Abstract
Patterns of nitrogen (N) isotope composition (δ15 N) 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 δ15 N decreased consecutively. Under enhanced ozone concentrations total N was reduced in fine roots and δ15 N showed a decrease in roots and leaves. In the soil and in most types of mycorrhizae, δ15 N 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 - δ15 N - 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
Georges-Köhler-Allee 053/054
79110 Freiburg
Germany
Email: kristine.haberer@ctp.uni-freiburg.de
Guest Editor: R. Matyssek