Inhibition of baculoviral disease by plant-mediated peroxidase activity and free radical generation

Journal of Chemical Ecology

Volumn 24, Issue 12, 1998, Pages 1949-2001

  Hoover, Kelli ^a,b   Kishida, Kenneth T ^a   Digiorgio, Louis A ^a   Workman, Jeff ^a   Alaniz, Susan A ^a   Hammock, Bruce D ^a   Duffey, Sean S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Baculovims; Clastogenesis; Free radicals; Nucleopolyhedrovims; Peroxidase; Phenolic redox cycling; Polyphenol oxidase

Indexed keywords

BACULOVIRUS; CLASTOGENESIS; COTTON; ENZYME ACTIVITY; FREE RADICAL; HELICOVERPA ZEA; HELIOTHIS VIRESCENS; LETTUCE; METHEMOGLOBIN; PEROXIDASE; PHENOLASE; PHYTOCHEMICAL; TOMATO; VIRUS INFECTION; VIRUS INHIBITION;

ANTIOXIDANT; FREE RADICAL; HYDROGEN PEROXIDE; METHEMOGLOBIN; MONOPHENOL MONOOXYGENASE; OXIDIZING AGENT; PEROXIDASE; PHENOL;

AGRICULTURE; ARTICLE; BACULOVIRUS; CHEMICAL INTERACTION; ENZYME ACTIVITY; LETTUCE; NONHUMAN; OXIDATION REDUCTION REACTION; PHYTOCHEMISTRY; PLANT; POLYHEDROSIS VIRUS; RESPIRATORY BURST; TOMATO; VIRUS INFECTION;

ANIMALIA; CYPOVIRUS; GOSSYPIUM HIRSUTUM; HELICOVERPA ZEA; HELIOTHIS VIRESCENS; LACTUCA; LYCOPERSICON ESCULENTUM; NOCTUIDAE; UNIDENTIFIED BACULOVIRUS; ZEA;

EID: 0032427508     PISSN: 00980331     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020777407980     Document Type: Article

References (85)

1. AHMAD, S. 1995. Oxidative Stress and Antioxidant Defenses in Biology. Chapman & Hall, New York.
2. AHMAD, S., DUVAL, D. L., WEINHOLD, L. C., and PARDINI, R. S. 1991. Cabbage looper antioxidant enzymes: Tissue specificity. Insect Biochem. 21:563-572.
3. ANASNTHASWAMY, H. N., and EISENSTARK, A. 1976. Near UV-induced breaks in phage DNA: Sensitization by hydrogen peroxide (a tryptophane photo-produce). Photochem. Photobiol. 24:439-442.
4. APPEL, H. M., and MAINES, L. W. 1995. The influence of host plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. J. Insect Physiol. 41:241-246.
5. AYERS, M. D., HOWARD, S. C., KUZIO, J., LOPEZFERBER, M., and POSSEE, R. D. 1994. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586-605.
6. BARBEHENN, R. V., and MARTIN, M. M. 1995. Tannin sensitivity in larvae of Malacosoma disstria (Lepidoptera): Roles of the peritrophic envelope and midgut oxidation. J. Chem. Ecol. 20:1985-2001.
7. BERENBAUM, M. 1983. Effect of tannins on growth and digestion in two species of papilionids. Entomol. Exp. Appl. 34:245-250.
8. BERNAYS, E. A., CHAMBERLAIN, D. J., and MCCARTHY, P. 1980. The differential effects of ingested tannic acid on different species of Acridoidea. Entomol. Exp. Appl. 28:158-166.
9. BI, J. L., and FELTON, G. W. 1995. Foliar oxidative stress and insect herbivory. Primary compounds, secondary metabolites, and reactive oxygen species as components of oxidative stress. J. Chem. Ecol. 21:1511-1530.
10. BI, J. L., MURPHY, J. B., and FELTON, G. W. 1997. Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J. Chem. Ecol. 23:97-117.
11. BROADWAY, R., DUFFEY, S. S., PEARCE, G., and RYAN, C. A. 1986. Plant proteinase inhibitors: A defense against herbivorous insects. Entomol. Exp. Appl. 41:33-38.
12. BUETTNER, G. R., and JURKIEWICS, B. A. 1993. Ascorbate free radical as a marker of oxidative stress: An EPR study. Free Radic. Biol. Med. 14:49-55.
13. BUTT, V. S. 1981. Direct oxidases and related enzymes, pp. 81-123, in P. K. Stumpf and E. E. Conn (eds.). The Biochemistry of Plants: A Comprehensive Treatise. Academic Press, New York.
14. BUTT, V. S., and LAMB, J. C. 1981. Oxygenases and the metabolism of plant products, pp. 627-655, in P. K. Stumpf and E. E. Conn (eds.). The Biochemistry of Plants: A Comprehensive Treatise. Secondary Plant Products. Academic Press, New York.
15. COLLETT, D. 1994. Modelling Survival Data in Medical Research. Chapman & Hall, London.
16. CRAWFORD, R. M. M., LINDSAY, D. A., WALTON, J. C., and WOLLENWEBER-RATZER, B. 1994. Towards the characterization of radicals formed in rhizomes of Iris germanica. Phytochemistry 37:979-985.
17. DUFFEY, S. S., and STOUT, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3-37.
18. DUFFEY, S. S., HOOVER, K., BONNING, B. C., and HAMMOCK, B. D. 1995. The impact of host-plant on the efficacy of baculoviruses, pp. 137-275, in M. Roe and R. Kuhr (eds.) Reviews in Pesticide Toxicology. CTI Toxicology Communications, Raleigh, North Carolina.
19. ELSTNER, E. F. 1987. Metabolism of activated oxygen species, pp. 253-315, in D. D. Davies (ed.). Biochemistry and Metabolism, The Biochemistry of Plants: A Comprehensive Treatise. Academic Press, New York.
20. ENGELHARD, E. K., and VOLKMAN, L. E. 1995. Developmental resistance within fourth instar Trichoplusia ni orally incoulated with Autographa californica M nuclear polyhedrosis virus. Virology 209:384-389.
21. ENGLARD, S., and SEIFTER, S. 1986. The biochemical functions of ascorbic acid. Annu. Rev. Nutri. 6:364-406.
22. FARRAR, R. R., JR., MARTIN, P. A. W., and RIDGWAY, R. L. 1996. Host plant effects on activity of Bacillus thuringiensis against gypsy moth (Lepidoptera: Lymantriidae) larvae. Environ. Entomol. 25:1215-1223.
23. FAZAL, F., RAHMAN, A., GREENSILL, J., AINLEY, K., HADI, S. M., and PARISH, J. H. 1990. Strand scission in DNA by quercetin and Cu(II): Identification of free radical intermediates and the biological consequences of scission. Carcinogensis 11:2005-2008.
24. FELTON, G. W. 1995. Oxidative stress of vertebrates and invertebrates, pp. 356-434, in S. Ahmad (ed.). Oxidative Stress and Antioxidant Defenses in Biology. Chapman & Hall, New York.
25. FELTON, G. W., and DUFFEY, S. S. 1990. Inactivation of a baculovirus by quinones formed in insect-damaged plant tissue. J. Chem. Ecol. 16:1211-1236.
26. FELTON, G. W., and DUFFEY, S. S. 1991. Reassessment of the role of gut alkalinity and detergency in insect herbivory. J. Chem. Ecol. 17:1821-1836.
27. FELTON, G. W., and SUMMERS, C. B. 1995. Antioxidant systems in insects. Arch. Insect Biochem. Physiol. 29:187-197.
28. FELTON, G. W., DUFFEY, S. S., VAIL, P. V., KAYA, H. K., and MANNING, J. 1987. Interaction of nuclear polyhedrosis virus with catechols: Potential incompatibility for host-plant resistance against noctuid larvae. J. Chem. Ecol. 13:947-957.
29. FELTON, G. W., DONATO, K., DEL VECCHIO, R. J., and DUFFEY, S. S. 1989. Activation of plant foliar oxidases by insect feeding reduces the nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667-2694.
30. FORSCHLER, B. T., YOUNG, S. Y., and FELTON, G. W. 1992. Diet and the susceptibility of Helicoverpa zea (Noctuidae: Lepidoptera) to a nuclear polyhedrosis virus. Environ. Entomol. 21:1220-1223.
31. FREI, B., ENGLAND, L., and AMES, B. N. 1989. Ascorbate is an outstanding antioxidant in human blood plasma. Proc. Natl. Acad. Sci. U.S.A. 86:6377-6381.
32. GARNER, C. W. 1984. Peroxidation of free and esterified fatty acids by horseradish peroxidase. Lipids 19:863-868.
33. GENTILE, I. A., FERRARIS, L., and MATTA, A. 1988. Variations of polyphenoloxidase activities as a consequence of stresses that induce resistance to Fusarium wilt of tomato. J. Phytopathol. 122:45-53.
34. HABER, F., and WEISS, J. 1934. The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. London Ser. A 147:332-351.
35. HALLIWELL, B. 1978. Lignin synthesis: The generation of hydrogen peroxide and superoxide by horseradish peroxidase and its stimulation by manganese(II) and phenols. Planta 140:81-88.
36. HALLIWELL, B., and GUTTERIDGE, J. M. C. 1990. The antioxidants of human extracellular fluids. Arch. Biochem. Biophys. 280:1-8.
37. HASSON, C., and SUGUMARAN, M. 1987. Protein cross-linking by peroxidase: Possible mechanism for sclerotization of insect cuticle. Arch. Insect Biochem. Physiol. 5:13-28.
38. HAYASHIYA, K., NISHIDA, J., and MATSUBARA, F. 1968. Inactivation of nuclear polyhedrosis virus in the digestive juice of silkworm larvae, Bombyx mori L. I. Comparison of anti-viral activities in the digestive juice of larvae reared on natural and artificial diets. Jpn. J, Entomol. Zool. 12:189-193.
39. HEDIN, P. A., JENKINS, J. N., and PARROTT, W. L. 1992. Evaluation of flavonoids in Gossypium arboreum (L.) cottons as potential source of resistance to tobacco budworm. J. Chem. Ecol. 18:105-114.
40. HOOVER, K., SCHULTZ, C. M., LANE, S. S., BONNING, B. C., MCCUTCHEN, B. F., DUFFEY, S. S., and HAMMOCK, B. D. 1995. Reduction in damage to cotton plants by a recombinant baculovirus that knocks moribund larvae of Heliothis virescens off the plant. Biol. Control 5:419-426.
41. HOOVER, K., YEE, J. L., SCHULTZ., C. M., ROCKE, D. M., HAMMOCK, B. D., and DUFFEY, S. S. 1998a. Effects of plant identity and chemical constituents on the efficacy of a baculovirus against Heliothis virescens. J. Chem. Ecol. 24:221-252.
42. HOOVER, K., STOUT, M. J., ALANIZ, S. A., HAMMOCK, B. D., and DUFFEY, S. S. 1998b. Influence of induced plant defenses in cotton and tomato on the efficacy of baculoviruses on noctuid larvae. J. Chem. Ecol. 24:253-271.
43. HUANG, M.-T., and FERRARO, T. 1992. Phenolic compounds in food and cancer prevention, pp. 8-34, in M.-T. Huang, C.-T. Ho and C. Y. Lee (eds.). Phenolic Compounds in Food and Their Effects on Health II: Antioxidants and Cancer Prevention. ACS Symposium Series 507. American Chemical Society, Washington, D.C.
44. HUANG, M.-T., HO., C.-T., and LEE, C. Y. 1992. Phenolic Compounds in Food and Their Effects on Health II: Antioxidants and Cancer Prevention. American Chemical Society, Washington, D.C., 402 pp.
45. HUNTER, M. D., and SCHULTZ, J. C. 1993. Induced plant defenses breached? Phytochemical induction protects an herbivore from disease. Oecologia 94:195-203.
46. IGNOFFO, C. M., and GARCIA, C. 1978. UV-photoactivation of cells and spores of Bacillus thuringiensis and effects of peroxidase on inactivation. Environ. Entomol. 7:270-272.
47. IGNOFFO, C. M., and GARCIA, C. 1994. Antioxidant and oxidative effects of the inactivation of inclusion bodies of Heliothis baculovirus by simulated sunlight-UV. Environ. Entomol. 23:1025-1029.
48. ISMAN, M. B., and DUFFEY, S. S. 1982a. Toxicity of tomato phenolic compounds to the fruitworm, Heliothis zea. Entomol. Exp. Appl. 31:370-376.
49. ISMAN, M. B., and DUFFEY, S. S. 1982b. Phenolic compounds in the foliage of commercial tomato cultivars as growth inhibitors to the fruitworm, Heliothis zea. J. Am. Hortic. Sci. 107:167-170.
50. JOHNSON, K. S., and FELTON, G. W. 1996. Physiological and dietary influences on midgut redox conditions in generalist lepidopteran larvae. J. Insect Physiol. 42:191-198.
51. KALBFLEISCH, J. D., and PRENTICE, R. L. 1980. The Statistical Analysis of Failure Time Data. Wiley, New York.
52. KEATING, S. T., and YENDOL, W. G. 1987. Influence of selected host plants on gypsy moth (Lepidoptera: Lymantriidae) larval mortality caused by a baculovirus. Environ. Entomol. 16:459-462.
53. KEATING, S. T., MCCARTHY, W. J., and YENDOL, W. G. 1989. Gypsy moth (Lymantria dispar) larval susceptibility to a baculovirus affected by selected nutrients, hydrogen ions (pH), and plant allelochemicals in artificial diets. J. Invertebr. Pathol. 54:165-174.
54. KEATING, S. T., HUNTER, M. D., and SCHULTZ, J. C. 1990. Leaf phenolic inhibition of gypsy moth nuclear polyhedrosis virus. Role of polyhedral inclusion body aggregation. J. Chem. Ecol. 16:1445-1457.
55. KOPPENOL, W. H., and BUTLER, J. 1985. Energetics of interconversion reactions of oxygen radicals. Adv. Free Rad. Biol. Med. 1:91-132.
56. LARSON, R. A. 1988. The antioxidants of higher plants. Phytochemistry 27:969-978.
57. LARSON, R. A. 1995. Antioxidant mechanisms of secondary natural products, pp. 210-237, in S. Ahmad (ed.). Oxidative Stress and Antioxidant Defenses in Biology. Chapman & Hall, New York.
58. MAYER, A. M. 1987. Polyphenol oxidases in plants-recent progress. Phytochemistry 26:11-20.
59. NORDSTROM, D. K. 1977. Thermochemical redox equilibria of ZoBell's solution. Geochim. Cosmochem. Acta 41:1835-1841.
60. NORTH, J. A., REIN, D., and TAPPEL, A. L. 1996. Multicomponent analysis of heme protein spectra in biological materials. Anal. Biochem. 233:115-123.
61. PIERPOINT, W. S. 1983. Reactions of phenolic compounds with proteins, and their relevance to the production of leaf protein, pp. 235-267, in L. Telek and H. D. Graham (eds.). Leaf Protein Concentrates. Avi Publ., Westport, Connecticut.
62. PITZER, R., and BABOCK, L. 1977. Mechanism of the complexation of boron acids with catechol and substituted catechols. Inorg. Chem. 16:1677-1681.
63. PUPPO, A. 1992. Effects of flavonoids on hydroxyl radical formation by Fenton-type reactions: Influence of the iron chelator. Phytochemistry 31:85-88.
64. RYAN, J. D., GREGORY, P., and TINGEY, W. M. 1982. Phenolic oxidase activities in glandular trichomes of Solanum berthaultii. Phytochemistry 21(8): 1185-1187.
65. SATO, M., RAMARATHNAM, N., SUZUKI, Y., OHKUBO, T., TAKEUCHI, M., and OCHI, H. 1996. Varietal differences in the phenolic content and Superoxide radical scavenging potential of wines from different sources. J. Agric. Food Chem. 44:37-41.
66. SCHULTZ, J. C., and KEATING, S. T. 1991. Host-plant-mediated interactions between the gypsy moth and a baculovirus, pp. 489-530, in Microbial Mediation of Plant-Herbivore Interactions. John Wiley & Sons, New York.
67. SHARPLES, G. C. 1964. Poly phenol content of head lettuce. Proc. Am. Soc. Hortic. Sci. 84:356-363.
68. SINGLETON, V. L. 1987. Oxygen with phenols and related reactions in musts, wines, and model systems: Observations and practical implications. Am. J. Enol. Vitic. 38:69-77.
69. SINGLETON, V. L., and ROSSI, J. A., JR. 1965. Colorimetry of total phenolics with phosphomolybdicphosphotungstic acid reagents. Am. J. Enol. Vitic. 16:144-158.
70. SOSA-GOMEZ, D. R., ALVES, S. B., and MARCHINI, L. C. 1991. Variation in the susceptibility of Bombyx mori L. to nuclear polyhedrosis virus when reared on different mulberry genotypes. J. Appl. Entomol. 111:318-320.
71. SPENCER, K. C. 1988. Chemical mediation of coevolution in the Passiflora-Heliconius interaction, pp. 167-240, in K. C. Spencer, (ed.). Chemical Mediation of Coevolution. Academic Press, San Diego.
72. STEEL, R. G. D., and Torrie, J. H. 1980. Principles and Procedures of Statistics: A Biometrical Approach, 2nd ed. McGraw-Hill, New York, 633 p.
73. STEINLY, B. A., and BERENBAUM, M. 1985. Histopathological effects of tannins on the midgut epithelium of Papilio polyxenes and Papilio glaucus. Entomol. Exp. Appl. 39:3-9.
74. STOUT, M. J., WORKMAN, K. V., and DUFFEY, S. S. 1994. Differential induction of tomato foliar proteins by arthropod herbivores. J. Chem. Ecol. 20:2575-2594.
75. SUMMERS, C. B., and FELTON, G. W. 1994. Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuidae): Potential mode of action for phenolic compounds in plant antiherbivore chemistry. Insect Biochem. Mol. Biol. 24:943-953.
76. SUMMERS, C. B., and FELTON, G. W. 1996. Peritrophic envelope as a functional antioxidant. Arch. Insect. Biochem. Physiol. 32:131-142.
77. SUTHERLAND, M. W. 1991. The generation of oxygen radicals during host plant responses to infection. Physiol. Mol. Plant Pathol. 39:79-93.
78. TOREL, J., CILLARD, J., and CILLARD, P. 1986. Antioxidant activity of flavonoids and reactivity with peroxy radical. Phytochemistry 25:383-385.
79. VLAK, J. M., and ROHRMANN, G. F. 1985. The nature of polyhedrin, pp. 489-542, in K. Maraorosch and K. E. Sherman (eds.). Viral Insecticides for Biological Control. Academic Press, Orlando, Florida.
80. WAISS, A. C., CHAN, B. G., ELLIGER, C. A., DRYER, D. L., BINDER, R. G., and GULEDNER, R. C. 1981. Insect growth inhibitors in crop plants. Entomol. Soc. Am. Bull. 27:217-221.
81. WASHBURN, J. O., KIRKPATRICK, B. A., HAAS-STAPLETON, E., and VOLKMAN, L. E. 1998. Evidence that the stilbene-derived optical brightener M2R enhances Autographa californica M nucleopolyhedrovirus infection of Trichoplusia ni and Heliothis virescens by preventing sloughing of infected midgut epithelial cells. Biol. Control 11:58-69.
82. WHITT, M. A., and MANNING, J. S. 1987. Role of chelating agents, monovalent anion and cation in the dissociation of Autographa californica nuclear polyhedrosis virus occlusion body. J. Invertebr. Pathol. 49:61-69.
83. WHITT, M. A., and MANNING, J. S. 1988. Stabilization of the Autographa californica nuclear polyhedrosis virus occlusion body matrix by zinc chloride. J. Invert. Pathol. 51:278-280.
84. WOLFSON, J. L., and MURDOCK, L. L. 1987. Method for applying chemicals to leaf surfaces for bioassay with herbivorous insects. J. Econ. Entomol. 80:1334-1336.
85. YOUNG, S. Y., YANG, J. G., and FELTON, G. W. 1995. Inhibitory effects of dietary tannins on the infectivity of a nuclear polyhedrosis virus to Helicoverpa zea (Noctuidae: Lepidoptera). Biol. Control 5:145-150.