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Plant Biol (Stuttg) 2005; 7(6): 659-669
DOI: 10.1055/s-2005-872943
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Beech Leaf Colonization by the Endophyte Apiognomonia errabunda Dramatically Depends on Light Exposure and Climatic Conditions

G. Bahnweg1 , W. Heller1 , S. Stich1 , C. Knappe1 , G. Betz1 , C. Heerdt2 , R. D. Kehr3 , D. Ernst1 , C. Langebartels1 , 6 , A. J. Nunn4 , J. Rothenburger1 , 7 , R. Schubert5 , 8 , P. Wallis1 , 9 , G. Müller-Starck5 , H. Werner2 , R. Matyssek4 , H. Sandermann Jr.1
  • 1GSF - National Research Centre for Environment and Health, Institute of Biochemical Plant Pathology, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany
  • 2Technische Universität München, Chair of Bioclimatology, Department of Ecology, Am Hochanger 13, 85354 Freising, Germany
  • 3HAWK Hochschule für Angewandte Wissenschaft und Kunst, Fachhochschule Hildesheim/Holzminden/Göttingen, Fakultät Ressourcenmanagement, Büsgenweg 1 A, 37077 Göttingen, Germany
  • 4Technische Universität München, Chair of Ecophysiology of Plants, Department of Ecology, Am Hochanger 13, 85354 Freising, Germany
  • 5Technische Universität München, Department of Plant Sciences, Section of Forest Genetics, Am Hochanger 13, 85354 Freising, Germany
  • 6Present address: GSF - National Research Centre for Environment and Health, Scientific-Technical Department, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany
  • 7Present address: Sanochemia Pharmazeutika AG, Landegger Straße 7, 2491 Neufeld, Austria
  • 8Present address: Biotechnology Group, University of Applied Sciences, Kuelzufer 2, 02763 Zittau, Germany
  • 9Present address: Department of Chemistry, Christopher Ingold Laboratories, University College London, 20 Gordon Street, London WC1H 0AJ, UK
Further Information

Publication History

Received: May 9, 2005

Accepted: September 22, 2005

Publication Date:
02 January 2006 (online)

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Abstract

Ozone and light effects on endophytic colonization by Apiognomonia errabunda of adult beech trees (Fagus sylvatica) and their putative mediation by internal defence compounds were studied at the Kranzberg Forest free-air ozone fumigation site. A. errabunda colonization was quantified by “real-time PCR” (QPCR). A. errabunda-specific primers allowed detection without interference by DNA from European beech and several species of common genera of plant pathogenic fungi, such as Mycosphaerella, Alternaria, Botrytis, and Fusarium. Colonization levels of sun and shade leaves of European beech trees exposed either to ambient or twice ambient ozone regimes were determined. Colonization was significantly higher in shade compared to sun leaves. Ozone exhibited a marginally inhibitory effect on fungal colonization only in young leaves in 2002. The hot and dry summer of 2003 reduced fungal colonization dramatically, being more pronounced than ozone treatment or sun exposure. Levels of soluble and cell wall-bound phenolic compounds were approximately twice as high in sun than in shade leaves. Acylated flavonol 3-O-glycosides with putatively high UV‐B shielding effect were very low in shade canopy leaves. Ozone had only a minor influence on secondary metabolites in sun leaves. It slightly increased kaempferol 3-O-glucoside levels exclusively in shade leaves. The frequently prominent hydroxycinnamic acid derivative, chlorogenic acid, was tested for its growth inhibiting activity against Apiognomonia and showed an IC50 of approximately 8 mM. Appearance of Apiognomonia-related necroses strongly correlated with the occurrence of the stress metabolite, 3,3′,4,4′-tetramethoxybiphenyl. Infection success of Apiognomonia was highly dependent on light exposure, presumably affected by the endogenous levels of constitutive phenolic compounds. Ozone exerted only minor modulating effects, whereas climatic factors, such as pronounced heat periods and drought, were dramatically overriding.

Key words

European beech (Fagus sylvatica) - Apiognomonia errabunda - endophyte - “real-time PCR” - plant phenolics - sun and shade leaves - light - ozone - climate - precipitation.

References

  • 1 Bahnweg G., Schulze S., Möller E. M., Rosenbrock H., Langebartels C., Sandermann H.. DNA isolation from recalcitrant materials such as tree roots, bark, and forest soil for the detection of fungal pathogens by PCR.  Analytical Biochemistry. (1998);  262 79-82
    CrossrefPubMedGoogle Scholar
  • 2 Bahnweg G., Schubert R., Kehr R. D., Müller-Starck G., Heller W., Langebartels C., Sandermann H.. Controlled inoculation of Norway spruce (Picea abies) with Sirococcus conigenus: PCR-based quantification of the pathogen in host tissue and infection-related increase of phenolic metabolites.  Trees. (2000);  14 435-441
    CrossrefPubMedGoogle Scholar
  • 3 Böhm J., Hahn A., Schubert R., Bahnweg G., Adler N., Nechwatal J., Oehlmann R., Oßwald W.. Real-time quantitative PCR: DNA determination in isolated spores of the mycorrhizal fungus Glomus mossae and monitoring of Phytophthora infestans and Phytophthora citricola in their respective host plants.  Journal of Phytopathology. (1999);  147 409-416
    CrossrefPubMedGoogle Scholar
  • 4 Butin H.. Tree Diseases and Disorders. Oxford; Oxford University Press (1995)
    Google Scholar
  • 5 Butin H.. Effect of endophytic fungi from oak (Quercus robur L.) on mortality of leaf-inhabiting gall insects.  European Journal of Forest Pathology. (1992);  22 237-246
    PubMedGoogle Scholar
  • 6 Carrol G.. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont.  Ecology. (1988);  69 2-9
    PubMedGoogle Scholar
  • 7 Danti R., Sieber T. N., Sanguineti G.. Endophytic mycobiota in bark of European beech (Fagus sylvatica) in the Apennines.  Mycological Research. (2002);  106 1343-1348
    CrossrefPubMedGoogle Scholar
  • 8 Dubois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F.. Colorimetric method for determination of sugars and related substances.  Analytical Chemistry. (1956);  28 350-356
    CrossrefPubMedGoogle Scholar
  • 9 Haemmerli U. A., Brändle U. E., Petrini O., McDermott J. M.. Differentiation of isolates of Discula umbrinella (teleomorph: Apiognomonia errabunda) from beech, chestnut, and oak using randomly amplified polymorphic DNA markers.  Molecular Plant-Microbe Interactions. (1992);  5 479-483
    PubMedGoogle Scholar
  • 10 Kowalski T., Kehr R. D.. Fungal endophytes of living branch bases in several European tree species. Redlin, S. C. and Carris, L. M., eds. Endophytic Fungi in Grasses and Woody Plants - Systematics, Ecology and Evolution , St. Paul,. Minnesota; APS Press (1996): 67-86
    Google Scholar
  • 11 Langebartels C., Heller W., Ernst D., Lippert M., Lütz C., Sandermann H.. Ozone responses of trees: results from controlled chamber exposures in the GSF phytotron. Sandermann, H., Wellburn, A. R., and Heath, R. L., eds. Forest Decline and Ozone: A Comparison of Controlled Chamber and Field Experiments, Ecological Studies No. 127. Berlin; Springer Verlag (1997): 163-200
    Google Scholar
  • 12 Langebartels C., Heller W., Führer G., Lippert M., Simons S., Sandermann H.. “Memory effects” in the action of ozone on conifers.  Ecotoxicology and Environmental Safety. (1998);  41 62-72
    CrossrefPubMedGoogle Scholar
  • 13 Lee S. B., Taylor J. W.. Phylogeny of five fungus-like protoctisan Phytophthora species, inferred from the internal transcribed spacer of ribosomal DNA.  Molecular Biology and Evolution. (1992);  9 636-653
    PubMedGoogle Scholar
  • 14 Manning W. J., von Tiedemann A.. Climate change: Potential effects of increased atmospheric carbon dioxide (CO2), ozone (O3), and ultraviolet-B (UV‐B) radiation on plant diseases.  Environmental Pollution. (1995);  88 219-245
    CrossrefPubMedGoogle Scholar
  • 15 Matyssek R., Sandermann H.. Impact of ozone on trees: an ecophysiological perspective.  Progress in Botany. (2003);  64 349-404
    PubMedGoogle Scholar
  • 16 Möller E. M., Bahnweg G., Sandermann H., Geiger H. H.. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues.  Nucleic Acids Research. (1992);  20 6115-6116
    PubMedGoogle Scholar
  • 17 Morelet M.. L'anthracnose des chênes et du hêtre en France.  Revue Forestière Française. (1989);  41 488-496
    PubMedGoogle Scholar
  • 18 Nunn A. J., Reiter I. M., Häberle K.-H., Werner H., Langebartels C., Sandermann H., Heerdt C., Fabian P., Matyssek R.. “Free-air” ozone canopy fumigation in an old-growth mixed forest: concept and observations in beech.  Phyton. (2002);  42 105-119
    PubMedGoogle Scholar
  • 19 Nunn A. J., Anegg S., Betz G., Simons S., Kalisch G., Seidlitz H., Grams T. E. E., Häberle K.-H., Matyssek R., Bahnweg G., Sandermann H., Langebartels C.. Role of ethylene in the regulation of cell death and leaf loss in ozone-exposed European beech.  Plant, Cell and Environment. (2005);  28 886-897
    CrossrefPubMedGoogle Scholar
  • 20 Pehl L., Butin H.. Endophytische Pilze in Blättern von Laubbäumen und ihre Beziehungen zu Blattgallen (Zoocecidien).  Mitteilungen der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Berlin-Dahlem. (1994);  297
    PubMedGoogle Scholar
  • 21 Petrini O.. Fungal endophytes of tree leaves. Andrews, J. H. and Hirano, S. S., eds. Microbial Ecology of Leaves. New York; Springer Verlag (1991): 179-187
    Google Scholar
  • 22 Pretzsch H., Kahn M., Grote R.. Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches „Wachstum oder Parasitenabwehr?“ im Kranzberger Forst.  Forstwissenschaftliches Centralblatt. (1998);  117 241-257
    PubMedGoogle Scholar
  • 23 Pronos J., Merrill L., Dahlsten D.. Insects and pathogens in a pollution-stressed forest. Miller, P. R. and McBride, J. M., eds. Oxidant Air Pollution Impacts in the Montane Forest of Southern California, Ecological Studies, Vol. 134. Berlin, Heidelberg, New York; Springer Verlag (1999): 317-336
    Google Scholar
  • 24 Reich P. B.. Quantifying plant response to ozone: a unifying theory.  Tree Physiology. (1987);  3 63-91
    PubMedGoogle Scholar
  • 25 Sandermann H.. Ozone/biotic disease interactions: molecular biomarkers as a new experimental tool.  Environmental Pollution. (2000);  108 327-332
    CrossrefPubMedGoogle Scholar
  • 26 Sandermann H., Matyssek R.. Scaling up from molecular to ecological processes. Sandermann, H. ed. Molecular Ecotoxicology of Plants, Ecological Studies, Vol. 170. Berlin; Springer Verlag (2004): 207-226
    Google Scholar
  • 27 Schulze S., Bahnweg G., Möller E. M., Sandermann H.. Identification of the genus Armillaria by specific amplification of an rDNA‐ITS fragment and evaluation of genetic variation within A. ostoyae by rDNA-RFLP and RAPD analysis.  European Journal of Forest Pathology. (1997);  27 225-239
    PubMedGoogle Scholar
  • 28 Sieber T., Hugentobler C.. Endophytische Pilze in Blättern und Ästen gesunder und geschädigter Buchen (Fagus sylvatica L.).  European Journal of Forest Pathology. (1987);  17 411-425
    PubMedGoogle Scholar
  • 29 Sinclair J. B., Cernauskas R. F.. Latent infection vs. endophytic colonization by fungi. Redlin, S. C. and Carris, L. M., eds. Endophytic Fungi in Grasses and Woody Plants - Systematics, Ecology and Evolution. St. Paul, Minnesota; APS Press (1996): 3-29
    Google Scholar
  • 30 Stevens (ed.) R. B.. Mycology Guidebook. Seattle; University of Washington Press (1974)
    Google Scholar
  • 31 Stone J. K.. Initiation and development of latent infections by Rhabdocline parkeri on Douglas-fir.  Canadian Journal of Botany. (1987);  65 2614-2621
    PubMedGoogle Scholar
  • 32 Stone J. K., Bacon C. W., White J. F.. An overview of endophytic microbes: Endophytism defined. Bacon, C. W. and White, J. F., eds. Microbial Endophytes. New York; Marcel Dekker (2000): 3-29
    Google Scholar
  • 33 Toti L., Viret O., Horat G., Petrini O.. Detection of the endophyte Discula umbrinella in buds and twigs of Fagus sylvatica.  European Journal of Forest Pathology. (1993);  23 147-152
    PubMedGoogle Scholar
  • 34 Turunen M., Heller W., Stich S., Sandermann H., Sutinen M. L., Norokorpi Y.. The effects of UV exclusion on the soluble phenolics of young Scots pine seedlings in the subarctic.  Environmental Pollution. (1999);  106 219-228
    CrossrefPubMedGoogle Scholar
  • 35 Viret O., Petrini O.. Colonization of beech leaves (Fagus sylvatica) by the endophyte Discula umbrinella (teleomorph: Apiognomonia errabunda).  Mycological Research. (1994);  98 423-432
    PubMedGoogle Scholar
  • 36 Werner H., Fabian P.. Free-air fumigation on mature trees: a novel system for controlled ozone enrichment in grown-up beech and spruce canopies.  Environmental Science and Pollution Research. (2002);  9 117-121
    PubMedGoogle Scholar
  • 37 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; Academic Press (1990): 315-322
    Google Scholar
  • 38 Wilson D.. Ecology of woody plant endophytes. Bacon, C. W. and White, J. F., eds. Microbial Endophytes. New York; Marcel Dekker (2000): 389-420
    Google Scholar
  • 39 Wilson D., Carroll G. C.. Infection studies of Discula quercina, an endophyte of Quercus garryana.  Mycologia. (1994);  86 635-647
    CrossrefPubMedGoogle Scholar
  • 40 Zielke H., Sonnenbichler J.. Natural occurrence of 3,3′,4,4′-tetramethoxy-1,1′-biphenyl in leaves of stressed European beech.  Naturwissenschaften. (1990);  77 384-385
    CrossrefPubMedGoogle Scholar

G. Bahnweg

GSF - National Research Centre for Environment and Health
Institute of Biochemical Plant Pathology

Ingolstädter Landstraße 1

85764 Neuherberg

Germany

Email: bahnweg@gsf.de

Editor: H. Rennenberg

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