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Differential Activity of Peroxidase Isozymes in Response to Wounding, Gypsy Moth, and Plant Hormones in Northern Red Oak (Quercus rubra L.)

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Abstract

We measured total peroxidase activity and the activities of peroxidase isoforms in leaves of red oak (Quercus rubra L.) seedlings exposed to wounding and plant hormones in the greenhouse. Activity of specific peroxidase isoforms was induced differentially by gypsy moth wounding, mechanical wounding, and the wound-associated plant hormone jasmonic acid. Activity of one isoform was enhanced modestly by treatment with salicylate. A study of peroxidase activity in naturally occurring galls elicited on red oak leaves by 12 hymenopteran and dipteran insect species found 16 POD isoforms, 11 of which were differentially induced or suppressed in galls compared with leaves. In both studies, total peroxidase activity as measured spectrophotometrically was not clearly related to activity of these isoforms. These results indicate that red oak seedlings and trees may respond specifically to wounding, particular insects, and plant signals through changes in the activities of individual isozymes.

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REFERENCES

  • APPEL, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19:1521–1552.

    Google Scholar 

  • 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.

    Google Scholar 

  • BASHAN, Y., OKON, Y., and HENIS, Y. 1987. Peroxidase, polyphenol oxidase, and phenols in relation to resistance against Pseudomonas syringaepv. tomatoin tomato plants. Can. J. Bot. 65:366–372.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • BOSTOCK, R. 1999. Signal conflicts and synergies in induced resistance to multiple attackers. Physiol. Mol. Plant Path. 55:99–109.

    Google Scholar 

  • BOSTOCK, R.M. and STERMER, B. A. 1989. Perspectives on wound healing in resistance to pathogens. Annu. Rev. Phytopath. 27:343–371.

    Google Scholar 

  • BRONNER, R., WESTPHAL, E., and DREGER, F. 1991. Enhanced peroxidase activity associated with the hypersensitive response of Solanum dulcamarato the gall mite Aceria cladophthirus(Acari: Eriophyoidea). Can. J. Bot. 69:2192–2196.

    Google Scholar 

  • BUZI, A., CHILOSI, G., DE SILLO, D., and MAGRO, P. 2004. Induction of resistance in melon to Didymella bryoniaeand Sclerotinia sclerotiorumby seed treatments with acibenzolar-S-methyl and methyl jasmonate but not with salicylic acid. J. Phytopathol. 152:34–42.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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 tuberosumL. Proc. Natl. Acad. Sci., U.S.A. 91:2329–2333.

    Google Scholar 

  • 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.

    Google Scholar 

  • CONTI, G. G., PIANEZZOLA, A., ARNOLDI, A., VIOLINI, G., and MAFFI,D. 1996. Possible involvement of salicylic acid in systemic acquired resistance of Cucumis sativusagainst Sphaerotheca fuliginea. Eur. J. Plant Path. 102:537–544.

    Google Scholar 

  • DÍAZ, J. and MERINO, F. 1998. Wound-induced shikimate dehydrogenase and peroxidase related to lignification in pepper (Capsicum annuumL.) leaves. J. Plant Physiol. 152:51–57.

    Google Scholar 

  • DOWD, P. F. 1994. Enhanced maize (Zea maysL.) pericarp browning: Associations with insect resistance and involvement of oxidizing enzymes. J. Chem. Ecol. 20:2497–2523.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • DUROUX, L. and WELINDER, K. G. 2003. The peroxidase gene family in plants: A phylogenetic overview. J. Mol. Evol. 57:397–407.

    Google Scholar 

  • ELSTNER, E. F. and HEUPEL, A. 1976. Formation of hydrogen peroxide by isolated cell walls from horseradish (Armoracia lapathifoliaGilib.). Planta 130:175–180.

    Google Scholar 

  • ENDO, T. 1968. Indoleacetate oxidase activity of horseradish and other plant peroxidase isozymes. Plant Cell Physiol. 9:331–341.

    Google Scholar 

  • 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 virus. Proc. Natl. Acad. Sci. U.S.A. 89:2480–2484.

    Google Scholar 

  • 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 woundhealing potato tuber tissue. Plant Physiol. 81:487–495.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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 acquiredresistance. Science 261:754–756.

    Google Scholar 

  • GASPAR, T., PENEL, C., CASTILLO, 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.

    Google Scholar 

  • GLAZEBROOK, J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol 4:301–308.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • HARTLEY, S. E. and LAWTON, J.H. 1992. Host-plant manipulation by gall-insects:Atest of the nutrition hypothesis. J. Anim. Ecol. 61:113–119.

    Google Scholar 

  • HOUSTON, D. B. 1983. Stand and seed source variation in peroxidase isozymes of Quercus rubraL. Silvae Genet. 32:59–63.

    Google Scholar 

  • 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.

    Google Scholar 

  • KANDAN, A., COMMARE, R. R., NANDAKUMAR, R., RAMIAH,M., RAGUCHANDER, T., and SAMIYAPPAN, R. 2002. Induction of phenylpropanoid metabolism by Pseudomonas fluorescensagainst tomato spotted wilt virus in tomato. Folia Microbiol (Praha). 47:121–129.

    Google Scholar 

  • KARBAN, R. and BALDWIN, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • KAWAOKA, A., KAWAMOTO, T., OHTA, H., SEKINE, M., TAKANO, M., and SHINMYO, A. 1994.Woundinduced expression of horseradish peroxidase. Plant Cell Rep. 13:149–154.

    Google Scholar 

  • 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.

    Google Scholar 

  • KUNKEL, B. N. and BROOKS, D.M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325–331.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • MÄDER, M., UNGEMACH, J., and SCHLOβ, P. 1980. The role of peroxidase isoenzyme groups of Nicotiana tabacumin hydrogen peroxide formation. Planta 147:467–470.

    Google Scholar 

  • MAKSIMOV, I. V., CHEREPANOVA, E. A., and KHAIRULLIN, R. M. 2003. “Chitin-specific” peroxidases in plants. Biochemistry (Mosc) 68:111–115.

    Google Scholar 

  • MATO, M. C., RÚA, M. L., and FERRO, E. 1988. Changes in levels of peroxidases and phenolics during root formation in Vitiscultured in vitro. Physiol. Plant 72:84–88.

    Google Scholar 

  • 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.

    Google Scholar 

  • MCDOUGALL, G. J. 1993. Accumulation of wall-associated peroxidases during wound-induced suberization of flax. Plant Physiol. 142:651–656.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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 taedaL.). J. Plant Physiol. 139:343–349.

    Google Scholar 

  • 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.

    Google Scholar 

  • RAO, M. V., PALIYATH, G. P., ORMROD, D. P., MURR, D. P., and WATKINS, C. B. 1997. Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Plant Physiol. 115:137–149.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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 sylvestrisL.) needles. J. Chem. Ecol. 29:1905–1918.

    Google Scholar 

  • 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.

    Google Scholar 

  • RYALIS, J., UKNES, S., and WARD, E. 1994. Systemic acquired-resistance. Plant Physiol. 104:1109–1112.

    Google Scholar 

  • SAS INSTITUTE. 1999. SAS/STAT User's Guide. SAS Institute, Cary, NC.

    Google Scholar 

  • SCHULTZ, J. C. and BALDWIN, I. T. 1982. Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151.

    Google Scholar 

  • SIEGEL, B. Z. 1993.Plant peroxidases-an organismic perspective. Plant Growth Regul. 12:303–312.

    Google Scholar 

  • SIEGEL, S. M. 1954. Studies on the biosynthesis of lignins. Physiol. Plant 7:41–50.

    Google Scholar 

  • SNYDER, E. B. and HAMAKER, J. M. 1978. Inheritance of peroxidase isozymes in needles of loblolly and longleaf pines. Silvae Genet. 27:125–129.

    Google Scholar 

  • SVALHEIM, Ø. and ROBERTSEN, B. 1990. Induction of peroxidases in cucumber hypocotyls bywounding and fungal infection. Physiol. Plant 78:261–267.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • TRAW, M. B., KIM, J., ENRIGHT, S., CIPOLLINI, D. F., and BERGELSON, J. 2003. Negative cross-talk between salicylate-and jasmonate-mediated pathways in theWassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12:1125–1135.

    Google Scholar 

  • VANCE, C. P., KIRK, T. K., and SHERWOOD, R. T. 1980. Lignification as a mechanism of disease resistance. Annu. Rev. Phytopath. 18:259–288.

    Google Scholar 

  • VANLOON, L. C. 1985. Pathogenesis-related proteins. Plant Mol. Biol. 4:111–116.

    Google Scholar 

  • 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.

    Google Scholar 

  • ZHANG, Z.-P. and BALDWIN, I. T. 1997. Transport of [2-14C] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436–441.

    Google Scholar 

  • 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 vulgarisL.). Biochem. J. 299:747–753.

    Google Scholar 

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  1. Department of Entomology, Pesticide Research Laboratory, The Pennsylvania State University, University Park, Pennsylvania, 16802, USA

    Steven D. Allison & Jack C. Schultz

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Allison, S.D., Schultz, J.C. Differential Activity of Peroxidase Isozymes in Response to Wounding, Gypsy Moth, and Plant Hormones in Northern Red Oak (Quercus rubra L.). J Chem Ecol 30, 1363–1379 (2004). https://doi.org/10.1023/B:JOEC.0000037745.66972.3e

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