Skip to main content
SpringerLink
Log in

Enhanced maize (Zea mays L.) pericarp browning: Associations with insect resistance and involvement of oxidizing enzymes

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The kernel pericarp of a maize (Zea mays L.) inbred, Mp313E, that browns rapidly at milk stage when damaged and that is resistant toAspergillus flavus Link and the dusky sap beetleCarpophilus lugubris Murray compared to a susceptible inbred, SC212M, was examined for differing oxidizing enzymes (peroxidases) and their substrate specificity. Additional pericarp enzymes were constitutively produced by the Mp313E inbred compared to the SC212M inbred, as indicated by gel electrophoresis and isoelectric focusing. These enzymes oxidized relevent pericarp substrates such as ferulic acid. Similar results were seen with two varieties of maize containing theCh mutant gene, which brown upon senescence in that enhanced oxidation of ferulic acid was seen in homogenates of browned pericarp compared to that which was cold-shocked and did not brown. Corn powder that was browned by mixing oxidizing enzymes with corn pericarp components ferulic acid and coumaric acid were typically less preferred/more toxic to caterpillars such asHelicoverpa zea (Boddie) and sap beetles such asC. lugubris. Thus, enhanced browning of maize pericarp can promote resistance to insects and is at least partly influenced by the presence of oxidizing enzymes. This mechanism may also promote resistance to maize pathogens, including those that produce mycotoxins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Assabgui, R.A., Reid, L.M., Hamilton, R.I., andArnason, J.T. 1993. Correlation of kernel (E)-ferulic acid content of maize with resistance toFusarium graminearum.Phytopathology 83:949–953.

    Google Scholar 

  • Barz, W., andHoesel, W. 1978. Metabolism and degradation of phenolic compounds in plants.Recent Adv. Phytochem. 12:339–369.

    Google Scholar 

  • Bilgrami, K.S., Sinha, K.K., andSingh, P. 1981. Inhibition of aflatoxin production by ferulic acid on some cereals and oil seeds.Curr. Sci. 50:997–998.

    Google Scholar 

  • Bio-Rad. 1976. Protein assay. Bio-Rad Corp., Richmond, California.

    Google Scholar 

  • Brad, I., Terbea, M., Marcu, Z., andHurduc, N. 1974. Influenta infectarii cuFusarium moniliforme Scheid a unor linii si hibrizi de porumb, asupra spectrului izoenzimelor peroxidazice.Stud. Cerret. Biochim. 17:11–14.

    Google Scholar 

  • Brewbaker, J.L., andHasegawa, Y. 1975. Polymorphisms of the major peroxidases of maize, pp. 659–673,in C.L. Markert (ed.). Isozymes III. Developmental Biology. Academic, New York.

    Google Scholar 

  • Brewbaker, J.L., Nagai, C., andLiu, E.H. 1985. Genetic polymorphisms of 13 maize peroxidases.J. Hered. 76:159–167.

    Google Scholar 

  • Byrde, R.J.W., Fielding, A.H., andWilliams, A.H. 1960. The role of oxidized polyphenols in the varietal resistance of apples to brown rot, pp. 95–99,in J.B. Pridham (ed.). Phenolics in Plants in Health and Disease. Pergamon Press, New York.

    Google Scholar 

  • Byrne, P.F., Darrah, L.L., Simpson, K.B., Keaster, A.J., Barry, B.D., andZuber, M.S. 1989. Maize silk pH as an indicator of resistance to the com earworm (Lepidoptera: Noctuidae).Environ. Entomol. 18:356–360.

    Google Scholar 

  • Campa, A. 1991. Biological roles of plant peroxidases: Known and potential function, pp. 25–50,in J. Everse, K.E. Everse, and M.B. Grisham (eds.). Peroxidases in Chemistry and Biology, Vol. II. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Cardena-Gomez, G.C., andNicholson, R.L. 1987. Papilla formation and associated peroxidase activity: A non-specific response to attempted fungal penetration of maize.Physiol. Mol. Plant Pathol. 31:51–67.

    Article  Google Scholar 

  • Chen, J.S., Wei, C., Rolle, R.S., Otwell, W.S., Balaban, M.O., andMarshall, M.R. 1991. Inhibitory effect of kojic acid on some plant and crustacean polyphenol oxidases.J. Agric. Food. Chem. 39:1396–1401.

    Article  Google Scholar 

  • Classen, D., Arnason, J.T., Serratos, J.A., Lambert, J.D.H., Nozzolillo, C., andPhilocéne, B.J.R. 1990. Correlation of phenolic acid content of maize to resistance toSitophilus zeamais, the maize weevil, in CIMMYT's collections.J. Chem. Ecol. 16:301–315.

    Article  Google Scholar 

  • Coley, P.D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol. Monogr. 53:209–233.

    Google Scholar 

  • Conyers, S.M., andKidwell, D.A. 1991. Chromogenic substrates for horseradish peroxidase.Anal. Biochem. 192:207–211.

    PubMed  Google Scholar 

  • Dowd, P.F. 1988. Toxicological and biochemical interactions of the fungal metabolites fusaric acid and kojic acid with xenobiotics inHeliothis zea (F.) andSpodoptera frugiperda (J.E. Smith).Pestic. Biochem. Physiol. 32:123–134.

    Article  Google Scholar 

  • Dowd, P.F. 1990. Responses ofCarpophilus hemipterus larvae and adults to selected secondary metabolites of maize.Entomol. Exp. Appl. 54:29–36.

    Article  Google Scholar 

  • Dowd, P.F. 1992. Corn kernel aryl alcohol oxidases as cross-resistance mechanisms for fungi and insects. Abstract AGRO-107,in Abstracts of the 203rd meeting of the American Chemical Society, Washington, DC.

  • Dowd, P.F. 1994. Examination of anAspergillus flavus resistant inbred of maize for cross-resistance to sap beetle vectors.Entomol. Exp. Appl. 77:177–180.

    Google Scholar 

  • Dowd, P.F., andLagrimini, L.M. 1994. Tissues of transgenic flowering tobacco and tomato overexpressing tobacco anionic peroxidase are resistant to insects. Submitted.

  • Dowd, P.F., andNorton, R.A. 1995. Browning-associated mechanisms of resistance to insects in com callus tissue. Submitted.

  • Dowd, P.F., andSparks, T.C. 1986. Characterization of atrans-permethrin hydrolyzing enzyme fromPseudoplusia includens.Pestic. Biochem. Physiol. 25:73–81.

    Article  Google Scholar 

  • Dowd, P.F., andVega, F.E. 1995. Arylalcohol oxidase generated products of allelochemicals as potential resistance mechanism against insects: Effects on the com leafhopperDalbulus maidis. Submitted.

  • Dowd, P.F., andWeber, C.M. 1991. A labor-saving method for rearing a corn sap beetle,Carpophilus freemani Dobson (Coleoptera: Nitidulidae) on pinto bean-based diet.J. Agric. Entomol. 8:149–153.

    Google Scholar 

  • Dowd, P.F., Bartelt, R.J., andWicklow, D.T. 1992. Novel insect trap useful in capturing sap beetles and other flying insects.J. Econ. Entomol. 85:772–778.

    Google Scholar 

  • Espelie, K.E., Franceschi, V.R., andKolattukudy, 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. 81:487–492.

    Google Scholar 

  • Evershed, R.P., Spooner, N., Prescott, M.C., andGoad, L.J. 1988. Isolation and characterization of intact steryl ferulates from seeds.J. Chromatogr. 440:23–35.

    Article  Google Scholar 

  • Felton, G.W., Donato, K.K., del Vecchio, R.J., andDuffey, S.S. 1989. Activation of plant polyphenol oxidases by insect feeding damage reduces the nutritive quality of foliage.J. Chem. Ecol. 15:2667–2694.

    Article  Google Scholar 

  • Felton, G.W., Donato, K.K., Broadway, R.M., andDuffey, S.S. 1992. Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore,Spodoptera exigua.J. Insect Physiol. 38:277–285.

    Article  Google Scholar 

  • Fry, S.C. 1979. Phenolic components of the primary cell wall and their possible role in the hormonal regulation of growth.Planta 146:343–351.

    Article  Google Scholar 

  • Fry, S.C. 1982. Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein.Biochem. J. 204:449–455.

    PubMed  Google Scholar 

  • Fry, S.C. 1986. Polymer-bound phenols as natural substrates of peroxidases, pp. 169–181,in H. Greppin, C. Penel, and T. Gaspar (eds.). Molecular and Physiological Aspects of Plant Peroxidases. University of Geneva, Switzerland.

    Google Scholar 

  • Gaspar, T., Penel, C., Thorpe, T., andGreppin, H. 1982. Peroxidases: 1970–1980: A Survey of their Biochemical and Physiological Roles in Higher Plants. Université de Geneve, Centre de Botanique, Geneva, Switzerland, 323 pp.

    Google Scholar 

  • Gatehouse, A.M.R., Howe, D.S., Flemming, J.E., Hilder, V.A., andGatehouse, J.A. 1991. Biochemical basis of insect resistance in winged bean (Psophocarpus tetragonolobus) seeds.J. Sci. Food Agric. 55:63–74.

    Google Scholar 

  • Gomez, L.A., Rodriguez, J.G., Poneleit, C.G., andBlake, D.F. 1983. Relationship between some characteristics of the corn kernel pericarp and resistance to the rice weevil (Coleoptera: Curculionidae).J. Econ. Entomol. 76:797–800.

    Google Scholar 

  • Harris, P.J., andHartley, R.D. 1970. Detection of bound ferulic acid in cell walls of the Graminae by ultraviolet fluorescence microscopy.Nature 259:508–510.

    Article  Google Scholar 

  • Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, R.F., andBoulter, D. 1987. A novel mechanism of insect resistance engineered into tobacco.Nature 330:160–163.

    Article  Google Scholar 

  • Hood, E.E., Hood, K.R., andFritz, S.E. 1991. Hydroxyproline-rich glycoproteins in cell walls of pericarp from maize.Plant Sci. 79:12–22.

    Article  Google Scholar 

  • Kahl, G. 1974. Metabolism in plant storage tissue slices.Bot. Rev. 40:263–314.

    Google Scholar 

  • Kato, Y., andNevins, D.J. 1985. Isolation and identification ofO-(5-O-feruloyl-l-arabinofuranosyl)-(1–3)-O-Β-d-xylopyranosyl-(1–4)-d-xylopyranose as a component ofZea shoot cell walls.Carbohydr. Res. 137:139–150.

    Article  Google Scholar 

  • Kojima, S. 1931. Studies on peroxidase. II. The effect of peroxidase on the bactericidal action of phenols.J. Biochem. (Tokyo) 14:95–109.

    Google Scholar 

  • Kollmorgan Instruments Corp. 1992. Munsell Soil Charts. Kollmorgan Instruments Corp., Newburg, NY.

    Google Scholar 

  • Lagrimini, L.M., Vaughn, J., Erb, W.A., andMiller, S.A. 1993. Peroxidase overproduction in tomato: wound-induced polyphenol deposition and disease resistance.HortSci. 28:218–221.

    Google Scholar 

  • Lee, C.Y. 1992. Enzymatic oxidation of phenolic compounds in fruits, pp. 305–319,in C.T. Ho, C.Y. Lee, and M.T. Huang (eds.). Phenolic Compounds in Food and Their Effects on Health. I. Analysis, Occurrence, and Chemistry. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Macri, F., DiLenna, P., andVianello, A. 1974. Preliminary research on peroxidase, polyphenol oxidase, and phenol content in healthy and infected com leaves, susceptible and resistant toHelminthosporium maidis race T.Riv. Pathol. Veg. Ser. 4. 10:109–121.

    Google Scholar 

  • Markwalder, H.-O., andNeukom, H. 1976. Diferulic acid as a possible crosslink in hemicelluloses from wheat germ.Phytochemistry 15:836–837.

    Article  Google Scholar 

  • McCallum, J.A., andWalker, J.R.L. 1991. Phenolic biosynthesis during grain development in wheat (Triticum aestivum L.) III. Changes in hydroxycinnamic acids during grain development.J. Cereal Sci. 13:161–172.

    Google Scholar 

  • Miles, P.W., andOertli, J.J. 1993. The significance of antioxidants in aphid-plant interactions: The redox hypothesis.Entomol. Exp. Appl. 67:275–283.

    Google Scholar 

  • Neuffer, M.G., Jones, L., andZuber, M.S. 1969. The Mutants of Maize. Crop Science Society of America, Madison, Wisconsin.

    Google Scholar 

  • Norton, R.A. 1994. Isolation and identification of steryl cinnamic acid derivatives from corn bran.Cereal Chem. 71:111–117.

    Google Scholar 

  • O'Connel, R.J., Brown, I.R., Mansfield, J.W., Bailey, J.A., Mazau, D., Rumeau, D., andEsquerre-Tugaye, M.T. 1990. Immunocytochemical localization of hydroxyproline-rich glycoproteins accumulating in melon and bean at sites of resistance to bacteria and fungi.Mol. Plant Microbe Interactions 3:33–40.

    Google Scholar 

  • Ohashi, H., Yamamoto, E., Lewis, N.G., andTowers, G.H.N. 1987. 5-hydroxyferulic acid inZea mays andHordeum vulgare cell walls.Phylochemistry 26:1915–1916.

    Google Scholar 

  • Ohba, T., Murakami, H., andHara, S. 1971. Identification ofl-dopa and protocatechuic acid as main precursor of pigment of brown rice-koji.Agric. Biol. Chem. 35:674–681.

    Google Scholar 

  • Pickering, J.W., Powell, B.L., Wender, S.H., andSmith, E.C. 1973. Ferulic acid: A substrate for two isoperoxidases fromNicotiana tabacum tissue cultures.Phytochemistry 12:2639–2643.

    Article  Google Scholar 

  • Ralph, J., andHelm, R.F. 1993. Lignin/hydroxycinnamic acid/polysaccharide complexes: synthetic models for regiochemical characterization, pp. 201–246,in H.G. Jung, D.R. Buxton, R.D. Hatfield, and J. Ralph (eds.). Forage Cell Wall Structure and Digestibility. American Society of Agronomy, Madison, Wisconsin.

    Google Scholar 

  • Raupp, M.J. 1985. Effects of leaf toughness on mandibular wear of the leaf beetle,Plagiodera versicolora.Ecol. Entomol. 10:73–79.

    Google Scholar 

  • Reese, J.C. 1978. Chronic effects of plant allelochemicals on insect nutritional physiology.Entomol. Exp. Appl. 24:425–431.

    Google Scholar 

  • Riley, R.G., andKolattukudy, P.E. 1975. Evidence for covalently attachedp-coumaric acid and ferulic acid in cutins and suberins.Plain Physiol. 56:650–654.

    Google Scholar 

  • Schloss, P., Walter, C., andMÄder, M. 1987. Basic peroxidases in isolated vacuoles ofNicotiana tabacum L. Planta 170:225–229.

    Article  Google Scholar 

  • Scott, G.E., andZummo, N. 1988. Sources of resistance in maize to kernel infection byAspergillus flavus in the field.Crop Sci. 28:504–507.

    Google Scholar 

  • Seitz, L.M. 1989. Stanol and sterol esters of ferulic andp-coumaric acids in wheat, corn, rye and triticale.J. Agric. Food Chem. 37:662–667.

    Google Scholar 

  • Serratos, A., Arnason, J.T., Nozzolillo, C., Lambert, J.D.H., Philogéne, B.J.R., Fulcher, G., Davidson, K., Peacock, L., Atkinson, J., andMorand, P. 1987. Factors contributing to resistance of exotic maize populations to maize weevil,Silophilus zeamaiz.J. Chem. Ecol. 13:751–762.

    Article  Google Scholar 

  • Steffens, J.C., andWaters, D.S. 1991. Biochemical aspects of glandular trichome-mediated insect resistance in theSolanaceae, pp. 136–149,in P.E. Hedin (ed.). Naturally Occurring Pest Bioregulators. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Tracy, W.F., andSchmidt, D.H. 1987. Effect of endosperm type on pericarp thickness in sweet corn inbreds.Crop. Sci. 27:692–694.

    Google Scholar 

  • Turner, W.F., andAldridge, D.C. 1983. Fungal Metabolites II. Academic Press, New York.

    Google Scholar 

  • Urbanska, A., andLeszczynski, B. 1992. Biochemical adaptations of cereal aphids to host plants, pp. 277–299,in S.B.J. Menken, J.H. Visser, and P. Harrewijn. (eds.). Proceedings, 8th International Symposium on Insect-Plant Relationships. Kluwer Academic, Dordrecht, The Netherlands.

    Google Scholar 

  • Urs, N.V.R., andDunleavy, J.M. 1975. Enhancement of the bactericidal activity of a peroxidase system by phenolic compounds.Phytopathology 65:686–690.

    Google Scholar 

  • Vance, C.P., Anderson, J.O., andSherwood, R.T. 1976. Soluble and cell wall peroxidases in reed canarygrass in relation to disease resistance and localized lignin formation.Plant Physiol. 57:920–922.

    Google Scholar 

  • Vance, C.P., Kirk, T.K., andSherwood, R.T. 1980. Lignification as a mechanism of disease resistance.Annu. Rev. Phytopathol. 18:259–288.

    Article  Google Scholar 

  • van Huystee, R.B.V., andZheng, X. 1993. Cationic peanut peroxidase and the oxidation of ferulic acid.Phytochemistry 34:933–939.

    Article  Google Scholar 

  • van Loon, L.C. 1971. Tobacco polyphenoloxidases: A specific staining method indicating nonidentity with peroxidases.Phytochemistry 10:503–507.

    Article  Google Scholar 

  • Waiss, A.C., Chan, B.G., Elliger, C.A., Wiseman, B.R., McMillian, W.W., Widstrom, N.W., Zuber, M.S., andKeaster, A.J. 1979. Maisin, a flavone glycoside from com silks with antibiotic activity toward corn earworm.J. Econ. Entomol. 72:256–258.

    Google Scholar 

  • Wiseman, B.R., andIsenhour, D.J. 1993. Interaction of diet ingredients with levels of silk of a corn genotype resistant to corn earworm (Lepidoptera: Noctuidae).J. Econ. Entomol. 86:1291–1296.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Mycotoxin Research Unit U.S.D.A., Agricultural Research Service, National Center for Agricultural Utilization Research, 1815 N. University St., 61604, Peoria, Illinois

    Patrick F. Dowd

Authors
  1. Patrick F. Dowd
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dowd, P.F. Enhanced maize (Zea mays L.) pericarp browning: Associations with insect resistance and involvement of oxidizing enzymes. J Chem Ecol 20, 2777–2803 (1994). https://doi.org/10.1007/BF02098389

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02098389

Key words

Search

Navigation