Journal of Chemical Ecology

, Volume 32, Issue 10, pp 2253–2267

Ellagitannins have Greater Oxidative Activities than Condensed Tannins and Galloyl Glucoses at High pH: Potential Impact on Caterpillars

  • Raymond V. Barbehenn
  • Christopher P. Jones
  • Ann E. Hagerman
  • Maarit Karonen
  • Juha-Pekka Salminen
Article

Abstract

Plants synthesize a diversity of tannin structures but little is known about whether these different types have different oxidative activities in herbivores. Oxidative activities of hydrolyzable and condensed tannins were compared at pH 10 with two methods: EPR spectrometry was used to quantify semiquinone radicals in anoxic conditions and a spectrophotometric assay was used to measure the rate of browning of phenolics oxidized in ambient oxygen conditions. A little-studied group of hydrolyzable tannins (ellagitannins) contained the most active tannins examined, forming high concentrations of semiquinone radicals and browning at the highest rates. On average, galloyl glucoses and high-molecular-weight gallotannins had intermediate to low oxidative activities. Condensed tannins generally formed low levels of semiquinone radicals and browned most slowly. The results suggest that ellagitannin-rich plants have active oxidative defenses against herbivores, such as caterpillars, whereas the opposite may hold true for plants that contain predominantly condensed tannins or high-molecular-weight gallotannins.

Key words

Tannin Ellagitannin Condensed tannin Galloyl glucose Gallotannin Phenolic compounds Oxidation Semiquinone radical Plant–herbivore interactions Caterpillar 

References

  1. Aerts, R. J., Barry, T. N., and McNabb, W. C. 1999. Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agric. Ecosyst. Environ. 75:1–12.CrossRefGoogle Scholar
  2. Appel, H. M. 1993. Phenolics in ecological interactions: the importance of oxidation. J. Chem. Ecol. 19:1521–1552.CrossRefGoogle Scholar
  3. Appel, H. M. and Martin, M. M. 1990. Gut redox conditions in herbivorous lepidopteran larvae. J. Chem. Ecol. 16:3277–3290.CrossRefGoogle Scholar
  4. Barbehenn, R. V., Cheek, S., Gasperut, A., Lister, E., and Maben, R. 2005. Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midguts of Malacosoma disstria and Orgyia leucostigma caterpillars. J. Chem. Ecol. 31:969–988.PubMedCrossRefGoogle Scholar
  5. Barbehenn, R. V., Poopat, U., and Spencer, B. 2003. Semiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry. Insect Biochem. Mol. Biol. 33:125–130.PubMedCrossRefGoogle Scholar
  6. Bors, W. and Michel, C. 1999. Antioxidant capacity of flavanols and gallate esters: Pulse radiolysis studies. Free Radic. Biol. Med. 27:1413–1426.PubMedCrossRefGoogle Scholar
  7. Bors, W., Michel, C., and Stettmaier, K. 2000. Electron paramagnetic resonance studies of radical species of proanthocyanins and gallate esters. Arch. Biochem. Biophys. 374:347–355.PubMedCrossRefGoogle Scholar
  8. Bors, W., Michel, C., and Stettmaier, K. 2001a. Structure–activity relationships governing antioxidant capacities of plant polyphenols. Methods Enzymol. 335:166–180.PubMedGoogle Scholar
  9. Bors, W., Yeap Foo, L., Hertkorn, N., Michel, C., and Stettmaier, K. 2001b. Chemical studies of proanthocyanidins and hydrolyzable tannins. Antiox. Redox Signal. 3:995–1008.CrossRefGoogle Scholar
  10. Cao, G., Sofic, E., and Prior, R. L. 1997. Antioxidant and prooxidant behavior of flavonoids: structure–activity relationships. Free Radic. Biol. Med. 22:749–760.PubMedCrossRefGoogle Scholar
  11. Chan, T., Galati, G., and O’Brien, P. J. 1999. Oxygen activation during peroxidase catalysed metabolism of flavones or flavanones. Chem.-Biol. Interact. 122:15–25.PubMedCrossRefGoogle Scholar
  12. Cilliers, J. J. L. and Singleton, V. L. 1989. Nonenzymatic autoxidative phenolic browning reactions in a caffeic acid model system. J. Agric. Food Chem. 37:390–396.CrossRefGoogle Scholar
  13. Fukuhara, K., Nakanishi, I., Shimada, T., Ohkubo, K., Miyazaki, K., Hakamata, W., Urano, S., Ozawa, T., Okuda, H., Miyata, N., Ikota, N., and Fukuzumi, S. 2003. A planar catechin analogue as a promising antioxidant with reduced prooxidant activity. Chem. Res. Toxicol. 16:81–86.PubMedCrossRefGoogle Scholar
  14. Fukumoto, L. R. and Mazza, G. 2000. Assessing antioxidant and prooxidant activities of phenolic compounds. J. Agric. Food Chem. 48:3597–3604.PubMedCrossRefGoogle Scholar
  15. Gant, T. W., Ramakrishna, R., Mason, R. P., and Cohen, G. M. 1988. Redox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes. Chem. Biol. Interact. 65:157–173.PubMedCrossRefGoogle Scholar
  16. Grace, S. C., Yamasaki, H., and Pryor, W. A. 1999. Spin stabilizing approach to radical characterization of phenylpropanoid antioxidants: an ESR study of chlorogenic acid oxidation in the horseradish peroxidase, tyrosinase, and ferrylmyoglobin protein radical systems, pp. 435–450, in G. G. Gross, R. W. Hemingway, T. Yoshida, and S. J. Branham (eds.). Plant Polyphenols 2: Chemistry, Biology, Pharmacology, Ecology. Kluwer Academic/Plenum Publishers, New York.Google Scholar
  17. Gross, G. G. 1999. Biosynthesis of hydrolyzable tannins, pp. 799–826, in B. M. Pinto (ed.). Comprehensive Natural Products Chemistry, vol. 3, Elsevier, Amsterdam, the Netherlands.Google Scholar
  18. Guo, Q., Zhao, B., Shen, S., Hou, J., Hu, J., and Xin, W. 1999. ESR study on the structure–activity relationship of tea catechins and their epimers. Biochim. Biophys. Acta 1427:13–23.PubMedGoogle Scholar
  19. Hagerman, A. E. and Butler, L. G. 1991. Tannins and lignins, pp. 355–388, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Second edition. Vol. I: The Chemical Participants. Academic Press, San Diego, CA, USA.Google Scholar
  20. Hagerman, A. E., Riedl, K. M., Jones, G. A., Sovik, K. N., Ritchard, N. T., Hartzfeld, P. W., and Riechel, T. L. 1998. High molecular weight plant polyphenolics (tannins) as biological antioxidants. J. Agric. Food Chem. 40:801–805.Google Scholar
  21. Hagerman, A. E. 1989. Chemistry of tannin–protein complexation, pp. 323–333, in R.W. Hemingway, and J.J. Karchesy, (eds.). Chemistry and Significance of Condensed Tannins. Plenum Publishing Corp., New York, NY, USA.Google Scholar
  22. Hagerman, A. E. and Butler, L. G. 1978. Protein precipitation method for the determination of tannins. J. Agric. Food Chem. 26:809–812.CrossRefGoogle Scholar
  23. Hagerman, A. E. and Robbins, C. T. 1993. Specificity of tannin binding salivary proteins relative to diet selection by mammals. Can. J. Zool. 71:628–633.CrossRefGoogle Scholar
  24. Hatano, T., Edamatsu, R., Hiramatsu, M., Mori, A., Fujiat, Y., Yasuhara, T., Yoshida, T., and Okuda, T. 1989. Effects of the interaction of tannins with co-existing substances. VI. Effects of tannins and related polyphenols on superoxide anion radical, and on 1,1-diphenyl-2-picrylhydrazyl radical. Chem. Pharm. Bull. 37:2016–2021.Google Scholar
  25. Hodnick, W. F., Milosavljevic, E. B., Nelson, J. H., and Pardini, R. S. 1988. Relationship between redox potentials, inhibition of mitochondrial respiration, and production of oxygen radicals by flavonoids. Biochem. Pharmacol. 37:2607–2611.PubMedCrossRefGoogle Scholar
  26. Ito, H., Yamaguchi, K., Kim, T.-H., Khennouf, S., Gharzouli, K., and Yoshida, T. 2002. Dimeric and trimeric hydrolyzable tannins from Quercus coccifera and Quercus suber. J. Nat. Prod. 65:339–345.PubMedCrossRefGoogle Scholar
  27. Johnson, K. S. and Barbehenn, R. V. 2000. Oxygen levels in the gut lumens of herbivorous insects. J. Insect Physiol. 46:897–903.PubMedCrossRefGoogle Scholar
  28. Jovanovic, S. V., Hara, Y., Steenken, S., and Simic, M. G. 1995. Antioxidant potential of gallocatechins. A pulse radiolysis and laser photolysis study. J. Am. Chem. Soc. 117:9881–9888.CrossRefGoogle Scholar
  29. Karonen, M., Loponen, J., Ossipov, V., and Pihlaja, K. 2004. Analysis of procyanidins in pine bark with reversed-phase and normal-phase high-performance liquid chromatography-electrospray ionization mass spectrometry. Anal. Chim. Acta 522:105–112.CrossRefGoogle Scholar
  30. Karonen, M., Ossipov, V., Sinkkonen, J., Loponen, J., Haukioja, E., and Pihlaja, K. 2006. Quantitative analysis of polymeric proanthocyanidins in birch leaves with normal-phase HPLC. Phytochem. Anal. 17:149–156.PubMedCrossRefGoogle Scholar
  31. Martin, J. S., Martin, M. M., and Bernays, E. A. 1987. Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J. Chem. Ecol. 13:605–621.CrossRefGoogle Scholar
  32. McAllister, T. A., Martinez, T., Bae, H. D., Muir, A. D., Yanke, L. J., and Jones, G. A. 2005. Characterization of condensed tannins purified from legume forages: Chromophore production, protein precipitation, and inhibitory effects on cellulose digestion. J. Chem. Ecol. 31:2049–2067.PubMedCrossRefGoogle Scholar
  33. Misra, H. P. and Fridovich, I. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247:3170–3175.PubMedGoogle Scholar
  34. Mukai, K., Mitani, S., Ohara, K., and Nagaoka, S.-I. 2005. Structure–activity relationship of the tocopherol-regeneration reaction by catechins. Free Radic. Biol. Med. 38:1243–1256.PubMedCrossRefGoogle Scholar
  35. Musso, H. 1967. Phenol coupling, pp. 1–94, in W. I. Taylor and A. R. Battersby (eds.). Oxidative Coupling of Phenols. Marcel Dekker, New York, NY, USA.Google Scholar
  36. Northrup, R. R., Dahlgren, R. A., and McColl, J. G. 1998. Polyphenols as regulators of plant–litter–soil interactions in northern California’s pygmy forest: A positive feedback? Biogeochemistry 42:189–220.CrossRefGoogle Scholar
  37. Okuda, T. 1999a. Novel aspects of tannins—renewed concepts and structure–activity relationships. Curr. Org. Chem. 3:609–622.Google Scholar
  38. Okuda, T. 1999b. Antioxidants in herbs: Polyphenols, pp. 393–410, in L. Packer and M. Hiramatsu (eds.). Antioxidant Food Supplements in Human Health. Academic Press, San Diego, CA, USA.Google Scholar
  39. Okuda, T., Yoshida, T., and Hatano, T. 2000. Correlation of oxidative transformations of hydrolyzable tannins and plant evolution. Phytochemistry 55:513–529.PubMedCrossRefGoogle Scholar
  40. Ossipov, V., Haukioja, E., Ossipova, S., Hanhimäki, S., and Pihlaja, K. 2001. Phenolic and phenolic-related factors as determinants of suitability of mountain birch leaves to an herbivorous insect. Biochem. Syst. Ecol. 29:223–240.PubMedCrossRefGoogle Scholar
  41. Ossipova, S., Ossipov, V., Haukioja, E., Loponen, J., and Pihlaja, K. 2001. Proanthocyanidins of mountain birch leaves: quantification and properties. Phytochem. Anal. 12:128–133.PubMedCrossRefGoogle Scholar
  42. Pryor, W. 1986. Oxy-radicals and related species: Their formation, lifetimes, and reactions. Annu. Rev. Physiol. 8:657–667.CrossRefGoogle Scholar
  43. Quideau, S., Varadinova, T., Karagiozova, D., Jourdes, M., Pardon, P., Baudry, C., Genova, P., Diakov, T., and Petrova, R. 2004. Main structural and stereochemical aspects of the antiherpetic activity of nonahydroxyterphenoyl-containing C-glycosidic ellagitannins. Chem. Biodiv. 1:247–258.CrossRefGoogle Scholar
  44. Rice-Evans, C. A., Miller, N. J., and Paganga, G. 1996 Structure–antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20:933–956.PubMedCrossRefGoogle Scholar
  45. Riipi, M., Ossipov, V., Lempa, K., Haukioja, E., Koricheva, J., Ossipova, S., and Pihlaja, K. 2002. Seasonal changes in birch leaf chemistry: Are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380–390.CrossRefGoogle Scholar
  46. Salminen, J.-P. and Lempa, K. 2002. Effects of hydrolysable tannins on a herbivorous insect: fate of individual tannins in insect digestive tract. Chemoecology 12:203–211.CrossRefGoogle Scholar
  47. Salminen, J.-P., Ossipov, V., Haukioja, E., and Pihlaja, K. 2001. Seasonal variation in the content of hydrolyzable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22.PubMedCrossRefGoogle Scholar
  48. Salminen, J.-P., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolyzable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry. J. Chromatogr. A 864:283–291.CrossRefGoogle Scholar
  49. Salminen, J.-P., Roslin, T., Karonen, M., Sinkkonen, J., Pihlaja, K., and Pulkkinen, P. 2004. Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J. Chem. Ecol. 30:1675–1693.CrossRefGoogle Scholar
  50. Simic, M. G. and Jovanovic, S. V. 1994. Inactivation of oxygen radicals by dietary phenolic compounds in anticarcinogenesis, pp. 20–33, in C.-T. Ho, T. Osawa, M.-T. Huang, and R. T. Rosen (eds.). Food Phytochemicals for Cancer Prevention II. American Chemical Society, Washington DC, USA.Google Scholar
  51. 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 anti-herbivore chemistry. Insect Biochem. Mol. Biol. 24:943–953.CrossRefGoogle Scholar
  52. Swain, T. 1979. Tannins and lignins, pp. 657–682, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York, NY, USA.Google Scholar
  53. Thiboldeaux, R. L., Lindroth, R. L. and Tracy, J. W. 1998. Effects of juglone (5-hydroxy-1,4-naphthoquinone) on midgut morphology and glutathione status in Saturniid moth larvae. Comp. Biochem. Physiol. 120:481–487.Google Scholar
  54. Vuorela, S., Kreander, K., Karonen, M., Nieminen, R., Hämäläinen, M., Galkin, A., Laitinen, L., Salminen, J.-P., Moilanen, E., Pihlaja, K., Vuorela, H., Vuorela, P., and Heinonen, M. 2005. Preclinical evaluation of rapeseed, raspberry, and pine bark phenolics for health related effects. J. Agric. Food Chem. 53:5922–5931.PubMedCrossRefGoogle Scholar
  55. Waite, J. H. 1976. Calculating extinction coefficients for enzymatically produced O-quinones. Anal. Biochem. 75:211–218.PubMedCrossRefGoogle Scholar
  56. Wilkinson, L. 2000. SYSTAT: The system for Statistics. SYSTAT, Inc, Evanston, IL.Google Scholar
  57. Wright, J. S., Carpenter, D. J., McKay, D. J., and Ingold, K. U. 1997. Theoretical calculation of substituent effects on the O–H bond strength of phenolic antioxidants related to vitamin E. J. Am. Chem. Soc. 119:4245–4252.CrossRefGoogle Scholar
  58. Yoshioka, H., Sugiura, K., Kawahara, R., Fujita, T., Makino, M., Kamiya, M., and Tsuyuma, S. 1991. Formation of radicals and chemiluminescence during the autoxidation of tea catechins. Agric. Biol. Chem. 55:2717–2723.Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Raymond V. Barbehenn
    • 1
  • Christopher P. Jones
    • 1
  • Ann E. Hagerman
    • 2
  • Maarit Karonen
    • 3
  • Juha-Pekka Salminen
    • 3
  1. 1.Departments of Molecular, Cellular and Developmental Biology and Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of Chemistry and BiochemistryMiami UniversityOxfordUSA
  3. 3.Laboratory of Organic Chemistry and Chemical BiologyDepartment of Chemistry, University of TurkuTurkuFinland

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