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DOI: 10.1055/s-2006-924758
Georg Thieme Verlag Stuttgart KG · New York
Effects of Long-Term Free-Air Ozone Fumigation on δ15N and Total N in Fagus sylvatica and Associated Mycorrhizal Fungi
Publication History
Received: March 3, 2006
Accepted: October 11, 2006
Publication Date:
13 March 2007 (online)
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Abstract
Patterns of nitrogen (N) isotope composition (δ15N) and total N contents were determined in leaves, fine roots, root-associated ectomycorrhizal fungi (ECM) of adult beech trees (Fagus sylvatica), and soil material under ambient (1 × O3) and double ambient (2 × O3) atmospheric ozone concentrations over a period of two years. From fine root to leaf material δ15N decreased consecutively. Under enhanced ozone concentrations total N was reduced in fine roots and δ15N showed a decrease in roots and leaves. In the soil and in most types of mycorrhizae, δ15N and total N were not altered due to ozone fumigation. The number of vital ectomycorrhizal root tips increased and the mycorrhizal community structure changed in 2 × O3. Simultaneously, the specific rate of inorganic N-uptake by the roots was reduced under the double ozone regime. From these results it is assumed that 2 × O3 changes N-nutrition of the trees at the level of N-acquisition, as indicated by enhanced mycorrhizal root tip density, altered mycorrhizal species composition, and reduced specific N-uptake rates.
Key words
Free-air ozone fumigation - δ15N - total N - net N-uptake - ectomycorrhiza.
References
- 1 Andersen C. P.. Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytologist. (2003); 157 213-228
- 2 Andersen C. P., Hogsett W. E., Plocher M., Rodecap K., Lee E. H.. Blue wild-rye grass competition increases the effect of ozone on ponderosa pine seedlings. Tree Physiology. (2001); 21 319-327
- 3 Andersen C. P., Hogsett W. E., Wessling R., Plocher M.. Ozone decreases spring root-growth and root carbohydrate content in Ponderosa pine the year following exposure. Canadian Journal of Forest Research - Revue Canadienne de Recherche Forestière. (1991); 21 1288-1291
- 4 Atlas R. M., Bartha R.. Microbial Ecology: Fundamentals and Applications. Reading, London; Addison-Wesley Publishing Company (1981)
- 5 Baier M., Kandlbinder A., Golldack D., Dietz K. J.. Oxidative stress and ozone: perception, signalling and response. Plant, Cell and Environment. (2005); 28 1012-1020
- 6 BassiriRad H., Constable J. V. H., Lussenhop J., Kimball B. A., Norby R. J., Oechel W. C., Reich P. B., Schlesinger W. H., Zitzer S., Sehtiya H. L., Silim S.. Widespread foliage delta N‐15 depletion under elevated CO2: inferences for the nitrogen cycle. Global Change Biology. (2003); 9 1582-1590
- 7 Bayrische Landesanstalt für Wald- und Forstwirtschaft .Bayrische Waldklimastation - Jahrbuch. (1999)
- 8 Bergersen F. J., Peoples M. B., Turner G. L.. Isotopic discriminations during the accumulation of nitrogen by soybeans. Australian Journal of Plant Physiology. (1988); 15 407-420
- 9 Bidartondo M. I., Ek H., Wallander H., Soderstrom B.. Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi?. New Phytologist. (2001); 151 543-550
- 10 Bielenberg D. G., Lynch J. P., Pell E. J.. Nitrogen dynamics during O3-induced accelerated senescence in hybrid poplar. Plant, Cell and Environment. (2002); 25 501-512
- 11 Blum U., Tingey D. T.. Study of potential ways in which ozone could reduce root-growth and nodulation of soybean. Atmospheric Environment. (1977); 11 737-739
- 12 Chapman J. A., King J. S., Pregitzer K. S., Zak D. R.. Effects of elevated concentrations of atmospheric CO2 and tropospheric O3 on decomposition of fine roots. Tree Physiology. (2005); 25 1501-1510
- 13 Chung H. G., Zak D. R., Lilleskov E. A.. Fungal community composition and metabolism under elevated CO2 and O3. Oecologia. (2006); 147 143-154
- 14 Coleman M. D., Dickson R. E., Isebrands J. G., Karnosky D. F.. Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone. Tree Physiology. (1996); 16 145-152
- 15 Dohmen G. P., Koppers A., Langebartels C.. Biochemical response of Norway spruce (Picea abies [L] Karst) towards 14-month exposure to ozone and acid mist - effects on amino-acid, glutathione and polyamine titers. Environmental Pollution. (1990); 64 375-383
- 16 Edwards G. S., Kelly J. M.. Ectomycorrhizal colonization of Loblolly-pine seedlings during 3 growing seasons in response to ozone, acidic precipitation, and soil Mg status. Environmental Pollution. (1992); 76 71-77
- 17 Emmerton K. S., Callaghan T. V., Jones H. E., Leake J. R., Michelsen A., Read D. J.. Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytologist. (2001); 151 503-511
- 18 Evans R. D.. Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science. (2001); 6 121-126
- 19 Evans R. D., Bloom A. J., Sukrapanna S. S., Ehleringer J. R.. Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T‐5) grown under ammonium or nitrate nutrition. Plant, Cell and Environment. (1996); 19 1317-1323
- 20 Fotelli M. N., Rennenberg H., Gessler A.. Effects of drought on the competitive interference of an early successional species (Rubus fruticosus) on Fagus sylvatica L. seedlings: N‐15 uptake and partitioning, responses of amino acids and other N compounds. Plant Biology. (2002); 4 311-320
- 21 Gebauer G., Schulze E. D.. Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia. (1991); 87 198-207
- 22 Gebauer G., Taylor A. F. S.. N‐15 natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization. New Phytologist. (1999); 142 93-101
- 23 Gessler A.. Untersuchungen zum Stickstoffhaushalt von Buchen (Fagus sylvatica) in einem stickstoffübersättigten Waldökosystem. Schriftenreihe der Professur für Baumphysiologie. (1999); 6
- 24 Gessler A., Jung K., Gasche R., Papen H., Heidenfelder A., Borner E., Metzler B., Augustin S., Hildebrand E., Rennenberg H.. Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots. European Journal of Forest Research. (2005); 124 95-111
- 25 Grebenc T., Kraigher H.. Types of ectomycorrhiza of mature beech and spruce at at ozone-fumigated and control forest plots. Envrionmental Monitoring and Assessment. (2006);
- 26 Grebenc T., Kraigher H.. Changes in the community of ectomycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration. Plant Biology. (2007); 9 279-287
- 27 Handley L. L., Brendel O., Scrimgeour C. M., Schmidt S., Raven J. A., Turnbull M. H., Stewart G. R.. The N‐15 natural abundance patterns of field-collected fungi from three kinds of ecosystems. Rapid Communications in Mass Spectrometry. (1996); 10 974-978
- 28 Handley L. L., Raven J. A.. The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell and Environment. (1992); 15 965-985
- 29 Handley L. L., Scrimgeour C. M.. Terrestrial plant ecology and N‐15 natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old field. Advances in Ecological Research. (1997); 27 133-212
- 30 Heaton T. H. E., Spiro B., Madeline S., Robertson C.. Potential canopy influences on the isotopic composition of nitrogen and sulphur in atmospheric deposition. Oecologia. (1997); 109 600-607
- 31 Hietz P., Wanek W., Popp M.. Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant, Cell and Environment. (1999); 22 1435-1443
- 32 Hobbie E. A., Jumpponen A., Trappe J.. Foliar and fungal (15) N : (14) N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia. (2005); 146 258-268
- 33 Hobbie E. A., Macko S. A., Shugart H. H.. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia. (1999); 118 353-360
- 34 Hobbie E. A., Macko S. A., Williams M.. Correlations between foliar delta N‐15 and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia. (2000); 122 273-283
- 35 Högberg P.. Tansley review No 95 - N‐15 natural abundance in soil-plant systems. New Phytologist. (1997); 137 179-203
- 36 Högberg P., Högberg M. N., Quist M. E., Ekblad A., Näsholm T.. Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phytologist. (1999); 142 569-576
- 37 Högberg P., Hogbom L., Schinkel H., Hogberg M., Johannisson C., Wallmark H.. N‐15 abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia. (1996); 108 207-214
- 38 Ingelög T., Nohrstedt H. O.. Ammonia formation and soil-pH increase caused by decomposing fruitbodies of macrofungi. Oecologia. (1993); 93 449-451
- 39 Jung K., Rolle W., Schlee D., Tintemann H., Schuurmann G.. Ozone effects on nitrogen incorporation and superoxide-dismutase activity in spruce seedlings (Picea abies L). New Phytologist. (1994); 128 505-508
- 40 Kamachi K., Yamaya T., Mae T., Ojima K.. A role for glutamine-synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiology. (1991); 96 411-417
- 41 Karnosky D. F., Gagnon Z. E., Dickson R. E., Coleman M. D., Lee E. H., Isebrands J. G.. Changes in growth, leaf abscission, and biomass associated with seasonal tropospheric ozone exposures of Populus tremuloides clones and seedlings. Canadian Journal of Forest Research - Revue Canadienne de Recherche Forestière. (1996); 26 23-37
- 42 Kasurinen A., Helmisaari H. S., Holopainen T.. The influence of elevated CO2 and O3 on fine roots and mycorrhizas of naturally growing young Scots pine trees during three exposure years. Global Change Biology. (1999); 5 771-780
- 43 Kasurinen A., Keinanen M. M., Kaipainen S., Nilsson L. O., Vapaavuori E., Kontro M. H., Holopainen T.. Below-ground responses of silver birch trees exposed to elevated CO2 and O3 levels during three growing seasons. Global Change Biology. (2005); 11 1167-1179
- 44 King J. S., Kubiske M. E., Pregitzer K. S., Hendrey G. R., McDonald E. P., Giardina C. P., Quinn V. S., Karnosky D. F.. Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2. New Phytologist. (2005); 168 623-635
- 45 Kitayama K., Iwamoto K.. Patterns of natural N‐15 abundance in the leaf-to-soil continuum of tropical rain forests differing in N availability on Mount Kinabalu, Borneo. Plant and Soil. (2001); 229 203-212
- 46 Koch K. E.. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology. (1996); 47 509-540
- 47 Kohl D. H., Shearer G.. Isotopic fractionation associated with symbiotic N2 fixation and uptake of NO3- by plants. Plant Physiology. (1980); 66 51-56
- 48 Kohzu A., Yoshioka T., Ando T., Takahashi M., Koba K., Wada E.. Natural C13 and N15 abundance of field-collected fungi and their ecological implications. New Phytologist. (1999); 144 323-330
- 49 Kölling C.. Profile von Lösungskonzentrationen und Stofffrachten-Stoffhaushaltsgrößen als charakteristische Eigenschaften von Waldökosystemen. Forst und Holz. (1997); 52 171-175
- 50 Koopmans C. J., van Dam D., Tietema A., Verstraten J. M.. Natural N‐15 abundance in two nitrogen saturated forest ecosystems. Oecologia. (1997); 111 470-480
- 51 Krupa S. V., Manning W. J.. Atmospheric ozone - formation and effects on vegetation. Environmental Pollution. (1988); 50 101-137
- 52 Kytöviita M. M., Le Thiec D., Dizengremel P.. Elevated CO2 and ozone reduce nitrogen acquisition by Pinus halepensis from its mycorrhizal symbiont. Physiologia Plantarum. (2001); 111 305-312
- 53 Laisk A., Kull O., Moldau H.. Ozone concentration in leaf intercellular air spaces is close to zero. Plant Physiology. (1989); 90 1163-1167
-
54 Langebartels C., Kangasjärvi J..
Ethylen and jasmonate as regulators of cell death in desease resistance. Sandermann, H., ed. Molecular Ecotoxicology of Plants. Berlin, Heidelberg; Springer Verlag (2004): 75-109 - 55 Lilleskov E. A., Hobbie E. A., Fahey T. J.. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytologist. (2002); 154 219-231
- 56 Mariotti A., Germon J. C., Hubert P., Kaiser P., Letolle R., Tardieux A., Tardieux P.. Experimental determination of nitrogen kinetic isotope fractionation - some principles - illustration for the denitrification and nitrification processes. Plant and Soil. (1981); 62 413-430
- 57 Mariotti A., Mariotti F., Amarger N., Pizelle G., Ngambi J. M., Champigny M. L., Moyse A.. Nitrogen isotope fractionation during nitrate absorption and atmospheric nitrogen-fixation by plants. Physiologie Végétale. (1980); 18 163-181
- 58 Mariotti A., Mariotti F., Champigny M. L., Amarger N., Moyse A.. Nitrogen isotope fractionation associated with nitrate reductase-activity and uptake of NO3 - by Pearl-Millet. Plant Physiology. (1982); 69 880-884
- 59 Matyssek R., Bahnweg G., Ceulemans R., Fabian P., Grill D., Hanke D. E., Kraigher H., Oßwald W., Rennenberg H., Sandermann H., Tausz M., Wieser G.. Synopsis of the CASIROZ case study: carbon sink strength of Fagus sylvatica L. in a changing environment - experimental risk assessment of mitigation by chronic ozone impact. Plant Biology. (2007); 9 163-180
-
60 Matyssek R., Häberle K. H..
Freising canopy crane, Germany. Mitchell, A. M., Secoy, K., and Jackson, T., eds. The Global Canopy Handbook. Oxford, UK; GCP Publisher (2002): 47-50 - 61 Matyssek R., Le Thiec D., Löw M., Dizengremel P., Nunn A. J., Häberle K. H.. Interactions between drought and O3 stress in forest trees. Plant Biology. (2006); 8 11-17
-
62 Nadelhoffer K., Fry B..
Nitrogen isotope studies in forest ecosystems. Lajtha, K., ed. Stable Isotopes in Ecology and Environmental Science. Oxford; Blackwell Scientific (1994): 23-44 - 63 Nadelhoffer K. F., Fry B.. Controls on natural N15 and C13 abundances in forest soil organic matter. Soil Science Society of America Journal. (1988); 52 1633-1640
- 64 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
- 65 Pearson J., Stewart G. R.. The deposition of atmospheric ammonia and its effects on plants. New Phytologist. (1993); 125 283-305
- 66 Piccolo M. C., Neill C., Melillo J. M., Cerri C. C., Steudler P. A.. N15 natural abundance in forest and pasture soils of the Brazilian Amazon Basin. Plant and Soil. (1996); 182 249-258
- 67 Pritchard E. S., Guy R. D.. Nitrogen isotope discrimination in white spruce fed with low concentrations of ammonium and nitrate. Trees - Structure and Function. (2005); 19 89-98
- 68 Qiu Z., Chappelka A. H., Somers G. L., Lockaby B. G., Meldahl R. S.. Effects of ozone and simulated acidic precipitation on ectomycorrhizal formation on Loblolly pine seedlings. Environmental and Experimental Botany. (1993); 33 423-431
- 69 Rantanen L., Palomaki 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
- 70 Rennenberg H., Loreto F., Polle A., Brilli S., Fares S., Beniwal R. S., Gessler A.. Physiological responses of forest trees to heat and drought. Plant Biology. (2006); 8 556-571
- 71 Riikonen J., Lindsberg M. M., Holopainen T., Oksanen E., Lappi J., Peltonen P., Vapaavuori E.. Silver birch and climate change: variable growth and carbon allocation responses to elevated concentrations of carbon dioxide and ozone. Tree Physiology. (2004); 24 1227-1237
- 72 Saxe H.. Physiological responses of trees to ozone-interactions and mechanisms. Current Topics in Plant Biology. (2002); 3 27-55
- 73 Schmitt R., Sandermann H.. Biochemical response of Norway spruce (Picea abies [L] Karst) towards 14-month exposure to ozone and acid mist. 2. Effects on protein-biosynthesis. Environmental Pollution. (1990); 64 367-373
- 74 Shearer G., Kohl D. H.. N2-fixation in field settings - estimations based on natural N15 abundance. Australian Journal of Plant Physiology. (1986); 13 699-756
- 75 Smith S. E., Read D. J.. Mycorrhizal Symbiosis. London; Acadamic Press (1997)
- 76 Ta C. T.. Nitrogen-metabolism in the stalk tissue of maize. Plant Physiology. (1991); 97 1375-1380
- 77 Taylor A. F. S., Hogbom L., Högberg M., Lyon A. J. E., Nasholm T., Högberg P.. Natural N15 abundance in fruit bodies of ectomycorrhizal fungi from boreal forests. New Phytologist. (1997); 136 713-720
- 78 Trudell S. A., Rygiewicz P. T., Edmonds R. L.. Patterns of nitrogen and carbon stable isotope ratios in macrofungi, plants and soils in two old-growth conifer forests. New Phytologist. (2004); 164 317-335
- 79 Turner G. L., Bergersen F. J., Tantala H.. Natural enrichment of N15 during decomposition of plant material in soil. Soil Biology and Biochemistry. (1983); 15 495-497
- 80 Wellburn A. R.. Why are atmospheric oxides of nitrogen usually phytotoxic and not alternative fertilizers?. New Phytologist. (1990); 115 395-429
- 81 Werner H., Fabian P.. Free-air fumigation of 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
- 82 Yoneyama T., Handley L. L., Scrimgeour C. M., Fisher D. B., Raven J. A.. Variations of the natural abundances of nitrogen and carbon isotopes in Triticum aestivum, with special reference to phloem and xylem exudates. New Phytologist. (1997); 137 205-213
- 83 Yoneyama T., Matsumaru T., Usui K., Engelaar W. M. H. G.. Discrimination of nitrogen isotopes during absorption of ammonium and nitrate at different nitrogen concentrations by rice (Oryza sativa L.) plants. Plant, Cell and Environment. (2001); 24 133-139
- 84 Yoneyama T., Omata T., Nakata S., Yazaki J.. Fractionation of nitrogen isotopes during the uptake and assimilation of ammonia by plants. Plant and Cell Physiology. (1991); 32 1211-1217
K. Haberer
Institute of Forest Botany and Tree Physiology
Chair of Tree Physiology
Albert Ludwigs University
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