Abstract
Within the scope of quantifying ozone (O3 ) effects on forest tree crowns it is still an open question whether cuvette branches of adult trees are reasonable surrogates for O3 responses of entire tree crowns and whether twigs exhibit autonomy in defense metabolism in addition to carbon autonomy. Therefore, cuvette-enclosed branches of mature beech (Fagus sylvatica) trees were compared with branches exposed to the same and different ozone regimes by a free-air fumigation system under natural stand conditions by means of a vice versa experiment. For this purpose, cuvettes receiving 1 × O3 air were mounted in trees exposed to 2 × O3 and cuvettes receiving 2 × O3 air were mounted in trees exposed to 1 × O3 in the upper sun crown. At the end of the fumigation period in September 2004, leaves were examined for differences in gas exchange parameters, pigments, antioxidants, carbohydrates, and stable isotope ratios. No significant differences in foliar gas exchange, total carbohydrates, stable isotope ratios, pigment, and antioxidant contents were found as a consequence of cuvette enclosure (cuvette versus free-air branches) of the same O3 concentrations besides increase of glucose inside the cuvettes and reduction of the de-epoxidation state of the xanthophyll cycle pigments. No significant ozone effect was found for the investigated gas exchange and most biochemical parameters. The total and oxidized glutathione level of the leaves was increased by the 2 × O3 treatment in the cuvette and the free-air branches, but this effect was significant only for the free-air branches. From these results we conclude that cuvette branches are useful surrogates for examining the response of entire tree crowns to elevated O3 and that the defence metabolism of twigs seems to be at least partially autonomous.
Key words
Branch cuvettes - ozone -
Fagus sylvatica
- free-air fumigation - gas exchange - antioxidants - carbohydrates - stable isotopes
References
1
Alexou M., Hofer N., Liu X., Rennenberg H., Haberer K..
Significance of ozone exposure for inter-annual differences in primary metabolites of old-growth beech (Fagus sylvatica L.) and Norway spruce (Picea abies L.) trees in a mixed forest stand.
Plant Biology.
(2007);
9
227-241
2
Arndt S. K., Wanek W., Clifford S. C., Popp M..
Contrasting adaptations to drought stress in field-grown Ziziphus mauritiana and Prunus persica trees: water relations, osmotic adjustment and carbon isotope composition.
Australian Journal of Plant Physiology.
(2000);
27
985-996
3
Asada K..
The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.
Annual Review of Plant Physiology and Plant Molecular Biology.
(1999);
50
601-639
4
Blumenröther M. C., Löw M., Matyssek R., Oßwald W..
Flux-based response of sucrose and starch in leaves of adult beech trees (Fagus sylvatica L.) under chronic free-air O3 fumigation.
Plant Biology.
(2007);
9
207-214
5
Chen L.-S., Cheng L..
Photosynthetic enzymes and carbohydrate metabolism of apple leaves in response to nitrogen limitation.
Journal of Horticultural Science and Biotechnology.
(2004);
79
923-929
6
Couée I., Sulmon C., Gouesbet G., El Amrani A..
Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants.
Journal of Experimental Botany.
(2006);
57
449-459
7 DeKok L. J., Tausz M.. The role of glutathione in plant reaction and adaptation to air pollutants. Significance of Glutathione in Plant Adaptation to the Environment, Kluwer Handbook Series of Plant Ecophysiology. Amsterdam; Kluwer Publishers (2001): 185-208
8 Demmig-Adams B., Adams W. W.. Light stress and photoprotection related to the xanthophyll cycle. Foyer, C. H. and Mullineaux, P. M., eds. Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton; CRC Press (1994): 105-126
9
Einig W., Lauxmann U., Hauch B., Hampp R., Landolt W., Maurer S., Matyssek R..
Ozone-induced accumulation of carbohydrates changes enzyme activities of carbohydrate metabolism in birch leaves.
New Phytologist.
(1997);
137
673-680
10
Ferdinand J. A., Fredericksen T. S., Kouterick K. B., Skelly J. M..
Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) trees.
Environmental Pollution.
(2000);
108
297-302
11 Foyer C.. Oxygen metabolism and electron transport in photosynthesis. Scandalios, G., ed. Oxidative Stress and the Molecular Biology of Antioxidant Defense. Cold Spring Harbor; Cold Spring Harbor Laboratory Press (1997): 587-621
12
Foyer C., Noctor G..
Oxygen processing in photosynthesis: regulation and signaling. Tansley Review No. 112.
New Phytologist.
(2000);
146
359-388
13
Fredericksen T. S., Joyce B. J., Skelly J. M., Steiner K. C., Kolb T. E., Kouterick K. B., Savage J. E., Snyder K. R..
Physiology, morphology, and ozone uptake of leaves of black cherry seedlings, saplings and canopy trees.
Environmental Pollution.
(1995);
89
273-283
14
Fredericksen T. S., Skelly J. M., Steiner K. C., Kolb T. E., Kouterick K. B..
Size mediated foliar response to ozone in black cherry trees.
Environmental Pollution.
(1996);
91
53-63
15
Gäb M., Hoffmann K., Lobe M., Metzger R., van Oyen S., Elbers G., Köllner B..
NIR-spectroscopic investigation of foliage of ozone-stressed Fagus sylvatica trees.
Journal of Forest Research.
(2006);
11
69-75
16
Göttlicher S., Knohl A., Wanek W., Buchmann N., Richter A..
Short-term changes in carbon isotope composition of soluble carbohydrates and starch: from canopy leaves to the root system.
Rapid Communication in Mass Spectrometry.
(2006);
20
653-660
17
Grulke N. E., Miller P. R..
Changes in gas exchange characteristics during the life span of giant sequoia - implications for response to current and future concentrations of atmospheric ozone.
Tree Physiology.
(1994);
14
659-668
18
Günthardt-Goerg M. S., Matyssek R., Scheidegger C., Keller T..
Differentiation and structural decline in the leaves and bark of birch (Betula pendula) under low ozone concentration.
Trees.
(1993);
7
104-114
19
Haberer K., Herbinger K., Alexou M., Tausz M., Rennenberg H..
Antioxidative defence of old growth beech (Fagus sylvatica) under double ambient O3 concentrations in a free-air exposure system.
Plant Biology.
(2007 a);
9
215-226
20
Haberer K., Grebenc T., Alexou M., Gessler A., Kraigher H., Rennenberg H..
Effects of long-term free-air ozone fumigation on δ15 N and total N in Fagus sylvatica and associated mycorrhizal fungi.
Plant Biology.
(2007 b);
9
242-252
21 Häberle K.-H., Reiter I. M., Nunn A. J., Gruppe A., Simon U., Gossner M., Werner H., Leuchner M., Heerdt C., Fabian P., Matyssek R.. KROCO, Freising, Germany: Canopy research in a temperate mixed forest of Southern Germany. Basset, Y., Horlyck, V., and Wright, S. J., eds. Studying Forest Canopies from Above: The International Canopy Crane Network. Smithsonian Tropical Research Institute and UNEP (2003): 71-78
22
Havranek W. M., Wieser G., Bodner M..
Ozone fumigation of Norway spruce at timberline.
Annales des Sciences Forestières.
(1989);
46
581-585
23
Havranek W. M., Wieser G..
Design and testing of twig chambers for ozone fumigation and gas exchange measurements in mature trees.
Proceedings of the Royal Society of Edinburgh, Section B.
(1994);
102
541-546
24
Herbinger K., Then C., Löw M., Haberer K., Alexou M., Koch N., Remele K., Heerdt C., Grill D., Rennenberg H., Häberle K.-H., Matyssek R., Tausz M., Wieser G..
Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure.
Environmental Pollution.
(2005);
173
476-482
25
Herbinger K., Then C., Haberer K., Alexou M., Löw M., Remele K., Rennenberg H., Matyssek R., Grill D., Wieser G., Tausz M..
Gas exchange and antioxidative compounds in young beech trees under free-air ozone exposure and comparisons to adult trees.
Plant Biology.
(2007);
9
288-297
78
Hoch G., Richter A., Körner C..
Non-structural carbon compounds in temperate forest trees.
Plant, Cell and Environment.
(2003);
26
1067-1081
26
Houpis J. L., Costella M. P., Cowels S..
A branch exposure chamber for fumigating ponderosa pine to atmospheric pollution.
Journal of Environmental Quality.
(1991);
20
467-474
27 Klotsche B.. Einfluß von Ozon auf Phänologie und visuelle Schäden des Laubes bei Fagus sylvatica L. und Picea abies L. im Kranzberger Forst. Diplomarbeit der Studienfakultät für Forstwissenschaft und Ressourcenmanagement der Technischen Universität München. (2005)
28
Kolb T. E., Fredericksen T. S., Steiner K. C., Skelly J. M..
Issues in scaling tree size and age responses to ozone: a review.
Environmental Pollution.
(1997);
98
195-208
29
Kolb T. E., Matyssek R..
Limitations and perspectives about scaling ozone impacts in trees.
Environmental Pollution.
(2001);
115
373-393
30
Kronfuß G., Polle A., Tausz M., Havranek W. M., Wieser G..
Effects of ozone and mild drought stress on gas exchange, antioxidants and chloroplast pigments in current- year needles of young Norway spruce (Picea abies [L.] Karst.).
Trees.
(1998);
12
482-489
31
Landolt W., Günthardt-Goerg M. S., Pfenninger I., Einig W., Hampp R., Maurer S., Matyssek R..
Effect of fertilization on ozone-induced changes in the metabolism of birch leaves (Betula pendula) .
New Phytologist.
(1997);
37
389-397
32
Liu X. P., Kozovits A. R., Grams T. E. E., Blaschke H., Rennenberg H., Matyssek R..
Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech.
Tree Physiology.
(2004);
24
1045-1055
33
Liu X. P., Grams T. E. E., Rennenberg H., Matyssek R..
Effects of elevated pCO2 and/or pO3 on C-, N-, and S-metabolites in the leaves of juvenile beech and spruce differ between trees grown in monoculture and mixed culture.
Plant Physiology and Biochemistry.
(2005);
43
147-154
34
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);
20
539-548
35
Luwe M..
Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variation and responses to changing ozone concentrations in air.
Plant, Cell and Environment.
(1996);
19
321-328
36
Matyssek R., Günthardt-Goerg M. S., Saurer M., Keller T..
Seasonal growth, δ13 C in leaves and stem, and phloem structure of birch (Betula pendula) under low ozone concentrations.
Trees.
(1992);
6
69-76
37
Matyssek R., Sandermann H..
Impact of ozone on trees: an ecophysiological perspective.
Progress in Botany.
(2003);
64
349-404
38 Matyssek R., Wieser G., Nunn A. J., Löw M., Then C., Herbinger K., Blumenröther M., Jehnes S., Reiter I. M., Heerdt C., Koch N., Häberle K.-H., Haberer K., Werner H., Tausz M., Fabian P., Rennenberg H., Grill D., Oßwald W.. How sensitive are forest trees to ozone - new research on an old issue. Omasa, K., Nouchi, I., and De Kok, L. J., eds. Plant Responses to Air Pollution and Global Change. Tokyo; Springer-Verlag (2005): 21-28
39
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
40 Musselman R. C., Hale B. A.. Methods for controlled and field ozone exposure of forest tree species in North America. Sandermann Jr., H., Wellburn, A. R., and Heath, R. L., eds. Forest Decline and Ozone: A Comparison of Controlled Chamber and Field Experiments. Berlin, Heidelberg, New York; Springer Verlag (1997): 277-315
41
Niyogi K. K..
Photoprotection revisited: genetic and molecular approaches.
Annual Review of Plant Physiology and Plant Molecular Biology.
(1999);
50
333-359
42
Noctor G., Foyer C. H..
Ascorbate and glutathione: keeping active oxygen under control.
Annual Review of Plant Physiology and Plant Molecular Biology.
(1998);
49
249-279
43
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
44 Nunn A. J.. Risiko-Einschätzung der chronisch erhöhten Ozonbelastung mittels „Free-Air“-Begasung von Buchen (Fagus sylvatica) und Fichten (Picea abies) eines forstlich begründeten Mischbestandes. Dissertation (PhD), Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt, Technische Universität München. (2004)
45
Pahlsson A. M. B..
Mineral nutrients, carbohydrates and phenolic-compounds in leaves of beech (Fagus sylvatica L.) in Southern Sweden as related to environmental factors.
Tree Physiology.
(1989);
5
485-495
46
Pell E. J., Schlagnhaufer C. D., Arteca R. N..
Ozone-induced oxidative stress: mechanisms of action and reaction.
Physiologia Plantarum.
(1997);
100
264-273
47 Polle A., Rennenberg H.. Photooxidative stress in trees. Foyer, C. H. and Mullineaux, P. M., eds. Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton; CRC Press (1994): 199-218
48
Pretzsch H., Kahn M., Grote R..
Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches „Wachstum oder Parasitenabwehr?“ im Kranzberger Forst.
Forstwissenschaftliches Centralblatt.
(1998);
117
241-257
49
Rennenberg H., Herschbach C., Polle A..
Consequences of air pollution on shoot-root interaction.
Journal of Plant Physiology.
(1996);
148
296-301
50
Samuelson L. J., Edwards G. S..
A comparison of sensitivity to ozone in seedlings and trees of Quercus rubra L.
New Phytologist.
(1993);
64
93-106
51
Samuelson L. J., Kelly J. M..
Carbon partitioning and allocation in northern red oak seedlings and mature trees in response to ozone.
Tree Physiology.
(1996);
16
853-858
52 Sandermann H., Wellburn A. R., Heath R. L.. Forest decline and ozone: a comparison of controlled chamber and field experiments. Ecological Studies 127. Berlin, Heidelberg, New York; Springer (1997): 400p
53
Scheidegger Y., Saurer M., Bahn M., Siegwolf R..
Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model.
Oecologia.
(2000);
125
350-357
54
Schloter M., Winkler J. B., Aneja M., Koch N., Fleischmann F., Pritsch K., Heller W., Stich S., Grams T. E. E., Göttlein A., Matyssek R., Munch J. C..
Short term effects of ozone on the plant-rhizosphere-bulk soil system of young beech trees.
Plant Biology.
(2005);
7
728-736
55
Skärby L., Troeng E., Boström C.-A..
Ozone uptake and effects on transpiration, net photosynthesis, and dark respiration in scots pine.
Forest Science.
(1987);
33
801-808
56
Smeekens S..
Sugar-induced signal transduction in plants.
Annual Review of Plant Physiology.
(2000);
51
49-81
57
Smirnoff N..
The function and metabolism of ascorbic acid in plants.
Annals of Botany.
(1996);
78
661-669
58
Smirnoff N., Pallanca J. E..
Ascorbate metabolism in relation to oxidative stress.
Biochemical Society Transacta.
(1996);
24
472-478
59
Smirnoff N., Wheeler G. L..
Ascorbic acid in plants: biosynthesis and function.
Critical Reviews in Plant Sciences.
(2000);
19
267-290
60
Sprugel D. G., Hinckley T. M., Schaap W..
The theory and practice of branch autonomy.
Annual Review of Ecology and Systematics.
(1991);
22
309-334
61
Tausz M., Bytnerowicz A., Weidner W., Arbaugh M. J., Padgett P., Grill D..
Changes in free radical scavengers describe the susceptibility of Pinus ponderosa to ozone in southern Californian forests.
Water, Air, and Soil Pollution.
(1999);
116
249-254
62 Tausz M.. The role of glutathione in plant reaction and adaptation to natural stresses. Grill, D., Tausz, M., and DeKok, L. J., eds. Significance of Glutathione in Plant Adaptation to the Environment. Kluwer Handbook Series of Plant Ecophysiology, Amsterdam; Kluwer Publishers (2001): 101-122
63
Tausz M., Wonisch A., Grill D., Morales D., Jiménez M. S..
Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation.
Journal of Experimental Botany.
(2003);
54
1505-1510
64
Tausz M., Šircelj H., Grill D..
The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid?.
Journal of Experimental Botany.
(2004);
55
1955-1962
65
Taylor Jr. G. E., Hanson P. J..
Forest trees and tropospheric ozone: role of canopy deposition and leaf uptake in developing exposure-response relationships.
Agriculture, Ecosystems and Environment.
(1992);
42
255-273
66
Tegischer K., Tausz M., Wieser G., Grill D..
Tree- and needle-age-dependent variations in antioxidants and photoprotective pigments in Norway spruce needles at the alpine timberline.
Tree Physiology.
(2002);
22
591-596
67 Then C., Wieser G., Heerdt C., Herbinger K., Gigele T., Lohner H.. Diagnostics in beech exposed to chronic free air O3 fumigation. 2. Comparison between young and adult trees at the branch and tree level. In Proceedings of the Meeting “Forests under changing climate, enhanced UV and air pollution”, August 25 - 30, 2004, Oulu, Finland. (2004): 143-150
68 Then C., Herbinger K., Remele K., Grill D., Wieser G., Tausz M.. Differences in gas exchange and antioxidative compounds between young and adult beech trees at the branch and tree level exposed to defined ozone regimes. In Proceedings of the CASIROZ Session at the UN/ECE Workshop “Critical levels of ozone: further applying and developing the flux-based concept”, November 15 - 19, 2005, Obergurgl, Austria. (2005): 28-33
69
Ulger S., Sonmez S., Karkacier M., Ertoy N., Akdesir O., Aksu M..
Determination of endogenous hormones, sugars and mineral nutrition levels during the induction, initiation and differentiation stage and their effects on flower formation in olive.
Plant Growth Regulation.
(2004);
42
89-95
70
Wellburn F. A. M., Wellburn A. R..
Variable patterns of antioxidant protection but similar ethene emission differences in several ozone-sensitive and ozone-tolerant plant species.
Plant, Cell and Environment.
(1996);
19
761-767
71
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
72
Wieser G., Häsler R., Götz B., Koch W., Havranek W. M..
Role of climate, crown position, tree age and altitude in calculated ozone flux into needles of Picea abies and Pinus cembra : a synthesis.
Environmental Pollution.
(2000);
110
415-422
73
Wieser G., Tausz M., Wonisch A., Havranek W. M..
Free radical scavengers and photosynthetic pigments in needles of a cembran pine (Pinus cembra L.) tree growing at the alpine timberline as affected by ozone exposure.
Biologia Plantarum.
(2001);
44
225-232
74
Wieser G., Tegischer K., Tausz M., Häberle K.-H., Grams T. E. E., Matyssek R..
Age effects on Norway spruce (Picea abies) susceptibility to ozone uptake: a novel approach relating stress avoidance to defense.
Tree Physiology.
(2002 a);
22
583-590
75
Wieser G., Tegischer K., Tausz M., Häberle K.-H., Grams T. E. E., Matyssek R..
The role of antioxidative defense in determining ozone sensitivity of Norway spruce (Picea abies [L.] Karst.) across tree age: implications for the sun- and shade-crown.
Phyton.
(2002 b);
42
245-253
76 Wieser G.. Exchange of trace gases at the tree-atmosphere interface-ozone. Papen, H., Gasche, R., and Rennenberg, H., eds. Trace Gas Exchange in Forest Ecosystems. Dordrecht; Kluwer Academic Publishers (2002): 211-226
77
Wieser G., Hecke K., Tausz M., Häberle K.-H., Grams T. E. E., Matyssek R..
The influence of microclimate and tree age on the defense capacity of European beech (Fagus sylvatica L.) against oxidative stress.
Annales of Forest Science.
(2003);
60
131-135
C. Then
Ecophysiology of Plants Department of Ecology TUM, Life Sciences Center Weihenstephan
85354 Freising
Germany
Email: christiane.then@uibk.ac.at
Guest Editor: R. Matyssek