Journal of Chemical Ecology

, Volume 33, Issue 9, pp 1721–1732 | Cite as

Phenolic Chemistry of Coast Live Oak Response to Phytophthora ramorum Infection

  • Frances S. Ockels
  • Alieta EylesEmail author
  • Brice A. McPherson
  • David L. Wood
  • Pierluigi Bonello


Since the mid 1990s, Phytophthora ramorum has been responsible for the widespread mortality of tanoaks, as well as several oak species throughout California and Oregon forests. However, not all trees die, even in areas with high disease pressure, suggesting that some trees may be resistant to the pathogen. In this study, the chemical basis of host resistance was investigated. Three field experiments were carried out in California between December 2004 and September 2005. The levels of nine phenolic compounds (gallic acid, catechin, tyrosol, a tyrosol derivative, ellagic acid, and four ellagic acid derivatives) extracted from the phloem of trees that had been either artificially inoculated with P. ramorum or trees putatively infected with P. ramorum (based on canker symptoms) were quantified by high-performance liquid chromatography (HPLC). Significant differences in phenolic profiles were found between phloem sampled from the active margins of cankers, healthy phloem from asymptomatic trees, and phloem sampled 60 cm away from canker sites, although the magnitude and direction of the responses was not consistent across all experiments. Concentrations of gallic acid, tyrosol, and ellagic acid showed the greatest differences in these different tissues, but varied considerably across treatments. Gallic acid and tyrosol were tested in in vitro bioassays and showed strong dose-dependent inhibitory effects against P. ramorum, P. cinnamomi, P. citricola, and P. citrophthora. These results suggest that phloem chemistry varies in response to pathogen infection in California coast live oak populations and that changes in phloem chemistry may be related to apparently resistant phenotypes observed in the field.


Sudden oak death Resistance Quercus agrifolia Canker In vitro bioassay 



The authors would like to thank Nadir Erbilgin, Tom Gordon, Gabriela Ritok-Owens, and Pavel Svihra for the assistance in the field and the lab, David Rizzo for providing the P. ramorum isolates, and Matthew Dileo for conducting the bioassay with P. ramorum. Special thanks to Larry Madden for the assistance with the statistical analyses and Duan Wang for conducting the fungal bioassays with P. cinnamomi, P. citricola, and P. citrophthora. Access to research sites was provided by Marin County Open Space District and China Camp State Park. Salaries and research support were provided by state funds appropriated to the Ohio Agricultural Research and Development Center, the Ohio State University, and the U.S. Forest Service (04-CA-11244225-432).


  1. Barry, K. M., Davies, N. W., and Mohammed, C. L. 2001. Identification of hydrolysable tannins in the reaction zone of Eucalyptus nitens wood by high performance liquid chromatography-electrospray ionisation mass spectrometry. Phytochem. Anal. 12:120–127.PubMedCrossRefGoogle Scholar
  2. Bennett, R. and Wallsgrove, R. M. 1994. Tansley Review No. 72: Secondary metabolites in plant defense mechanisms. New Phytol. 127:617–633.CrossRefGoogle Scholar
  3. Blodgett, J. T., Eyles, A., and Bonello, P. 2007. Organ-dependent induction of systemic resistance and systemic susceptibility in Pinus nigra inoculated with Sphaeropsis sapinea and Diplodia scrobiculata. Tree Physiol. 27:511–517.PubMedGoogle Scholar
  4. Bonello, P. and Blodgett, J. T. 2003. Pinus nigra–Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol. Mol. Plant Pathol. 63:249–261.CrossRefGoogle Scholar
  5. Brown, A. V. and Brasier, C. M. 2007. Colonization of tree xylem by Phytophthora ramorum, P. kernoviae and other Phytophthora species. Plant Pathol. 56:227–241.CrossRefGoogle Scholar
  6. Davidson, J. M., Werres, S., Garbelotto, M., Hansen, E. M., and Rizzo, D. M. 2003. Sudden oak death and associated diseases caused by Phytophthora ramorum. Plant Health Progress Online. DOI  10.1094/PHP-2003-0707-01-DG.
  7. Davidson, J. M., Wickland, A. C., Patterson, H. A., Falk, K. R., and Rizzo, D. M. 2005. Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95:587–596.CrossRefPubMedGoogle Scholar
  8. Del Rio, J. A., Baidez, A. G., Botia, J. M., and Ortuno, A. 2003. Enhancement of phenolic compounds in olive plants (Olea europaea L.) and their influence on resistance against Phytophthora sp. Food Chem. 83:75–78.CrossRefGoogle Scholar
  9. De Simon, B. F., Sanz, M., Cadahia, E., Poveda, P., and Broto, M. 2006. Chemical characterization of oak heartwood from Spanish forests of Quercus pyrenaica (Wild.). Ellagitannins, low molecular weight phenolic, and volatile compounds. J. Agric. Food Chem. 54:8314–8321.CrossRefGoogle Scholar
  10. Dodd, R. S., Huberli, D., Douhovnikoff, V., Harnik, T. Y., Afzal-Rafii, Z., and Garbelotto, M. 2005. Is variation in susceptibility to Phytophthora ramorum correlated with population genetic structure in coast live oak (Quercus agrifolia)? New Phytol. 165:203–214.PubMedCrossRefGoogle Scholar
  11. Evensen, P. C., Solheim, H., Hoiland, K., and Stenersen, J. 2000. Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. For. Pathol. 30:97–108.Google Scholar
  12. Eyles, A., Davies, N. W., Yuan, Z. Q., and Mohammed, C. 2003. Host responses to natural infection by Cytonaema sp. in the aerial bark of Eucalyptus globulus. For. Path. 33:317–331CrossRefGoogle Scholar
  13. Feucht, W. and Treutter, D. 1999. The role of flavan-3-ols in plant defense, pp. 307–338, in K. M. M. Dakshini and C. L. Foy (eds.). Principles and Practices in Plant Ecology: Allelochemical Interactions. CRC, Boca Raton.Google Scholar
  14. Field, J. A. and Lettinga, G. 1992. Toxicity of tannic compounds to microorganisms, pp. 673–692, in R. W. Hemingway and P. E. Laks (eds.). Plant Polyphenols. Synthesis, Properties, Significance. Plenum, New York.Google Scholar
  15. Garbelotto, M., Svihra, P., and Rizzo, D. M. 2001. Sudden oak death syndrome fells 3 oak species. Calif. Agric. 55:9–19.CrossRefGoogle Scholar
  16. 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. 46:1887–1892.CrossRefGoogle Scholar
  17. Hart, J. H. and Hillis, W. E. 1972. Inhibition of wood-rotting fungi by ellagitannins in the heartwood of Quercus alba. Phytopathology 62:620–626.Google Scholar
  18. Hart, J. H. and Hillis, W. E. 1974. Inhibition of wood-rotting fungi by stilbenes and other polyphenols in Eucalyptus sideroxylon. Phytopathology 64:939–948.CrossRefGoogle Scholar
  19. Hillis, W. E. 1999. Heartwood and Tree Exudates. Springer, Berlin.Google Scholar
  20. Kawamoto, H., Mizutani, K., and Nakatsubo, F. 1997. Binding nature and denaturation of protein during interaction with galloylglucose. Phytochemistry 46:473–478.PubMedCrossRefGoogle Scholar
  21. Klumpers, J., Scalbert, A., and Janin, G. 1994. Ellagitannins in European oak wood: polymerization during wood aging. Phytochemistry 36:1249–1252.CrossRefGoogle Scholar
  22. Malterud, K. E., Bremnes, T. E., Faegri, A., Moe, T., and Dugstad, E. K. S. 1985. Flavonoids from the wood of Salix caprea as inhibitors of wood-destroying fungi. J. Nat. Prod. 48:559–563.CrossRefGoogle Scholar
  23. Mammela, P., Savolainen H, Lindroos L, Kangas, J., and Vartiainen, T. 2000. Analysis of oak tannins by liquid chromatography-electrospray ionisation mass spectrometry. J. Chromatogr. 891:75–83.CrossRefGoogle Scholar
  24. McPherson, B. A., Mori, S. R., Wood, D. L., Storer, A. J., Svihra, P., Maggi Kelly N., and Standiford, R. B. 2005. Sudden oak death in California: Disease progression in oaks and tanoaks. For. Ecol. Manag. 213:71–89.CrossRefGoogle Scholar
  25. Okamura, H., Mimura, A., Yakou, Y., Niwano, M., and Takahara, Y. 1993. Antioxidant activity of tannins and flavonoids in a Eucalyptus rostrata. Phytochemistry 33:557–561.CrossRefGoogle Scholar
  26. Okuda, T., Yoshida, T., and Hatano, T. 1995. Hydrolysable tannins and related polyphenols. Prog. Chem. Org. Nat. Prod. 66:1–117.Google Scholar
  27. Ostrofsky, W. D., Shortle, W. C., and Blanchard, R. O. 1984. Bark phenolics of American beech (Fagus grandifolia) in relation to the beech bark disease. Eur. J. For. Pathol. 14:52–59.CrossRefGoogle Scholar
  28. Pavlik, B. M., Muick, P. C., Johnson, S. G., and Popper, M. 1991. Oaks of California. Cachuma Press, Los Olivos, CA.Google Scholar
  29. Pearce, R. B. 1996. Antimicrobial defences in the wood of living trees. New Phytol. 132:203–233.CrossRefGoogle Scholar
  30. Rizzo, D. M. and Garbelotto, M. 2003. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1:197–204.CrossRefGoogle Scholar
  31. Rizzo, D. M., Garbelotto, M., Davidson, J. M., Slaughter, G. W., and Koike, S. T. 2002. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis. 86:205–214.CrossRefGoogle Scholar
  32. Rizzo, D. M., Garbelotto, M., and Hansen, E. A. 2005. Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu. Rev. Phytopathol. 43:309–335.PubMedCrossRefGoogle Scholar
  33. 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. 30:1693–1711.PubMedCrossRefGoogle Scholar
  34. Schmitthenner, A. F. and Bhat, R. G. 1994. Useful methods for studying Phytophthora in the laboratory. Special Circular 143: Ohio Agricultural Research and Development Center (OARDC).Google Scholar
  35. Svihra, P. 1999. Sudden death of tanoak, Lithocarpus densiflorus. University of California Cooperative Extension Pest Alert no. 1, June, 2 p.Google Scholar
  36. Viiri, H., Annila, E., Kitunen, V., and Niemela, P. 2001. Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15:112–122.CrossRefGoogle Scholar
  37. Vivas, N., Nonier, M. F., De Gaulejac, N. V., and De Boissel, I. P. 2004. Occurrence and partial characterization of polymeric ellagitannins in Quercus petraea Liebl. and Q. robur L. wood. C. R. Chemie. 7:945–954.Google Scholar
  38. Werres, S., Marwitz, R., Veld, W., De Cock, A., Bonants, P. J. M., De Weerdt, M., Themann, K., Ilieva, E., and Baayen, R. P. 2001. Phytophthora ramorum sp nov., a new pathogen on Rhododendron and Viburnum. Mycol. Res. 105:1155–1165.Google Scholar
  39. Woodward, S. and Pearce, R. B. 1988. The role of stilbenes in resistance of Sitka spruce (Picea sitchensis (Bong.) Carr.) to entry of fungal pathogens. Physiol. Mol. Plant Pathol. 33:127–149.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Frances S. Ockels
    • 1
  • Alieta Eyles
    • 1
    Email author
  • Brice A. McPherson
    • 2
  • David L. Wood
    • 3
  • Pierluigi Bonello
    • 1
  1. 1.Department of Plant PathologyThe Ohio State UniversityColumbusUSA
  2. 2.Center for Forestry and Integrated Hardwood Rangeland Management Program, Department of Environmental Science, Policy, and ManagementUniversity of CaliforniaBerkeleyUSA
  3. 3.Division of Organisms and Environment, Department of Environmental Science, Policy and ManagementUniversity of CaliforniaBerkeleyUSA

Personalised recommendations