Skip to main content
SpringerLink
Log in

BIOCHEMICAL RESPONSES OF CHESTNUT OAK TO A GALLING CYNIPID

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

Abstract

We characterized the distribution of nutritional and defensive biochemical traits in galls elicited on chestnut oak (Quercus prinus L.) by the gall wasp Andricus petiolicolus Basse (Cynipidae) in comparison with gypsy moth-wounded and unwounded leaves. Gall cortex and epidermis exhibited elevated soluble peroxidase (POX) and soluble invertase activities, and greater condensed tannin concentrations than did nutritive tissues or leaves. Nutritive tissue, on which the insect feeds, contained few polyphenols, and lower POX and invertase activities compared with other gall tissues and leaves. Elevated total POX activity arose from a complex pattern of enhanced and suppressed isoform activities in galls. Invertase enzyme activity decreased in all tissues over the course of the 7-d study, although gypsy moth wounding suppressed this decline slightly in ungalled leaves. Our results indicate that the distribution of biochemical defenses in this typical cynipid gall differs significantly from the leaf tissue from which it is formed and support a role for invertases in establishing the gall as a sink. A. petiolicolus larvae do not induce, and may suppress, plant defense responses in nutritive tissue, while enzymatic activity and phenolic accumulation are enhanced in gall tissues surrounding feeding sites. These patterns suggest that the gall is manipulated by the insect to enhance its food and protective value.

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

  • Appel, H. M., Govenor, H. L., D’Ascenzo, M., Siska, E., and Schultz, J. C. 2001. Limitations of folin assays of foliar polyphenols in ecological studies. J. Chem. Ecol. 27:761–778.

    Google Scholar 

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

    Google Scholar 

  • Arnold, W. N. 1965. β -fructofuranosidase from grape berries. Biochim. Biophys. Acta 110:134–147.

    Google Scholar 

  • Arnold, T. M. and Schultz, J. C. 2002. Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593.

    Google Scholar 

  • Barrett, J. D., Clarke, P. V., and Richardson, D. H. S. 1998. The in-vitro culture of rose-gall tissue induced by the cynipid wasp (Diplolepsis spinosa Ashmead). Symbiosis 25:229–236.

    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. Anutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J. Chem. Ecol. 23:97–117.

    Google Scholar 

  • Billet, E. E., Billet, M. A., and Burnett, J. H. 1977. Stimulation of maize invertase activity following infection by Ustilago maydis. Phytochemistry 16:1163–1166.

    Google Scholar 

  • Bolwell, G. P. 1996. The origin of the oxidative burst in plants. Biochem. Soc. Trans. 24:438–442.

    Google Scholar 

  • Bronner, R. 1977. Contribution a l’Étude histochimique des tissus nourriciers des zoocÉcidies. Marcellia 40:1–134.

    Google Scholar 

  • Bronner, R. 1983. Adaptation insect-plant in cynipid galls, pp. 61–68, N. S. Margaris, M. Arianoutsou-Faraggitaki, and R. J. Reiter (eds.). Adaptations to Terrestrial Environments International Symposium on Adaptations to Terrestrial Environment. 1982: (ChalkidikÉ, Greece). Plenum Press, New York.

    Google Scholar 

  • Bronner, R. 1992 The role of nutritive cells in the nutrition of cynipids and cecidomyiids, pp. 118–140, in J. D. Shorthouse and O. Rohfritsch (eds.). Biology of Insect-Induced Galls. Oxford University Press, New York.

    Google Scholar 

  • Burton, S. G. and Kirchmann, S. 1997 Optimised detergent-based method for extraction of a chloroplast membrane-bound enzyme: polyphenol oxidase from tea (Camellia sinensis). Biotechnol. Tech. 11: 645–648

    Google Scholar 

  • Carroll, G. 1988 Fungal endophytes in stems and leaves: From latent pathogen to mutualistic symbiont. Ecology 69: 2–9

    Google Scholar 

  • Chaman, M. E., Corcuera, L. J., Zuniga, G. E., Cardemil, L., and Argandona, V. H. 2001 Induction of soluble and cell wall peroxidases by aphid infestation in barley. J. Agric. Food Chem. 49: 2249–2253

    Google Scholar 

  • Christensen, J. H., Bauw, G., Welinder, K. G., VanMontagu, M., and Boerjan, 1998 Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol. 118: 125–135

    Google Scholar 

  • Cornell, H. V. 1983 The secondary chemistry and complex morphology of galls formed by the Cynipidae (Hymenoptera): Why and how? Am. Midl. Nat. 110: 225–234

    Google Scholar 

  • Doke, N., Miura, Y., Sanchez, L. M., Park, H.-J., Noritake, T., Yoshioka, H., and Kawakita, K. 1996 The oxidative burst protects plants against pathogen attack: Mechanism and role as an emergency signal for plant bio-defence—a review. Gene 179: 45–51

    Google Scholar 

  • Dreger-Jauffret, F. and Shorthouse, J. D. 1992 Diversity of gall-inducing insects and their galls, pp. 8–33, inJ. D. Shorthouse and O. Rohfritsch, (eds.). Biology of Insect-Induced Galls. Oxford University Press, New York.

    Google Scholar 

  • Felt, E. P. 1940 Plant Galls and Gall Makers. Comstock, New York.

  • 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 

  • Gaspar, T., Penel, C., Thorpe, T., and Greppin, H. 1982 Peroxidases 1970–1980. A Survey of their Biochemical and Physiological Roles in Higher Plants. UniversitÉ de Genève, Genève.

  • Gijzen, M., Miller, S. S., Bowman, L. A., Batchelor, A. K., Boutilier, K., and Miki, B. L. 1999 Localization of peroxidase mRNAs in soybean seeds by in situ hybridization. Plant Mol. Biol. 411: 57–63

    Google Scholar 

  • Gopichandran, R., Peter, A. J., and Subramaniam, V. R. 1992 Age-correlated biochemical profiles of thrips galls in relation to population density of thrips. J. Nat. History. 26: 609–619

    Google Scholar 

  • Grisebach, H. 1981 Lignins, pp. 457–478, in P. K. Stumpf and E. E. Conn (eds.). The Biochemistry of Plants, Vol. 7. Academic Press, New York.

    Google Scholar 

  • Halder, J., Tamuli, P., and Bhaduri, A. N. 1998 Isolation and characterization of polyphenol oxidase from Indian tea leaf (Camellia sinensis). Nutr. Biochem. 9: 75–80

    Google Scholar 

  • Harris, N., Spence, J., and Oparka, K. J. 1994 General and enzyme histochemistry, pp. 51–68, in N. Harris and K. J. Oparka (eds.). Plant Cell Biology: A Practical Approach. Oxford University Press, New York.

    Google Scholar 

  • Hartley, S. E. 1998 The chemical composition of plant galls: Are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113: 492–501

    Article  Google Scholar 

  • Haruta, M., Pedersen, J. A., and Constabel, C. P. 2001 Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant.112: 552–558

    Google Scholar 

  • Hiraga, S., Ito, H., Sasaki, K., Yamakawa, H., Mitsuhara, I., Toshima, H., Matsui, H., Honma, M., and Ohashi, Y. 2000a. Wound-induced expression of a tobacco peroxidase is not enhanced by ethephon and suppressed by methyl jasmonate and coronatine. Plant Cell Physiol. 41: 165–170

    Google Scholar 

  • Hiraga, S., Yamamoto, K., Ito, H., Sasaki, K., Matisui, H., Honma, M., Nagamura, Y., Sasaki, T., and Ohashi, Y. 2000b. Diverse expression profiles of 21 rice peroxidase genes. FEBS Letters471: 245–250

    Google Scholar 

  • Hsu, A. F., Thomas, C. E., and Brauer, D. 1988 Evaluation of several methods for estimation of the total activity of potato polyphenol oxidase. J. Food Sci. 53: 1743–1745

    Google Scholar 

  • Huber, S. C. 1989 Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol. 91: 656–662

    Google Scholar 

  • Hunter, M. D. and Schultz, J. C. 1995 Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology 76: 1226–1232

    Google Scholar 

  • Inbar, M., Eshel, A., and Wool, D. 1997 Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76: 1506–1515

    Google Scholar 

  • Janzen, D. H. 1977 Why fruits rot, seeds mold, and meat spoils. Am. Nat.111: 691–713

    Google Scholar 

  • Kahn, V. 1985 Tropolone—-a compound that can aid in differentiating between tyrosinase and peroxidase. Phytochemistry 24: 915–920

    Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997 Induced Responses to Herbivory, University Chicago Press, Chicago.

    Google Scholar 

  • Kim, K. Y., Kwon, H. K., Kwon, S. Y., Lee, H. S., Hur, Y., Bang, J. W., Choi, K. S., and Kwak, S. S. 2000 Differential expression of four sweet potato peroxidase genes in response to abscisic acid and ethephon. Phytochemistry54: 19–22

    Google Scholar 

  • Kinsey, A. C. 1920 Phylogeny of cynipid genera and biological characteristics. Am. Mus. Nat. History Bull. 42: 357–402

    Google Scholar 

  • Kinsey, A. C. 1930 The gall wasp genus Cynips: A study in the origin of species. Indiana Univ. Stud.16: 84–86

    Google Scholar 

  • Lamb, C. and Dixon, R. A. 1997 The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 251–275

    Google Scholar 

  • Larson, K. C. and Whitham, T. G. 1997 Competition between plant galls and natural plant sinks: Plant architecture affects resistance to galling. Oecologia 109: 575–582

    Google Scholar 

  • Lebeda, A., Luhova, L., Sedlarova, M., and Jancova, D. 2001 The role of enzymes in plant-fungal pathogens interactions—Review. J. Plant Dis. Protect. 108: 89–111

    Google Scholar 

  • Leigh, R. A., Ap Rees, T., Fuller, W. A., and Banfield, J. 1979 The location of acid invertase activity and sucrose in the vacuoles of storage roots of beetroot (Beta vulgaris). Biochem. J. 178: 539–547

    Google Scholar 

  • Limam, F., Chahed, K., Ouelhazi, N., Ghrir, R., and Ouelhazi, L. 1998 Phytohormone regulation of isoperoxidases in Catharanthus roseussuspension cultures. Phytochemistry49: 1219–1225

    Google Scholar 

  • MacAdam, J. W., Nelson, C. J., and Sharp, R. E. 1992 Peroxidase activity in the leaf elongation zone of tall fescue. Plant Physiol. 99: 872–878

    Google Scholar 

  • Mäder, M., Ungemach, J., and Schlo β, P. 1980 The role of peroxidase isozyme groups of Nicotiana tabacum in hydrogen peroxide formation. Planta 147: 467–470

    Google Scholar 

  • Miller, L. 1959 Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426–428.

    CAS  Google Scholar 

  • Nierenstein, M. 1930 Galls. Nature 125: 348–349

    Google Scholar 

  • Nyman, T. and Julkunen-Tiitto, R. 2000 Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. PNAS USA 97: 13184–13187

    Google Scholar 

  • Paclt, J. and Hässler, J. 1967 Concentration of nitrogen in some plant galls. Phyton12: 173–176

    Google Scholar 

  • Patrick, J. W. 1990 Sieve element unloading, cellular pathway, mechanism, and control. Physiol. Plant. 78: 298–308

    Google Scholar 

  • Price, P. W., Fernandes, G. W., and Waring, G. L. 1987 Adaptive nature of insect galls. Environ. Entomol. 16: 15–24

    Google Scholar 

  • Rehill, B. J. and Schultz, J. C. 2003 Enhanced invertase activities in the galls of Hormaphis hamamelidis. J. Chem. Ecol. 29: 2703–2720

    Google Scholar 

  • Ricardo, C. P. P. and Ap Rees, T. 1970 Invertase activity during the development of carrot roots. Phytochemistry 9: 239–247

    Google Scholar 

  • Richard-Forget, F. C. and Gauillard, F. A. 1997 Oxidation of chlorogenic acid, catechins, and 4-methylcatechol in model solutions of pear Pyrus communis Cv. Williams. Polyphenol oxidase and peroxidase: A possible involvement of peroxidase in enzymatic browning. J. Agric. Food Chem. 45: 2472–2476

    Google Scholar 

  • Rohfritsch, O. and Arnold-Rinehart, H. 1991 Gall development and fine structure of the nutritive cells of Myopites blotti (Diptera, Tephritidae) on Inula salicina. Can. J. Bot. 69: 2232–2241

    Google Scholar 

  • Rossiter, M., Schultz, J. C., and Baldwin, I. T. 1988 Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69: 267–277

    CAS  Google Scholar 

  • SAS Institute, Inc. 1999 SAS/STAT® User’s Guide, Version 8. SAS Institute Inc., Cary, NC.

  • Scholes, J. D., Lee, P. J., Horton, P., and Lewis, D. H. 1994 Invertase: Understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew. New Phytol. 126: 213–222

    Google Scholar 

  • Schonrogge, K., Harper, L. J., and Lichtenstein, C. P. 2000 The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): Similarities between cynipid galls and seeds. Plant Cell Environ. 23: 215–222

    Google Scholar 

  • Schultz, B. B. 1992 Insect herbivores as potential causes of mortality and adaptation in gallforming insects. Oecologia 90: 297–299

    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 

  • Shin, R., Froderman, T., and Flurkey, W. H. 1997 Isolation and characterization of a mung bean leaf polyphenol oxidase. Phytochemistry 45: 15–21

    Google Scholar 

  • Spruce, J., Mayer, A. M., and Osborne, D. J. 1987 A simple histochemical method for locating enzymes in plant tissue using nitrocellulose blotting. Phytochemistry 26: 2901–2903

    Google Scholar 

  • Sturm, A. and Chrispeels, M. J. 1990 cDNA cloning of carrot extracellular β -fructosidase and its expression in response to wounding and bacterial infection. Plant Cell2: 1107–1119

    Article  Google Scholar 

  • Sumner, J. B. 1925 A more specific reagent for the determination of sugar in urine. J. Biol. Chem. 65: 393–395

    Google Scholar 

  • Tang, X., Ruffner, H.-P., Scholes, J. D., and Rolfe, S. A. 1996 Purification and characterisation of soluble invertases from leaves of Arabidopsis thaliana. Planta 198: 17–23

    Google Scholar 

  • Taper, M. L., Zimmerman, E. M., and Case, T. J. 1986 Sources of mortality for a cynipid all-wasp Dryocosmus dubiosus (Hymenoptera: Cynipidae): The importance of the tannin/fungus interaction. Oecologia 68: 437–445

    Google Scholar 

  • Tenhaken, R., Levine, A., Brisson, L. F., Dixon, R. A., and Lamb, C. 1995 Function of the oxidative burst in hypersensitive disease resistance. PNAS USA 92: 4158–4163

    Google Scholar 

  • Tono, T. and Fujita, S. 1995 Difference spectra spectrophotometry for polyphenol oxidase assay, pp. 188–199, in C. Y. Lee and J. R. Whitaker (eds.). Enzymatic Browning and Its Prevention. American Chemical Society, Washington DC.

  • Vaughn, K. C. and Duke, S. O. 1984 Function of polyphenol oxidase in higher plants. Physiol. Plant. 60: 106–112

    Google Scholar 

  • Weil, M. and Rausch, T. 1990 Cell wall invertase in tobacco crown gall cells. Enzyme properties and regulation by auxin. Plant Physiol. 94: 1575–1581

    Google Scholar 

  • Wilson, D. 1995 Fungal endophytes which invade insect galls: Insect athogens, benign saprophytes, or fungal inquilines? Oecologia 103: 255–260

    Google Scholar 

  • Wobus, U. and Weber, H. 1999 Seed maturation: Genetic programmes and control signals. Curr. Opin. Plant Biol. 21: 33–8

    Google Scholar 

  • Wojtaszek, P. 1997 Oxidative burst: an early plant response to pathogen infection. Biochem. J. 322: 681–692

    Google Scholar 

  • Wool, D., Aloni, R., Ben-Zvi, O., and Wollberg, M. 1999 A galling aphid furnishes its home with a built-in pipeline to the host food supply. Entomol. Exp. Appl. 9: 183–186

    Google Scholar 

  • Yelle, S., Chetelat, R. T., Dorais, M., Deverna, J. W., and Bennet, A. B. 1991. Sink metabolism in tomato fruit: IV. Genetic and biochemical analysis of sucrose accumulation. Plant Physiol. 95:1026–1035.

    Google Scholar 

  • Zhang, L., Cohn, N. S., and Mitchell, J. P. 1996. Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol. 112:1111–1117.

    Google Scholar 

Download references

Author information

Author notes

  1. STEVEN D. ALLISON

    Present address: Department of Biological Sciences, Stanford University, Stanford, CA, 94305-5020, USA

Authors and Affiliations

  1. Department of Biological Sciences, The Pennsylvania State University, University Park, PA, 16802, USA

    STEVEN D. ALLISON

  2. Department of Entomology, The Pennsylvania State University, University Park, PA, 16802, USA

    JACK C. SCHULTZ

Authors
  1. STEVEN D. ALLISON
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. JACK C. SCHULTZ
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to JACK C. SCHULTZ.

Rights and permissions

Reprints and permissions

About this article

Cite this article

ALLISON, S.D., SCHULTZ, J.C. BIOCHEMICAL RESPONSES OF CHESTNUT OAK TO A GALLING CYNIPID. J Chem Ecol 31, 151–166 (2005). https://doi.org/10.1007/s10886-005-0981-5

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-0981-5

Key Words

Search

Navigation