Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in Northern Red Oak (Quercus rubra L.)

Journal of Chemical Ecology

Volumn 30, Issue 7, 2004, Pages 1363-1379

  Allison, Steven D ^a   Schultz, Jack C ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

galls; gypsy moth; isozyme; jasmonic acid; Peroxidase; PR protein; Quercus rubra; salicylic acid; wounding

Indexed keywords

ISOENZYME; JASMONIC ACID; PEROXIDASE; PHYTOHORMONE; SALICYLIC ACID;

ENZYME ACTIVITY; GALL; HORMONE; MOTH; WOUNDING;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXPOSURE; FLY; GREENHOUSE; GYPSY MOTH; HYMENOPTERA; INSECT; MEASUREMENT; NONHUMAN; OAK; PLANT DISEASE; PLANT LEAF; QUERCUS RUBRA; SEEDLING; SPECTROPHOTOMETRY;

ANIMALS; CYCLOPENTANES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ISOENZYMES; LARVA; MOTHS; PEROXIDASE; PLANT GROWTH REGULATORS; PLANT LEAVES; QUERCUS; SALICYLIC ACID; SEEDLING;

DIPTERA; HEXAPODA; HYMENOPTERA; INSECTA; LEPIDOPTERA; LYMANTRIA DISPAR; LYMANTRIIDAE; QUERCUS; QUERCUS RUBRA;

EID: 4444311116     PISSN: 00980331     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:JOEC.0000037745.66972.3e     Document Type: Article

References (73)

1. APPEL, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19:1521-1552.
2. ARNASON, J. T., BAUM, B., GALE, J., LAMBERT, J. D. H., BERGVINSON, D., and PHILOGENE, B. J. R. 1994. Variation in resistance of Mexican land races of maize to maize weevil Sitophilus zeamais, in relation to taxonomic and biochemical parameters. Euphytica 74:227-236.
3. BASHAN, Y., OKON, Y., and HENIS, Y. 1987. Peroxidase, polyphenol oxidase, and phenols in relation to resistance against Pseudomonas syringae pv. tomato in tomato plants. Can. J. Bot. 65:366-372.
4. 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 induced resistance. J. Chem. Ecol. 21:1511-1530.
5. 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.
6. BILES, C. L. and MARTYN, R. D. 1993. Peroxidase, polyphenoloxidase, and shikimate dehydrogenase isozymes in relation to tissue type, maturity and pathogen induction of watermelon seedlings. Plant Physiol. Biochem. 31:499-506.
7. BIRECKA, H. and MILLER, A. 1974. Cell wall and protoplast isoperoxidases in relation to injury, indoleacetic acid, and ethylene effects. Plant Physiol. 53:569-574.
8. BOSTOCK, R. 1999. Signal conflicts and synergies in induced resistance to multiple attackers. Physiol. Mol. Plant Path. 55:99-109.
9. BOSTOCK, R. M. and STERMER, B. A. 1989. Perspectives on wound healing in resistance to pathogens. Annu. Rev. Phytopath. 27:343-371.
10. BRONNER, R., WESTPHAL, E., and DREGER, F. 1991. Enhanced peroxidase activity associated with the hypersensitive response of Solanum dulcamara to the gall mite Aceria cladophthirus (Acari: Eriophyoidea). Can. J. Bot. 69:2192-2196.
11. BUZI, A., CHILOSI, G., DE SILLO, D., and MAGRO, P. 2004. Induction of resistance in melon to Didymella bryoniae and Sclerotinia sclerotiorum by seed treatments with acibenzolar-S-methyl and methyl jasmonate but not with salicylic acid. J. Phytopathol. 152:34-42.
12. CALDERÓN, A. A., ANGELES PEDREÑO, M., ROS-BARCELÓ, A., and MUÑOZ, R. 1990. Zymographic screening of plant peroxidase isoenzymes oxidizing 4-hydroxystilbenes. Electrophoresis 11:507-508.
13. CHOI, D., BOSTOCK, R. M., AVDIUSHKO, S., and HILDEBRAND, D. F. 1994. Lipid-derived signals that discriminate wound- and pathogen-response isoprenoid pathways in plants: Methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc. Natl. Acad. Sci., U.S.A. 91:2329-2333.
14. CIPOLLINI, D. F. and REDMAN, A. M. 1999. Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J. Chem. Ecol. 25:271-280.
15. CONTI, G. G., PIANEZZOLA, A., ARNOLDI, A., VIOLINI, G., and MAFFI, D. 1996. Possible involvement of salicylic acid in systemic acquired resistance of Cucumis sativus against Sphaerotheca fuliginea. Eur. J. Plant Path. 102:537-544.
16. DÍAZ, J. and MERINO, F. 1998. Wound-induced shikimate dehydrogenase and peroxidase related to lignification in pepper (Capsicum annuum L.) leaves. J. Plant Physiol. 152:51-57.
17. DOWD, P. F. 1994. Enhanced maize (Zea mays L.) pericarp browning: Associations with insect resistance and involvement of oxidizing enzymes. J. Chem. Ecol. 20:2497-2523.
18. DOWD, P. F., LAGRIMINI, L. M., and HERMS, D. A. 1998a. Differential leaf resistance to insects of transgenic sweetgum (Liquidambar styraciflue) expressing tobacco anionic peroxidase. Cell. Mol. Life Sci. 54:712-720.
19. DOWD, P. F., LAGRIMINI, L. M., and NELSEN, T. C. 1998b. Relative resistance of transgenic tomato tissues expressing high levels of tobacco anionic peroxidase to different insect species. Nat. Toxins. 6:241-249.
20. DUROUX, L. and WELINDER, K. G. 2003. The peroxidase gene family in plants: A phylogenetic overview. J. Mol. Evol. 57:397-407.
21. ELSTNER, E. F. and HEUPEL, A. 1976. Formation of hydrogen peroxide by isolated cell walls from horseradish (Armoracia lapathifolia Gilib.). Planta 130:175-180.
22. ENDO, T. 1968. Indoleacetate oxidase activity of horseradish and other plant peroxidase isozymes. Plant Cell Physiol. 9:331-341.
23. ENYEDI, A. J., YALPANI, N., SILVERMAN, P., and RASKIN, I. 1992. Localization, conjugation, and function of salicylic acid during the hypersensitive reaction to tobacco mosaic viras. Proc. Natl. Acad. Sci. U.S.A. 89:2480-2484.
24. ESPELIE, K. E., FRANCESCHI, V. R., and KOLATTUKUDY, P. E. 1986. Immunocytochemical localization and time course of appearance of an anionic peroxidase associated with suberization in wound-healing potato tuber tissue. Plant Physiol. 81:487-495.
25. EVERDEEN, D. S., KIEFER, S., WILLARD, J. J., MULDOON, E. P., DEY, P. M., LI, X.-B., and LAMPORT, D. T. A. 1988. Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol. 87:616-621.
26. FELTON, G. W., DONATO, K. K., BROADWAY, R. M., and DUFFEY, S. S. 1992. Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore. J. Insect Physiol. 38:277-285.
27. FELTON, G. W., SUMMERS, C. B., and MUELLER, A. J. 1994. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J. Chem. Ecol. 20:639-650.
28. FIELDES, M. A. and GERHARDT, K. E. 1998. Apparent differences in the posttranslational modification of peroxidase between flax genotrophs and genotypes and between normal and stress-induced isozymes. Intern. J. Plant Sci. 159:504-512.
29. GAFFNEY, T., FRIEDRICH, L., VERNOOIJ, B., NEGROTTO, D., NYE, G., UKNES, S., WARD, E., KESSMANN, H., and RYALS, J. 1993. Requirement of salicylic-acid for the induction of systematic acquired-resistance. Science 261:754-756.
30. GASPAR, T., PENEL, C., CASTTLLO, F. J., and GREPPIN, H. 1985. A two-step control of basic and acidic peroxidases and its significance for growth and development. Physiol. Plant 64:418-423.
31. GLAZEBROOK, J. 2001. Genes controlling expression of defense responses in Arabidopsis - 2001 status. Curr. Opin. Plant Biol 4:301-308.
32. GOODIN, M. M., BIGGS, A. R., and CASTLE, A. M. 1993. Changes in levels and isozymes of peroxidase in wounded peach bark. Fruit Var. J. 47:185-192.
33. GRISEBACH, H. 1981. Lignins, in pp. 457-478, P. K., Stumpf, and E. E. Conn (eds), The Biochemistry of Plants, Vol. 7. Academic Press, New York.
34. HARTLEY, S. E. and LAWTON, J. H. 1992. Host-plant manipulation by gall-insects: A test of the nutrition hypothesis. J. Anim. Ecol. 61:113-119.
35. HOUSTON, D. B. 1983. Stand and seed source variation in peroxidase isozymes of Quercus rubra L. Silvae Genet. 32:59-63.
36. JANSEN, M. A. K., VAN DEN NOORT, R. A., ADILLAH TAN, M. Y., PRINSEN, E., LAGRIMINI, L. M., and THORNELEY, R. N. F. 2001. Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol. 126:1012-1023.
37. KANDAN, A., COMMARE, R. R., NANDAKUMAR, R., RAMIAH, M., RAGUCHANDER, T., and SAMIYAPPAN, R. 2002. Induction of phenylpropanoid metabolism by Pseudomonas fluorescens against tomato spotted wilt virus in tomato. Folia Microbiol (Praha). 47:121-129.
38. KARBAN, R. and BALDWIN, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.
39. KAWAOKA, A., KAWAMOTO, T., OHTA, H., SEKINE, M., TAKANO, M., and SHINMYO, A. 1994. Wound-induced expression of horseradish peroxidase. Plant Cell Rep. 13:149-154.
40. KRISTENSEN, B. K., BLOCH, H., and RASMUSSEN, S. K. 1999. Barley coleoptile peroxidases. Purification, molecular cloning, and induction by pathogens. Plant Physiol. 120:501-512.
41. KUNKEL, B. N. and BROOKS, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331.
42. LAGRIMINI, M. L. and ROTHSTEIN, S. 1987. Tissue specificity of tobacco peroxidase isozymes and their induction by wounding and tobacco mosaic virus infection. Plant Physiol. 84:438-442.
43. LI, H.-L. and HSIAO, J.-Y. 1975. A chemosystematic study of the series Laurifoliae of the red oaks: Phenolics of leaves. Bartonia 43:25-28.
44. MADER, M., UNGEMACH, J., and SCHLOß, P. 1980. The role of peroxidase isoenzyme groups of Nicotiana tabacum in hydrogen peroxide formation. Planta 147:467-470.
45. MAKSIMOV, I. V., CHEREPANOVA, E. A., and KHAIRULLIN, R. M. 2003. "Chitin-specific" peroxidases in plants. Biochemistry (Mosc) 68:111-115.
46. MATO, M. C., RÚA, M. L., and FERRO, E. 1988. Changes in levels of peroxidases and phenolics during root formation in Vitis cultured in vitro. Physiol. Plant 72:84-88.
47. MAYER, R. T., INBAR, M., MCKENZIE, C. L., SHATTERS, R., BOROWICZ, V., ALBRECHT, U., POWELL, C. A., and DOOSTDAR, H. 2002. Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Arch. Insect Biochem. Physiol. 51:151-169.
48. MCDOUGALL, G. J. 1993. Accumulation of wall-associated peroxidases during wound-induced suberization of flax. Plant Physiol. 142:651-656.
49. MOORE, J. P., PAUL, N. D., WHITTAKER, J. B., and TAYLOR, J. E. 2003. Exogenous jasmonic acid mimics herbivore-induced systemic increase in cell wall bound peroxidase activity and reduction in leaf expansion. Funct. Ecol. 17:549-554.
50. NEUMAN, P. R., FONG, F., NEWTON, R. J., and SEN, S. 1992. Induction of peroxidase isozymes during shoot enhancement by ABA in cotyledon explants of loblolly pine (Pinus taeda L.). J. Plant Physiol. 139:343-349.
51. PAO, C.-I. and MORGAN, P. W. 1988. Patterns of total peroxidase activity and isozyme complement during development of selected maturity genotypes of sorghum. Crop Sci. 28:531-535.
52. 2-metabolizing enzymes. Plant Physiol. 115:137-149.
53. REYMOND, P., WEBER, H., DAMOND, M., and FARMER, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding Arabidopsis. Plant Cell 12:707-719.
54. RIDGE, I. and OSBORNE, D. J. 1970. Hydroxyproline and peroxidases in cell walls of Pisum sativum: Regulation by ethylene. J. Exp. Bot. 69:843-856.
55. ROITTO, M., MARKKOLA, A., JULKUNEN-TIITTO, R., SARJALA, T., RAUTIO, P., KUIKKA, K., and TUOMI, J. 2003. Defoliation-induced responses in peroxidases, phenolics, and polyamines in scots pine (Pinus sylvestris L.) needles. J. Chem. Ecol. 29:1905-1918.
56. ROSSITER, M. C., SCHULTZ, J. C., and BALDWIN, I. T. 1988. Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267-277.
57. RYALIS, J., UKNES, S., and WARD, E. 1994. Systemic acquired-resistance. Plant Physiol. 104:1109-1112.
58. SAS INSTITUTE. 1999. SAS/STAT User's Guide. SAS Institute, Cary, NC.
59. SCHULTZ, J. C. and BALDWIN, I. T. 1982. Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149-151.
60. SIEGEL, B. Z. 1993. Plant peroxidases - an organismic perspective. Plant Growth Regul. 12:303-312.
61. SIEGEL, S. M. 1954. Studies on the biosynthesis of lignins. Physiol. Plant 7:41-50.
62. SNYDER, E. B. and HAMAKER, J. M. 1978. Inheritance of peroxidase isozymes in needles of loblolly and longleaf pines. Silvae Genet. 27:125-129.
63. SVALHEIM, Ø. and ROBERTSEN, B. 1990. Induction of peroxidases in cucumber hypocotyls by wounding and fungal infection. Physiol. Plant 78:261-267.
64. TAMARI, G., BOROCHOV, A., ATZORN, R., and WEISS, D. 1995. Methyl jasmonate induces pigmentation and flavonoid gene expression in petunia corollas: A possible role in wound response. Physiol. Plant 94:45-50.
65. THALER, J., STOUT, M. J., KARBAN, R., and DUFFEY, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767-1781.
66. THOMMA, B. P. H. J., TIERENS, K. F. M., PENNINCKY, I. A. M., MAUCHMANI, B., BROEKAERT, W. F., and CAMMUE, B. P. A. 2001. Different microorganisms differentially induce Arabidopsis disease response pathways. Plant. Physiol. Biochem. 39:673-680.
67. TOGNOLLI, M., PENEL, C., GREPPIN, H., and SIMON, P. 2002. Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129-138.
68. TRAW, M. B., KIM, J., ENRIGHT, S., CIPOLLINI, D. F., and BERGELSON, J. 2003. Negative cross-talk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12:1125-1135.
69. VANCE, C. P., KIRK, T. K., and SHERWOOD, R. T. 1980. Lignification as a mechanism of disease resistance. Annu. Rev. Phytopath. 18:259-288.
70. VANLOON, L. C. 1985. Pathogenesis-related proteins. Plant Mol. Biol. 4:111-116.
71. YE, X. S., PAN, S. Q., and KUC, J. 1990. Activity, isozyme pattern, and cellular localization of peroxidase as related to systemic resistance of tobacco to blue mold (Peronospora tabacina) and to tobacco mosaic virus. Phytopathology 80:1295-1299.
72. 14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436-441.
73. ZIMMERLIN, A., WOJTASZEK, P., and BOLWELL, G. P. 1994. Synthesis of dehydrogenation polymers of ferulic acid with high specificity by a purified cell-wall peroxidase from French bean (Phaseolus vulgaris L.). Biochem. J. 299:747-753.