that Prolong Larval Period of the Host, Pseudaletia separata (Lepidoptera: Noctuidae) , 1987 .

[35]  S. L. Berger.  [6] Quantifying 32P-labeled and unlabeled nucleic acids , 1987 .

[36]  D. Cook,et al.  Parasitism-induced hemolymph polypeptides in Manduca sexta (L.) larvae parasitized by the braconid wasp Cotesia congregata (Say) , 1987 .

[37]  Toshiharu Tanaka.  Effect of the venom of the endoparasitoid, Apanteles kariyai Watanabe, on the cellular defence reaction of the host, Pseudaletia separata Walker , 1987 .

[38]  L. Riddiford,et al.  Larval cuticular morphogenesis in the tobacco hornworm, Manduca sexta, and its hormonal regulation. , 1986, Developmental biology.

[39]  H. Kitano.  The role of Apanteles glomeratus venom in the defensive response of its host, Pieris rapae crucivora , 1986 .

[40]  Grace Jones,et al.  Pseudoparasitism of host Trichoplusia ni by Chelonus spp. as a new model system for parasite regulation of host physiology , 1986 .

[41]  T. J. Templeton,et al.  Physiological effects of parasitism by Apanteles congregatus in terminalstage tobacco hornworm larvae , 1986 .

[42]  J. Truman,et al.  The physiology of wandering behaviour in Manduca sexta. II. The endocrine control of wandering behaviour. , 1985, The Journal of experimental biology.

[43]  N. Beckage.  Endocrine Interactions Between Endoparasitic Insects and Their Hosts , 1985 .

[44]  L. Riddiford,et al.  Growth and development of the endoparasitic wasp Apanteles congregatus: dependence on host nutritional status and parasite load , 1983 .

[45]  H. Kitano.  Effect of the venom of the gregarious parasitoid Apanteles glomeratus on its hemocytic encapsulation by the host, Pieris , 1982 .

[46]  L. Riddiford,et al.  Effects of parasitism by Apanteles congregatus on the endocrine physiology of the tobacco hornworm Manduca sexta. , 1982, General and comparative endocrinology.

[47]  P. Krell,et al.  Virus-like particles in the ovary of an ichneumonid wasp: Purification and preliminary characterization. , 1980, Virology.

[48]  S. Vinson,et al.  A COMPARATIVE MORPHOLOGY OF THE VENOM APPARATUS OF FEMALE BRACONIDS (HYMENOPTERA: BRACONIDAE) , 1979, The Canadian Entomologist.

[49]  L. Riddiford,et al.  DEVELOPMENTAL INTERACTIONS BETWEEN THE TOBACCO HORNWORM MANDUCA SEXTA AND ITS BRACONID PARASITE APANTELES CONGREGATUS 1 , 1978 .

[50]  R. A. Bell,et al.  Techniques for Rearing Laboratory Colonies of Tobacco Hornworms and Pink Bollworms , 1976 .

[51]  G. Coles.  Studies on the hormonal control of metabolism in Rhodnius prolixus Stål. II. The fifth-stage insect. , 1966, Journal of insect physiology.