Types of Ectomycorrhiza of Mature Beech and Spruce at Ozone-Fumigated and Control Forest Plots



In the Kranzberg forest near Freising (Germany) a novel “Free-Air Canopy O3 Exposure” system has been employed for analysing O3-induced responses from sub-cellular to ecosystem levels that are relevant for carbon balance and CO2 demand of 60-year-old beech trees. The below-ground ectomycorrhizal community was studied in two-fold ambient O3 concentrations (five cores per sampling) and in a control plot with an ambient O3 concentration (four cores per sampling). Five samplings were taken throughout two vegetation seasons (2003 and 2004). Types of ectomycorrhiza were determined by their morphological, anatomical and molecular characteristics and quantified by counting. The total number of mycorrhizal fine roots was higher at the fumigated plot as compared with the control site. The numbers of ectomycorrhizal types at the fumigated and control plots were 28 and 26, respectively. Cenococcum geophilum was present in all soil cores at all sampling times with a significant increase in abundance under ozone-fumigated trees. Other mycorrhizal types present at higher abundance at the fumigated than at the control plot were identified as Russula densiflora, R. fellea, R. illota, Tuber puberulum, Lactarius sp. 2 and Russula sp. 2. Some mycorrhizal types were present exclusively at the fumigated plot (Fagirhiza fusca, F. setifera, Lactarius acris, Piceirhiza nigra and Russula sp. 1). A possible ecological role for the abundant types of ectomycorrhiza and their putative application in bio-indication is discussed.


beech ectomycorrhizal types elevated ozone mature forest PCR-RFLP sequencing spruce 


  1. Agerer, R. (1987–2002). Colour atlas of ectomycorrhizae. Schwäbisch Gmünd, Munich: Einhorn-Verlag.Google Scholar
  2. Agerer, R. (1991). Characterisation of ectomycorrhiza. In J. R. Norris, D. J. Read, & A. K. Varma (Eds.), Methods in microbiology, 23 (pp. 25–73). London: Academic Press.Google Scholar
  3. Agerer, R., Danielson, R. M., Egli, S., Ingleby, K., Luoma, D., & Treu, R. (2001). Descriptions of ectomycorrhizae. Schwäbisch Gmünd, Munich: Einhorn-Verlag.Google Scholar
  4. Agerer, R., & Rambold, G. (2004–2005) [first posted on 2004–06–01; most recent update: 2005–07–15]. DEEMY - An Information System for Characterization and Determination of Ectomycorrhizae, http://www.deemy.de, Ludwig-Maximilians University, Munich.
  5. Al Sayegh Petkovšek, S. (2000). Types of ectomycorrhizae from the forest research plots in Kočevska Reka and Zavodnje. In H. Kraigher & I. Smolej (Eds.), The rhizosphere (pp. 119–153). Professional and Scientific Works, Slovenian Forestry Institute, Ljubljana.Google Scholar
  6. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programmes. Nucleic Acids Research, 25, 3389–3402.CrossRefGoogle Scholar
  7. Andersen, C. P. (2003). Source-sink balance and carbon allocation below ground in plants exposed to ozone (Tansley review). New Phytologist, 157, 213–228.CrossRefGoogle Scholar
  8. Beenken, L. (2004). Die Gattung Russula Untersuchung zu ihrer Systematik anhand von Ektomykorrhizen. Ph.D. Thesis, Faculty of Biology, Ludwig-Maximilians University, Munich.Google Scholar
  9. Berg, B., & Gronbach, E. (1988). Piceirhiza nigra. In R. Agerer (Ed.), Colour atlas of ectomycorrhizae. Schwäbisch Gmünd: Einhorn-Verlag, plate 19.Google Scholar
  10. Blaschke, H. (1987). Vorkommen und Charakterisierung der Ektomykorrhizaassoziation Tuber puberulum mit Picea abies. Zeitschrift für Mykologie, 53, 283–288Google Scholar
  11. Bon, M. (1988). Pareys Buch der Pilze (p. 362). Hamburg und Berlin: Verlag Paul Payer.Google Scholar
  12. Bortier, K., Ceulemans, R., & De Temmerman, L. (1999). Effects of tropospheric ozone on woody plants. In S. B. Agrawal & M. Agrawal (Eds.), Environmental pollution and plant response (pp. 153–182). Boca Raton: Lewis.Google Scholar
  13. Brand, F. (1991). Ektomykorrhizen an Fagus sylvatica: Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung. Libri Botanici, 2, 1–229Google Scholar
  14. Coleman, M. D., Dickson, R. E., Isebrands, J. G., & Karnosky, D. F. (1995). Carbon allocation and partitioning in aspen clones varying in sensitivity to tropospheric ozone. Tree Physiology, 15, 593–604.Google Scholar
  15. Coleman, M. D., Dickson, R. E., Isebrands, J. G., & Karnosky, D. F. (1996). Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone. Tree Physiology, 16, 145–152.Google Scholar
  16. Courtecuisse, R., & Duhem, B. (1995). Mushrooms and toadstools of Britain and Europe, collins field guide (p. 480). London: Harper Collins.Google Scholar
  17. Douhan, G. W., & Rizzo, D. M. (2005). Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytologist, 166, 263–271.CrossRefGoogle Scholar
  18. Gardes, M., & Bruns, T. D. (1993). ITS primers with enchanced specificity for basidiomycetes - Application to the identification of ectomycorrhizae and rusts. Molecular Ecology, 2, 113–118.Google Scholar
  19. Gerhardt, E. (1997). Der grosse BLV-Pilzführer für unterwegs: über 1200 Arten, über 1000 Farbfotos (p. 718). München, Wien, Zürich: BLV Verlagsgesellschaft.Google Scholar
  20. Grebenc, T. (2005). Types of ectomycorrhizae in beech (Fagus sylaatica L.) in natural and managed forest. Ph.D. Thesis, Biotechnical Faculty, University of Ljubljana.Google Scholar
  21. Grebenc, T., Piltaver, A., & Kraigher H. (2000). Establishment of a PCR-RFLP library for Basidiomycetes, Ascomycetes and their ectomycorrhizae in Picea abies (L.) Karst. Phyton Annals of Botany, 40, 79–82.Google Scholar
  22. Grimond, P. A. D. (1998). Taxotron user’s manual (p. 125). Paris: Institute Pasteur.Google Scholar
  23. Holmes, W. E., Zak, D. R., Pregitzer, K. S., & King, J. S. (2003). Soil nitrogen transformations under Populus tremuloides, Betula papyrifera and Acer saccharum following 3 years exposure to elevated CO2 and O3. Global Change Biolology, 9, 1743–1750.CrossRefGoogle Scholar
  24. Kårén, O., Hogberg, N., Dahlberg, A., Jonsson, L., & Nylund, J. E. (1997). Inter- and intraspecific variation in the ITS region of rDNA of ectomycorrhizal fungi in Fennoscandia as detected by endonuclease analysis. New Phytologist, 136, 313–325.CrossRefGoogle Scholar
  25. King, J. S., Pregitzer, K. S., Zak, D. R., Karnosky, D. F., Isebrands, J. G., Dickson, R. E., et al. (2001). Fine root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia, 128, 237–250.CrossRefGoogle Scholar
  26. Kraigher, H. (1999). Diversity of types of ectomycorrhizae on Norway spruce in Slovenia. Phyton Annals of Botany, 39, 199–202.Google Scholar
  27. Kraigher, H., Agerer, R., & Javornik, B. (1995). Ectomycorrhiza of Lactarius lignyotus on Norway spruce, characterised by anatomical and molecular tools. Mycorrhiza, 5, 175–180.CrossRefGoogle Scholar
  28. McCrady, J. K., & Andersen, C. P. (2000). The effect of ozone on below-ground carbon allocation in wheat. Environmental Pollution, 107, 465–472.CrossRefGoogle Scholar
  29. McQuattie, C. J. (1992). Effect of ozone and aluminium on Pitch pine (Pinus rigida) seedlings—Anatomy of mycorrhizae. Canadian Journal of Forest and Research, 22, 1901–1916.CrossRefGoogle Scholar
  30. Meier, S., Grand, L. F., Schoeneberger, M. M., Reinert, R.A., & Bruck, R.I. (1990). Growth, ectomycorrhizae and nonstructural carbohydrates of loblolly pine seedlings exposed to ozone and soil water deficit. Environmental Pollution, 64, 11–27.CrossRefGoogle Scholar
  31. Perez-Soba, M., Dueck, T. A., Puppi, P., & Kuiper, P. J. C. (1995). ‘Interactions of elevated CO2, NH3 and O3 on mycorrhizal infection, gas exchange and N metabolism in saplings of Scots pine. Plant Soil, 176, 107–116.CrossRefGoogle Scholar
  32. Phillips, R. L., Zak, D. R., & Holmes, W. E. (2002). Microbial community composition and function beneath temperate trees exposed to elevated atmospheric CO2 and tropospheric O3. Oecologia, 131, 236–244.CrossRefGoogle Scholar
  33. Pretzsch, H., Kahn, M., & Grote, R. (1998). Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches “Wachstum oder Parasitenabwehr?” im Kranzberg Forst. Forstwissenschaftliches Centralblatt, 117, 241–257.Google Scholar
  34. Smith, G., Coulston, J., Jepsen, E., & Prichard, T. (2005). A national ozone biomonitoring program - results from field surveys of ozone sensitive plants in North-Eastern forests (1994–2000). Environmental Monitoring and Assessment, 87, 271–291.CrossRefGoogle Scholar
  35. Topa, M. A., McDermitt, D. J., Yun, S.-C., & King, P. S. (2004). Do elevated ozone and variable light alter carbon transport to roots in sugar maple? New Phytologist, 162, 173–186.CrossRefGoogle Scholar
  36. Waltert, B., Wiemken, V., Rusterholz, H.P., Boller, T., & Baur, B. (2002). Disturbance of forest by trampling: Effects on mycorrhizal roots of seedlings and mature trees of Fagus sylvatica. Plant Soil, 243, 143–154.CrossRefGoogle Scholar
  37. Werner, H., & Fabian P. (2002). Free-air fumigation of mature trees: (a novel system for controlled ozone enrichment in grown-up beech and spruce canopies). Environmental Science Pollution and Research, 9, 117–121.CrossRefGoogle Scholar
  38. White, T. J., Bruns, T., Lee, S., & Taylor J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols. A guide to methods and applications (pp. 315–322). San Diego: Academic Press.Google Scholar

Copyright information

© Springer Science + Business Media B.V. 2007

Authors and Affiliations

  1. 1.Slovenian Forestry InstituteLjubljanaSlovenia

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