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Seasonal Variation in the Content of Hydrolyzable Tannins, Flavonoid Glycosides, and Proanthocyanidins in Oak Leaves

Abstract

Oaks have been one of the classic model systems in elucidating the role of polyphenols in plant–herbivore interactions. This study provides a comprehensive description of seasonal variation in the phenolic content of the English oak (Quercus robur). Seven different trees were followed over the full course of the growing season, and their foliage repeatedly sampled for gallic acid, 9 individual hydrolyzable tannins, and 14 flavonoid glycosides, as well as for total phenolics, total proanthocyanidins, carbon, and nitrogen. A rare dimeric ellagitannin, cocciferin D2, was detected for the first time in leaves of Q. robur, and relationships between the chemical structures of individual tannins were used to propose a biosynthetic pathway for its formation. Overall, hydrolyzable tannins were the dominant phenolic group in leaves of all ages. Nevertheless, young oak leaves were much richer in hydrolyzable tannins and flavonoid glycosides than old leaves, whereas the opposite pattern was observed for proanthocyanidins. However, when quantified as individual compounds, hydrolyzable tannins and flavonoid glycosides showed highly variable seasonal patterns. This large variation in temporal trends among compounds, and a generally weak correlation between the concentration of any individual compound and the total concentration of phenolics, as quantified by the Folin–Ciocalteau method, leads us to caution against the uncritical use of summary quantifications of composite phenolic fractions in ecological studies.

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REFERENCES

  1. Brahamson, W. G., Hunter, M. D., Melika, G., and Price, P. W. 2003. Cynipid gall-wasp communities correlate with oak chemistry. J. Chem. Ecol. 29:209–223.

    Google Scholar 

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

    Google Scholar 

  3. Appel, H.M., Venor, H. L., D'Ascenzo, M., Siska, E., and Schultz, J. C. 2001. Limitations of folin assays of foliar phenolics in ecological studies. J. Chem. Ecol. 27:761–778.

    Google Scholar 

  4. Ayres, M. P., Clausen, T. P., Mclean, S. F., Redman, A. M., and Reichardt, P. B. 1997. Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712.

    Google Scholar 

  5. Cadahĺa, E., Varea, S., MuÑoz, L., FernÁndez De SimÓn, B., and Garcĺa-Vallejo, M. C. 2001.Evolution of ellagitannins in Spanish, French, and American oak woods during natural seasoning and toasting. J. Agric. Food Chem. 49:3677–3684.

    Google Scholar 

  6. Clausen, T. P., Provenza, F. D., and Burritt, E. A. 1990. Ecological implications of condensed tannin structure: A case study. J. Chem. Ecol. 16:2381–2392.

    Google Scholar 

  7. Close, D. C. and Mcarthur, C. 2002. Rethinking the role of many plant phenolics--Protection from photodamage not herbivores. Oikos 99:166–172.

    Google Scholar 

  8. Conde, E., Cadahĺa, E., Garcĺa-Vallejo, M. C., and Fern´andez De Sim´on, B. 1998. Polyphenolic composition of Quercus suber cork from different Spanish provenances. J. Agric. Food Chem. 46:3166–3171.

    Google Scholar 

  9. Crawley, M. and Akhteruzzaman, M. 1988. Individual variation in the phenology of oak trees and its consequences for herbivorous insects. Func. Ecol. 2:409–415.

    Google Scholar 

  10. Dudt, J. F. and Shure, D. J. 1994. The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98.

    Google Scholar 

  11. Faeth, S. 1986. Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494.

    Google Scholar 

  12. Feeny, P. P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581.

    Google Scholar 

  13. Feldman, K. S., Sambandam, A., Lemon, S.T., Nicewonger, R.B., Long, G. S., Battaglia, D.F., Ensel, S.M., and Laci, M. A. 1999. Binding affinities of gallotannin analogs with bovine serum albumin, ramifications for polyphenol-protein molecular recognition. Phytochemistry 51:867–872.

    Google Scholar 

  14. Fernández De Simón, B., Cadahĺa, E., Conde, E., and Garcĺa-Vallejo, M. C. 1999. Evolution of phenolic compounds of Spanish oak wood during natural seasoning. First results. J. Agric. Food Chem. 47:1687–1694.

    Google Scholar 

  15. Fisher, A. E. I., Hartley, S. E., and Young, M. 2000. Direct and indirect competitive effects of foliage feeding guilds on the performance of the birch leaf-miner Eriocrania. J. Anim. Ecol. 69:165–176.

    Google Scholar 

  16. Forkner, R.E., Marquis, R.J., and Lill, J. T. 2004. Feeny revisited: Condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol. Entomol. 29:174–187.

    Google Scholar 

  17. Gross, G. G. 1999. Biosynthesis of hydrolyzable tannins, pp. 799–826, in B. M. Pinto (ed.). Compre-hensive Natural Products Chemistry, Vol. 3. Elsevier, Amsterdam.

    Google Scholar 

  18. GrundhÖfer, P., Niemetz, R., Schilling, G., and Gross, G. G. 2001. Biosynthesis and subcellular distribution of hydrolyzable tannins. Phytochemistry 57:915–927.

    Google Scholar 

  19. Haslam, E. 1992. Gallic acid and its metabolites, pp. 169–194, in R. W. Hemingway and P. E. Laks (eds.). Plant Polyphenols. Plenum Press, New York.

    Google Scholar 

  20. Hatano, T., Kira, R., Yoshizaki, M., and Okuda, T. 1986. Seasonal changes in the tannins of Liquidambar formosana reflecting their biogenesis]. Phytochemistry 25:2787–2789.

    Google Scholar 

  21. Hatano, T., Okonogi, A., and Okuda, T. 1992. Oligomeric hydrolyzable tannins from Liquidambar formosana and spectral analysis of the orientation of valoneoyl groups in their molecules, pp. 195–207, in R. W. Hemingway and P. E. Laks (eds.). Plant Polyphenols. Plenum Press, New York.

    Google Scholar 

  22. Haukioja, E. 2003. Putting the insect into the birch–insect interaction. Oecologia 136:161–168.

    Google Scholar 

  23. Haukioja, E., Ossipov, V., and Lempa, K. 2002. Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomol. Exp. Appl. 104:125–136.

    Google Scholar 

  24. Helm, R.F., Zhentian, L., Ranatunga, T., Jervis, J., and Elder, T. 1999. Towards understanding monomeric ellagitannin biosynthesis, pp. 83–99, in G. G. Gross, R. W. Hemingway, and T. Yoshida (eds.). Plant Polyphenols, 2: Chemistry, Biology, Pharmacology, Ecology. Kluwer Academic/Plenum, New York.

    Google Scholar 

  25. Henriksson, J., Haukioja, E., Ossipov, V., Ossipova, S., Sillanpää, S., Kapari, L., and Pihlaja,K. 2003. Effects of host shading on consumption and growth of the geometrid Epirrita autumnata:Interactive roles of water, primary and secondary compounds. Oikos 103:3–16.

    Google Scholar 

  26. Herms, D. A. and Mattson, W. J. 1992. The dilemma of plants: To grow or defend. Q. Rev. Biol. 67:283–335.

    Google Scholar 

  27. HervÉdu Penhoat, C. L. M., Michon, V. M. F., Ohassan, A., Peng, S., Scalbert, A., and Gage, D. 1991a. Roburin A, a dimeric ellagitannin from heartwood of Quercus robur. Phytochemistry 30:329–332.

    Google Scholar 

  28. HervÉ du penhoat, C. L. M., Michon, V. M. F., Peng, S., Viriot, C., Scalbert, A.,and Gage, D. 1991b. Structural elucidation of new dimeric ellagitannins from Quercus robur L. J. Chem. Soc., Perkin Trans 1, 1653–1660.

    Google Scholar 

  29. Hoffman, G. and Lyr, H. 1973. Charakerisierung des Wachstumsverhaltens von Pflantzen durch Wachstumsschemata. Flora 162:81–98.

    Google Scholar 

  30. Inbar, M., Doostdar, H., and Maye, R. 2001. Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94:228–235.

    Google Scholar 

  31. Inoue, K. and Hagerman, A. 1988. Determination of gallotannin with rhodanine. Anal. Biochem. 169:363–369.

    Google Scholar 

  32. 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.

    Google Scholar 

  33. Jalas, J. and Suominen, J. 1976. Atlas Florae Europaea. Distribution of vascular plants in Europe. Quercus robur, Map 301. Committee for Mapping the Flora of Europe and Societatis Biologica Fennica, Helsinki.

    Google Scholar 

  34. Kause, A., Ossipov, V., Haukioja, E., Lempa, K., HanhimÄki, S., and Ossipova, S. 1999. Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112.

    Google Scholar 

  35. Kilkowski, W. J. and Gross, G. G. 1999. Color reaction of hydrolyzable tannins with Bradford reagent, Coomassie brilliant blue. Phytochemistry 51:363–366.

    Google Scholar 

  36. Kraus, T. E. C., Yu, Z., Preston, C.M., Dahlgren, R. A., and Zasoski, R. J. 2003. Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins. J. Chem. Ecol. 29:703–730.

    Google Scholar 

  37. Lill, J. T. and Marquis, R. J. 2001. The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126:418–428.

    Google Scholar 

  38. MÄmmelÄ, P., Savolainen, H., Lindroos, L., Kangas, J., and Vartiainen, T. 2000. Analysis of oak tannins by liquid chromatography–electrospray ionisation mass spectrometry. J. Chromatogr. A 891:75–83.

    Google Scholar 

  39. Masson, G., Puech, J.-L., and Moutounet, M. 1994. Localization of the ellagitannins in the tissues of Quercus robur and Quercus petraea woods. Phytochemistry 37:1245–1249.

    Google Scholar 

  40. Mattson, W. J. and Scriber, J. M. 1987. Nutritional ecology of insect folivores of woody plants: Nitrogen, water, fiber, and mineral considerations, pp. 105–146, in F. Slansky Jr. and J. G. Rodriquez (eds.), Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates. Wiley, New York.

    Google Scholar 

  41. Maufette, Y. and Oechel, W. C. 1989. Seasonal variation in leaf chemistry of the coast live oak Quer-cus agrifolia and implications for the California oak moth Phryganidia californica. Oecologia 79:439–445.

    Google Scholar 

  42. Mckinnon, M.L., Quiring, D.T., and Bauce, E. 1999. Influence of tree growth rate, shoot size an foliar chemistry on the abundance and performance of a galling adelgid. Func. Ecol. 13:859–867.

    Google Scholar 

  43. Mosedale, J.R., Feuillat, F., Baumes, R., Dupouey, J.-L., and Puech, J.-L. 1998. Variability of wood extractives among Quercus robur and Quercus petraea trees from mixed stands and their relation to wood anatomy and leaf morphology. Can. J. Forest Res. 28:994–1006.

    Google Scholar 

  44. NiemelÄ, P. 1983. Seasonal patterns in the incidence of specialism: Macrolepidopteran larvae on Finnish deciduous trees. Ann. Zool. Fenn. 20:199–202.

    Google Scholar 

  45. NiemelÄ, P. and Haukioja, E. 1982. Seasonal patterns in species richness of herbivores: Macrolepi-dopteran larvae on Finnish deciduous trees. Ecol. Entomol. 7:169–175.

    Google Scholar 

  46. Niemetz, R., Schilling, G., and Gross, G. G. 2001. Ellagitannin biosynthesis: Oxidation of pentagal-loylglucose to tellimagrandin II by an enzyme from Tellima grandiflora leaves. Chem. Commun.2001:35–36.

  47. Nurmi, K., Ossipov, V., Haukioja, E., and Pihlaja, K. 1996. Variation of total phenolic content and individual low-molecular-weight phenolics in foliage of mountain birch trees (Betula pubescens ssp. tortuosa). J. Chem. Ecol. 22:2023–2040.

    Google Scholar 

  48. Okuda, T., Yoshida, T., Hatano, T., Yazaki, K., and Ashida, M. 1982. Ellagitannins of the casuarinaceae, stachyuraceae and myrtaceae. Phytochemistry 21:2871–2874.

    Google Scholar 

  49. Ossipov, V., Nurmi, K., Loponen, J., Haukioja, E., and Pihlaja, K. 1996. HPLC separation and identification of phenolic compounds from leaves of Betula pubescens and Betula pendula. J. Chromatogr. A 721:59–68.

    Google Scholar 

  50. Ossipov, V., Nurmi, K., Loponen, J., Prokopiev, N., Haukioja, E., and Pihlaja, K. 1995. HPLC isolation and identification of flavonoids from white birch Betula pubescens leaves. Biochem. Syst. Ecol. 23:213–222.

    Google Scholar 

  51. 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.

    Google Scholar 

  52. Ozawa, T., Lilley, T. H., and Haslam, E. 1987. Polyphenol interactions: Astringency and the loss of astringency in ripening fruit. Phytochemistry 26:2937–2942.

    Google Scholar 

  53. 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.

    Google Scholar 

  54. 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 

  55. Salminen, J.-P. 2002. Birch leaf hydrolysable tannins: Chemical, biochemical and ecological aspects.PhD Dissertation, University of Turku, Finland.

    Google Scholar 

  56. Salminen, J.-P. 2003. Effects of sample drying and storage, and choice of extraction solvent and analysis method on the yield of birch leaf hydrolysable tannins. J. Chem. Ecol. 29:1289–1305.

    Google Scholar 

  57. Salminen, J.-P. and Lempa, K. 2002. Effects of hydrolysable tannins on an herbivorous insect: Fate of individual tannins in insect digestive tract. Chemoecology 12:203–211.

    Google Scholar 

  58. Salminen, J.-P., Ossipov, V., Haukioja, E., and Pihlaja, K. 2001. Seasonal variation in the content of hydrolysable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22.

    Google Scholar 

  59. Salminen, J.-P., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolysable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry. J. Chromatogr. A 864:283–291.

    Google Scholar 

  60. Scalbert, A. and Haslam, E. 1987. Plant polyphenols and chemical defense. Part 2: Polyphe-nols and chemical defense of the leaves of Quercus robur. Phytochemistry 26:3191–3195.

    Google Scholar 

  61. Scalbert, A., Monties, B., and Favre, J.-M. 1988. Polyphenols of Quercus robur: Adult tree and in vitro grown calli and shoots. Phytochemistry27:3483–3488.

    Google Scholar 

  62. Schultz, J.C. and Baldwin, I. T. 1982. Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science217:149–151.

    Google Scholar 

  63. Tikkanen, O.-P. and Julkunen-Tiitto, R. 2003. Phenological variation as protection against defoli-ating insects: The case of Quercus robur and Operophtera brumata. Oecologia136:244–251.

    Google Scholar 

  64. Viriot, C., Scalbert, A., Herv´e Dupenhoat, C.L.M., Rolando, C., and Moutounet, M. 1994.Methylation, acetylation and gel permeation of hydrolysable tannins. J. Chromatogr. A662: 77–85.

    Google Scholar 

  65. Vivas, N., Laguerre, M., Glories, Y., Bourgeois, G., and Vitry, C. 1995. Structure simulation of two ellagitannins from Quercus robur L. Phytochemistry39:1193–1199.

    Google Scholar 

  66. Wilson, T. C. and Hagerman, A. E. 1990. Quantitative determination of ellagic acid. J. Agric. Food Chem.38:1678–1683.

    Google Scholar 

  67. Yoshida, T., Hatano, T., Kuwajima, T., and Okuda, T. 1992. Oligomeric hydrolyzable tannins--Their 1 H NMR spectra and partial degradation. Heterocycles33:463–482.

    Google Scholar 

  68. Zhentian, L., Jervis, J., and Helm, R. F. 1999. C-glycosidic ellagitannins from white oak heartwood and callus tissues. Phytochemistry51:751–756.

    Google Scholar 

  69. Zucker, W. V. 1983. Tannins: Does structure determine function? An ecological perspective. Am. Nat. 121:335–365.

    Google Scholar 

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Salminen, JP., Roslin, T., Karonen, M. et al. Seasonal Variation in the Content of Hydrolyzable Tannins, Flavonoid Glycosides, and Proanthocyanidins in Oak Leaves. J Chem Ecol 30, 1693–1711 (2004). https://doi.org/10.1023/B:JOEC.0000042396.40756.b7

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  • Quercus robur
  • hydrolyzable tannins
  • ellagitannins
  • flavonoid glycosides
  • proanthocyanidins
  • HPLC
  • quantification of phenolics
  • biosynthetic pathways
  • compound-specific patterns