Evidence that Branch Cuvettes are Reasonable Surrogates for Estimating O₃ Effects in Entire Tree Crowns

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 δ¹⁵N 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, δ¹³C 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

Guest Editor: R. Matyssek