Plant Biol (Stuttg) 2007; 9(2): 279-287
DOI: 10.1055/s-2006-924489
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Changes in the Community of Ectomycorrhizal Fungi and Increased Fine Root Number Under Adult Beech Trees Chronically Fumigated with Double Ambient Ozone Concentration

T. Grebenc1 , H. Kraigher1
  • 1Slovenian Forestry Institute, Večna pot 2, SI-1000 Ljubljana, Slovenia
Weitere Informationen

Publikationsverlauf

Received: February 17, 2006

Accepted: July 13, 2006

Publikationsdatum:
28. September 2006 (online)

Abstract

Forest soils are an important but under-studied part of forest ecosystems. The effects of O3 on below-ground processes in a mature forest have only received limited attention so far. In our study, we have analysed the community of ectomycorrhizal fungi and beech fine root dynamics over two growing seasons (2003 - 2004) in a 70-year old mixed spruce-beech forest stand, in which two groups of five adult beech trees were either fumigated by 2 × ambient ozone concentration or used as control. The main difference between previous studies and our approach was that previous studies were performed on seedlings in pot experiments or in closed or open top chambers, and not in situ, in a mature forest stand. Although beech is a relatively unresponsive species to tropospheric O3, we found a pronounced effect of 2 × O3 on the number of vital ectomycorrhizal root tips and non-turgescent fine roots. Both categories of roots were significantly increased when compared to controls in two consecutive years at each sampling event. The number of types of ectomycorrhizae and species richness increased in 2004, but not in the extremely dry year 2003. We hypothesised that the observed changes might be an expression of a transitional state in below-ground succession of niches caused by an O3 induced effect on carbon allocation to roots and the rhizosphere. We have detected changes in ectomycorrhizal species level, however Shannon-Weavers species diversity index and percentage of types of ectomycorrhizae did not change significantly in any sampling year thus indicating our results cannot be unequivocally explained by summer drought in year 2003 or by O3 exposure alone.

References

  • 1 Agerer R.. Colour Atlas of Ectomycorrhizae. 11th ed. München, Germany; Einhorn-Verlag Schwäbisch Gmünd (1987 - 2002) (separate pagination)
  • 2 Agerer R.. Characterisation of ectomycorrhiza.  Methods in Microbiology. (1991);  23 25-27
  • 3 Agerer R., Rambold G.. An Information System for Characterization and Determination of Ectomycorrhizae. www.deemy.de [most recent update: 2005-07-15]. München, Germany; (2004 - 2005)
  • 4 Al Sayegh Petkovšek S.. Below-ground ectomycorrhizal fungal communities at Fagus stands in differently polluted forest research plots.  Zbornik gozdarstva in lesarstva. (2005);  76 5-38
  • 5 Allen A. S., Andrews J. A., Finzi A. C., Matamala R., Richter D. D., Schlesinger W. H.. Effects of free-air CO2 enrichment (FACE) on belowground processes in a Pinus taeda forest.  Ecological Applications. (2000);  10 437-448
  • 6 Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes.  Nucleic Acid Research. (1997);  25 3389-3402
  • 7 Andersen C. P.. Source-sink balance and carbon allocation below ground in plants exposed to ozone (Tansley review).  New Phytologist. (2003);  157 213-228
  • 8 Ashmore M. R.. Assessing the future global impacts of ozone on vegetation.  Plant, Cell and Environment. (2005);  28 949-964
  • 9 Atlas R., Bartha R.. Introduction to Mycology. Reading, UK; Addison-Wesley Publishing Company (1981): 242-244
  • 10 Beenken L.. Die Gattung Russula Untersuchung zu ihrer Systematik anhand von Ektomykorrhizen. PhD Thesis, Faculty of Biology, Ludwig-Maximilians University, Munich, 414 pp. (2004)
  • 11 Bortier K., Ceulemans R., De Temmerman L.. Effects of tropospheric ozone on woody plants. Agrawal, S. B. and Agrawal, M., eds. Environmental Pollution and Plant Response. Boca Raton, London, New York, Washington D.C.; Lewis Publishers (1999): 153-182
  • 12 Bortier K., De Temmerman L., Ceulemans R.. Effects of ozone exposure in open-top chambers on poplar (Populus nigra) and beech (Fagus sylvatica): a comparison.  Environmental pollution. (2000);  199 509-516
  • 13 Brand F.. Ektomykorrhizen an Fagus sylvatica: Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung.  Libri Botanici. (1991);  2 1-229
  • 14 Chung H., Zak D. R., Lilleskov E. A.. Fungal community composition and metabolism under elevated CO2 and O3.  Oecologia. (2006);  147 143-154
  • 15 Dohrmann A. B., Tebbe C. C.. Effect of elevated tropospheric ozone on the structure of bacterial communities inhabiting the rhizosphere of herbaceous plants native to Germany.  Applied and Environmental Microbiology. (2005);  71 7750-7758
  • 16 Doyle J. J., Doyle J. L.. A rapid DNA isolation procedure for small quantities of fresh leaf tissue.  Phytochemical Bulletin. (1990);  19 11-15
  • 17 Downes G. M., Alexander I. J., Cairney J. W. G.. A study of spruce (Picea sitchensis [Bong] Carr.) ectomycorrhizas. I. Morphological and cellular changes in mycorrhizas formed by Tylospora fibrillosa (Burt) Donk and Paxillus involutus (Batsch ex Fr.) Fr.  New Phytologist. (1992);  122 141-152
  • 18 Duckmanton L., Widden P.. Effect of ozone on the development of vesicular-arbuscular mycorrhizae in sugar maple saplings.  Mycologia. (1994);  86 181-186
  • 19 Gardes M., Bruns T. D.. ITS primers with enhanced specificity for basidiomycetes - application to the identification of ectomycorrhizae and rusts.  Molecular Ecology. (1993);  2 113-118
  • 20 Gianinazzi-Pearson V.. Host specificity in mycorrhizae. Verma, P. D. S and Hohn, T. H., eds. Genes Involved in Plant-Microbe Interactions. Vienna; Springer (1984): 225-253
  • 21 Grebenc T., Piltaver A., Kraigher H.. Establishment of a PCR-RFLP library for Basidiomycetes, Ascomycetes and their ectomycorrhizae in Picea abies (L.) Karst.  Phyton Annales rei Botanicae. (2000);  40 79-82
  • 55 Grebenc T., Kraigher H.. Types of ectomycorrhiza of mature beech and spruce at ozone-fumigated and control forest plots.  Environmental Monitoring and Assessment. (2006);  DOI: 10.1007/s10661-006-9414-3
  • 22 Grimond P. A. D.. Taxotron user's manual. Paris, France; Institute Pasteur (1998): 1-120
  • 23 Grulke N. E., Andersen C. P., Fenn M. E., Miller P. R.. Ozone exposure and nitrogen deposition lowers root biomass of ponderosa pine in the San Bernardino Mountains, California.  Environmental Pollution. (1998);  103 63-73
  • 24 Hong B. G., Lee K. J.. Interaction of ozone with simultaneous water deficit and water deficit preconditioning in one-year-old Pinus densiflora seedlings.  Journal of Forest Research. (2001);  6 273-279
  • 25 Joslin J. D., Wolfe M. H., Hanson P. J.. Effects of altered water regimes on forest root systems.  New Phytologist. (2000);  147 117-129
  • 26 Kårén O., Hogberg N., Dahlberg A., Jonsson L., Nylund J. E.. Inter- and intraspecific variation in the ITS region of rDNA of ectomycorrhizal fungi in Fennoscandia as detected by endonuclease analysis.  New Phytologist. (1997);  136 313-325
  • 27 Karnosky D. F., Pregitzer K. S., Zak D. R., Kubiske M. E., Hendrey G. R., Weinstein D., Nosal M., Percy K. E.. Scaling ozone responses of forest trees to the ecosystem level in a changing climate.  Plant, Cell and Environment. (2005);  28 965-981
  • 28 Kasurinen A., Helmisaari H. S., Holopainen T.. The influence of elevated CO2 and O3 on fine roots and mycorrhizas on naturally growing young Scots pine trees during three exposure years.  Global Change Biology. (1999);  5 771-780
  • 29 Kraigher H.. Mycobioindication of pollution of two forest sites.  Zbornik gozdarstva in lesarstva. (1997);  52 279-322
  • 30 Kraigher H.. Diversity of types of ectomycorrhizae on Norway spruce in Slovenia.  Phyton Annales rei Botanicae. (1999);  39 199-202
  • 31 Kraigher H., Batič F., Agerer R.. Types of ectomycorrhizae and mycobioindication of forest site pollution.  Phyton Annales rei Botanicae. (1996);  36 115-120
  • 32 Kraigher H., Agerer R., Javornik B.. Ectomycorrhiza of Lactarius lignyotus on Norway spruce, characterised by anatomical and molecular tools.  Mycorrhiza. (1995);  5 175-180
  • 33 Kraigher H., Hanke D. E.. Cytokinins in Norway spruce seedlings and forest soil pollution.  Phyton Annales rei Botanicae. (1996);  36 57-60
  • 34 Kraigher H., Grayling A., Wang T. L., Hanke D. E.. Cytokinin production by two ectomycorrhizal fungi in liquid culture.  Phytochemistry. (1991);  30 2249-2254
  • 35 Kraigher H., Strnad M., Hanke D. E., Batič F.. Cytokiningehalte von Fichtennadeln (Picea abies [L.] Karst) nach Inokulation mit zwei Stämmen des Mykorrhizapilzes Thelephora terrestris (Ehrh.) Fr.  Forstwissenschaftliches Centralblatt. (1993);  112 107-111
  • 36 LoBuglio K. F.. Cenococcum. Cairney, J. W. G. and Chambers, S. M., eds. Ectomycorrhizal Fungi Key Genera in Profile. Berlin, Heidelberg; Springer (1999): 287-309
  • 37 Löw M., Herbinger K., Nunn A. J., Häberle K.-H., Leuchner M., Heerdt C., Werner H., Wipfler P., Pretzsch H., Tausz M., Matyssek R.. Extraordinary drought of 2003 overrules ozone impact on adult beech trees (Fagus sylvatica). .  Trees. (2006);  DOI: 10.1007/s00468-00006-00069-z
  • 38 McCrady J. K., Andersen C. P.. The effect of ozone on below-ground carbon allocation in wheat.  Environmental Pollution. (2000);  107 465-472
  • 39 Meier S., Grand L. F., Schoeneberger M. M., Reinert R. A., Bruck R. I.. Growth, ectomycorrhizae and nonstructural carbohydrates of loblolly pine seedlings exposed to ozone and soil water deficit.  Environmental Pollution. (1990);  64 11-27
  • 40 Ottossen S., Wallin G., Skärby L., Karlsson P.-E., Medin E.-L., Räntfors M., Pleijel H., Selldén G.. Four years of ozone exposure at high or low phosphorus reduced biomass in Norway spruce.  Trees. (2003);  17 299-307
  • 41 Pérez-Soba M., Dueck T. A., Puppi P., Kuiper P. C. J.. Interactions of elevated CO2, NH3 and O3 on mycorrhizal infection, gas exchange and N metabolism in saplings of Scots pine.  Plant and Soil. (1995);  176 107-116
  • 42 Pretzsch H., Kahn M., Grote R.. Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches "Wachstum oder Parasitenabwehr?" im Kranzberger Forst.  Forstwissenschaftliches Centralblatt. (1998);  117 241-257
  • 43 Rantanen L., Palomäki V., Holopainen T.. Interactions between exposure to O3 and nutrient status of trees: effects on nutrient content and uptake, growth, mycorrhiza and needle ultrastructure.  New Phytologist. (1994);  128 679-687
  • 44 Read D. J.. Plants on the web.  Nature. (1998);  396 22-23
  • 45 Roth D. R., Fahley T. J.. The effect of acid precipitation and ozone on the ectomycorrhizae of red spruce saplings.  Water, Air, and Soil Pollution. (1998);  103 263-276
  • 46 Rygiewicz P. T., Andersen C. P.. Mycorrhizae alter quality and quantity of carbon allocated below-ground.  Nature. (1994);  369 58-60
  • 47 Scagel C. F., Andersen C. P.. Seasonal changes in root and soil respiration of ozone-exposed Ponderosa pine (Pinus ponderosa) grown in different substrates.  New Phytologist. (1997);  136 627-643
  • 48 Schloter M., Winkler Aneja J. B. M., Koch N., Fleischmann F., Pritsch K., Heller W., Stich S., Grams T. E. E., Gőttlein A., Matyssek R., Munch J. C.. Short term effect of ozone on the plant-rhizosphere-bulk soil system of young beech trees.  Plant Biology. (2005);  6 728-736
  • 49 Topa M. A., McDermitt D. J., Yun S.-C., King P. S.. Do elevated ozone and variable light alter carbon transport to roots in sugar maple?.  New Phytologist. (2004);  162 173-186
  • 50 Werner H., Fabian P.. Free-air fumigation of mature trees.  Environmental Science and Pollution Research. (2002);  9 117-121
  • 51 White T. J., Bruns T., Lee S., Taylor J.. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis, M. A., Gelfand, D. H., Sninsky, J. J., and White, T. J., eds. PCR Protocols. A Guide to Methods and Applications. San Diego, USA; Academic Press (1990): 315-322
  • 52 http://unite.zbi.ee/ (most recent update: 21 December, 2005). 
  • 53 http://www.casiroz.de/ (most recent update: 11 November, 2005). 
  • 54 http://www.gozdis.si/departments/fisiologygenetics/forfisiology_genetics_dept.htm (most recent update: 20 December, 2005). 

T. Grebenc

Slovenian Forestry Institute

Večna pot 2

SI-1000 Ljubljana

Slovenia

eMail: tine.grebenc@gozdis.si

Guest Editor: R. Matyssek

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