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Plant Biol (Stuttg) 2007; 9(2): 288-297
DOI: 10.1055/s-2006-924660
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Gas Exchange and Antioxidative Compounds in Young Beech Trees under Free-Air Ozone Exposure and Comparisons to Adult Trees

K. Herbinger1 , C. Then2 , 3 , K. Haberer4 , M. Alexou4 , M. Löw3 , K. Remele1 , H. Rennenberg4 , R. Matyssek3 , D. Grill1 , G. Wieser2 , M. Tausz1 , 5
  • 1Institut für Pflanzenwissenschaften, Universität Graz, Schuberstraße 51, 8010 Graz, Austria
  • 2Bundesamt und Forschungszentrum für Wald, Abteilung Forstpflanzenphysiologie, Rennweg 1, 6020 Innsbruck, Austria
  • 3Lehrstuhl für Ökophysiologie der Pflanzen, Technische Universität München, Life Science Center Weihenstephan, Am Hochanger 13, 85350 Freising, Germany
  • 4Institut für Forstbotanik und Baumphysiologie, Professur für Baumphysiologie, Albert-Ludwigs-Universität Freiburg, Georges-Köhler-Allee 053/054, 79085 Freiburg, Germany
  • 5School of Forest and Ecosystem Science, University of Melbourne, Water Street, Creswick, Victoria 3363, Australia
Further Information

Publication History

Received: April 28, 2006

Accepted: September 8, 2006

Publication Date:
13 March 2007 (online)

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Abstract

Three-year-old beech (Fagus sylvatica) seedlings growing in containers were placed into the sun and shade crown of a mature beech stand exposed to ambient (1 × O3) and double ambient (2 × O3) ozone concentrations at a free-air exposure system (“Kranzberg Forst”, Germany). Pigments, α-tocopherol, glutathione, ascorbate, and gas exchange were measured in leaves during 2003 (a drought year) and 2004 (an average year). Sun-exposed seedlings showed higher contents of antioxidants, xanthophylls, and β-carotene and lower contents of chlorophyll, α-carotene, and neoxanthin than shade-exposed seedlings. In 2003 sun-exposed seedlings showed higher contents of carotenoids and total glutathione and lower net photosynthesis rates (Amax) compared to 2004. O3 exposure generally affected the content of chlorophyll, the xanthophyll cycle, and the intercellular CO2 concentration (ci). Seedlings differed from the adjacent adult trees in most biochemical and physiological parameters investigated: Sun exposed seedlings showed higher contents of α-tocopherol and xanthophylls and lower contents of ascorbate, chlorophyll, neoxanthin, and α-carotene compared to adult trees. Shade exposed seedlings had lower contents of xanthophylls, α-carotene, and α-tocopherol than shade leaves of old-growth trees. In 2003, seedlings had higher Amax, stomatal conductance (gs), and ci under 2 × O3 than adult trees. The results showed that shade acclimated beech seedlings are more sensitive to O3, possibly due to a lower antioxidative capacity per O3 uptake. We conclude that beech seedlings are uncertain surrogates for adult beech trees.

Key words

Ozone - beech - Fagus sylvatica - tree age - antioxidants - pigments - leaf gas exchange.

References

  • 1 Adams III. W. W., Demmig-Adams B.. Carotenoid composition and down regulation of photosystem II in three conifer species during winter.  Physiologica Plantarum. (1994);  92 451-458
    PubMedGoogle Scholar
  • 2 Bortier K., Vandermeiren K., De Temmerman L., Ceulemans R.. Growth, photosynthesis and ozone uptake of young beech (Fagus sylvatica L.) in response to different ozone exposures.  Trees. (2001);  15 75-82
    CrossrefPubMedGoogle Scholar
  • 3 Demmig-Adams B., Adams III. W. W.. Photoprotection and other responses of plants to high light stress.  Annual Review of Plant Physiology and Plant Molecular Biology. (1992);  43 599-626
    CrossrefPubMedGoogle Scholar
  • 4 Demmig-Adams B., Adams III. W. W.. Chlorophyll and carotenoid composition in leaves of Euonymus kiatschovicus acclimated to different degrees of light stress in the field.  Australian Journal of Plant Physiology. (1996);  23 649-659
    PubMedGoogle Scholar
  • 5 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) seedlings.  Environmental Pollution. (2000);  108 297-302
    CrossrefPubMedGoogle Scholar
  • 6 Foyer C. H., Descourvieres P., Kunert K. J.. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants.  Plant, Cell and Environment. (1994);  15 507-523
    PubMedGoogle Scholar
  • 7 Foyer C. H., Noctor G.. Oxygen processing in photosynthesis: regulation and signalling.  New Phytologist. (2000);  146 359-388
    CrossrefPubMedGoogle Scholar
  • 8 Fryer M. J.. The antioxidative effect of thylakoid Vitamin E (α-tocopherol).  Plant, Cell and Environment. (1992);  15 381-392
    PubMedGoogle Scholar
  • 10 García-Plazaola J. I., Artetexe U., Duñabeitia M. K., Becerril J. M.. Role of photopreotecitve systems of Holm-Oak (Quercus ilex) in the adaptation to winter conditions.  Journal of Plant Physiology. (1999);  155 625-630
    PubMedGoogle Scholar
  • 11 García-Plazaola J. I., Becerril J. M.. Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings form diverse climatic origins.  Trees. (2000);  14 339-343
    PubMedGoogle Scholar
  • 12 García-Plazaola J. I., Becerril J. M.. Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis.  Australian Journal of Plant Physiology. (2001);  28 225-232
    PubMedGoogle Scholar
  • 13 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);  9 215-226
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Herbinger K., Tausz M., Wonisch A., Soja G., Sorger A., Grill D.. Complex interactive effects of drought and ozone stress on the antioxidant defence systems of two wheat cultivars.  Plant Physiology and Biochemistry. (2002);  40 691-696
    CrossrefPubMedGoogle Scholar
  • 15 Herbinger K., Then Ch., 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 antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure.  Environmental Pollution. (2005);  137 476-482
    CrossrefPubMedGoogle Scholar
  • 18 Johnson J. D., Tognetti R., Michelozzi M., Pinzauti S., Minotta G., Borghetti M.. Ecophysiological responses of Fagus sylvatica L. seedlings to changing light conditions. II. The interaction of light and environment and soil fertility on seedling physiology.  Physiologia Plantarum. (1999);  101 124-134
    PubMedGoogle Scholar
  • 16 Kärenlampi L., Skärby  (eds.) L.. Critical Levels for Ozone in Europe: Testing and Finalizing the Concepts (UN‐ECE Workshop Report), University of Kuopio, Department of Ecology and Environmental Science, Kuopio, Finland. (1996)
    Google Scholar
  • 17 Karnosky D. F., Zak D. R., Pregitzer K. S., Awmack C. S., Bockheim J. G., Dickson R. E., Hendrey G. R., Host G. E., King J. S., Kopper B. J., Kruger E. L., Kubiske M. E., Lindroth R. L., Mattson W. J., McDonald E. P., Noormets A., Oksanen E., Parsons W. F. J., Percy K. E., Podila G. K., Riemenschneider D. E., Sharma P., Thakur R., Sober A., Sober J., Jones W. S., Anttonen S., Vapaavuori E., Mankovska B., Heilman W., Isebrands J. G.. Tropospheric O3 moderates responses of temperate hardwood forest to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project.  Functional Ecological. (2003);  17 289-304
    CrossrefPubMedGoogle Scholar
  • 19 Kolb T. E., Fredricksen T. S., Steiner K. C., Skelly J. M.. Issues in scaling tree size and age responses to ozone: a review.  Environmental Pollution. (1997);  98 159-208
    PubMedGoogle Scholar
  • 20 Kolb T. E., Matyssek R.. Limitations and perspectives about scaling ozone impacts in trees.  Environmental Pollution. (2001);  115 373-393
    CrossrefPubMedGoogle Scholar
  • 21 Löw M., Herbinger K., Nunn A. J., Leuchner M., Heerdt C., Wipfler P., Pretzsch H., Häberle K.-H., Tausz M., Matyssek R.. Extraordinary drought of 2003 overrules ozone impact.  Trees. (2006);  DOI: 10.1007/s00468-006-0069-z
    PubMedGoogle Scholar
  • 22 Lütz C., Anegg S., Gernat D., Alaoui-Sosse B., Gérard J., Dizengremel P.. Beech trees exposed to high CO2 and to simulated summer ozone levels: effets on photosynthesis, chloroplast components and leaf enzyme activity.  Physiologia Plantarum. (2000);  109 252-259
    CrossrefPubMedGoogle Scholar
  • 23 Matyssek R., Innes J. L.. Ozone - a risk factor for forest trees and forests in Europe?.  Water, Air, and Soil Pollution. (1999);  116 199-226
    CrossrefPubMedGoogle Scholar
  • 24 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 26 Müller-Moulé P., Conklin P. L., Niyogi K. K.. Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo.  Plant Physiology. (2002);  128 970-977
    CrossrefPubMedGoogle Scholar
  • 27 Munné-Bosch S., Alegre L.. The function of tocopherols and tocotrienols in plants.  Critical Reviews in Plant Sciences. (2002);  21 31-57
    PubMedGoogle Scholar
  • 28 Munné-Bosch S.. The role of α-tocopherol in plant stress tolerance.  Journal of Plant Physiology. (2005);  162 743-748
    CrossrefPubMedGoogle Scholar
  • 30 Niyogi K. K.. Photoprotection revisited: genetic and molecular approaches.  Annual Review of Plant Physiology and Plant Molecular Biology. (1999);  50 333-359
    CrossrefPubMedGoogle Scholar
  • 29 Nunn A., Reiter I., Häberle K.-H., Werner H., Langebartels C., Sandermann H., Heerdt C., Fabian P., Matyssek R.. “Free-air” ozone canopy fumigation in old-growth mixed forests: concept and observations in beech.  Phyton. (2002);  42 105-119
    PubMedGoogle Scholar
  • 31 Oksanen E.. Physiological responses of birch (Betula pendula) to ozone: a comparison between open-soil-grown trees exposed for six growing seasons and potted seedlings exposed for one growing season.  Tree Physiology. (2003);  23 603-614
    PubMedGoogle Scholar
  • 32 Paludan-Müller G., Saxe H., Leverenz J. W.. Response to ozone in 12 provenances of European beech (Fagus sylvatica): genotypic variation and chamber effects on photosynthesis and dry matter partitioning.  New Phytologist. (1999);  144 261-273
    CrossrefPubMedGoogle Scholar
  • 33 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
  • 34 Pye J. M.. Impact of ozone on tree growth and yield of trees: a review.  Journal of Environmental Quality. (1988);  17 347-391
    PubMedGoogle Scholar
  • 35 Reich P. B.. Quantifying plant response to ozone: a unifying theory.  Tree Physiology. (1987);  3 63-91
    PubMedGoogle Scholar
  • 36 Sandermann H., Wellburn A. R., Heath R. L.. Forest decline and ozone: a comparison of controlled chamber and field experiments. Ecological Studies, Vol. 127. Berlin; Springer-Verlag (1997): 400
    Google Scholar
  • 37 Smirnoff N., Wheeler G. L.. Ascorbic acid in plants: biosynthesis and function.  Critical Reviews in Plant Sciences. (2000);  19 267-290
    CrossrefPubMedGoogle Scholar
  • 38 Strohm M., Eiblmeier M., Langebartels C., Jouanin L., Polle A., Sandermann H., Rennenberg H.. Responses of antioxidative system to acute ozone stress in transgenic popular (Populus tremula × P. alba) over expressing glutathione synthetase or glutathione reductase.  Trees. (2002);  16 262-273
    CrossrefPubMedGoogle Scholar
  • 39 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
    Google Scholar
  • 40 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
    CrossrefPubMedGoogle Scholar
  • 41 Tausz M., Olszyk D. M., Monschein S., Tingey D. T.. Combined effects of CO2 and O3 on antioxidative and photoprotective defense systems in needles of ponderosa pine.  Biologia Plantarum. (2004);  48 543-548
    CrossrefPubMedGoogle Scholar
  • 42 Tegischer K., Tausz M., Grill D., Wieser G.. Tree-age and needle-age dependent variations of antioxidants and photoprotective pigments in spruce needles at the alpine timberline.  Tree Physiology. (2002);  22 591-596
    PubMedGoogle Scholar
  • 43 Thayer S. S., Björkman O.. Leaf xanthophyll content and composition in sun and shade determined by HPLC.  Photosynthesis Research. (1990);  23 331-334
    CrossrefPubMedGoogle Scholar
  • 44 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
    CrossrefPubMedGoogle Scholar
  • 45 Tongetti R., Minotta G., Pinzauti S., Michelozzi M., Borghetti M.. Acclimation to changing light conditions of long-term shade-grown beech (Fagus sylvatica L.) seedlings of different geographic origins.  Trees. (1998);  12 326-333
    CrossrefPubMedGoogle Scholar
  • 46 Wellburn F. A. M., Lau K. K., Milling P. M. K., Wellburn A. R.. Drought and or pollution affect nitrogen cycling and free radical scavenging in Pinus halepensis (Mill.).  Journal of Experimental Botany. (1996);  47 1361-1367
    PubMedGoogle Scholar
  • 47 Wellburn F. A. M., Wellburn A. R.. Variable patterns of antioxidant protection but similar ethane emission differences in several ozone-sensitive and ozone-tolerant plant selections.  Plant, Cell and Environment. (1996);  19 754-760
    CrossrefPubMedGoogle Scholar
  • 48 Werner H., Fabian P.. Free-air fumigation of mature trees.  Environmental Sciences and Pollution Research. (2002);  9 117-121
    PubMedGoogle Scholar
  • 49 Wieser G., Hecke 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 a);  42 245-253
    PubMedGoogle Scholar
  • 50 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 b);  22 583-590
    PubMedGoogle Scholar
  • 51 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.  Annals of Forest Science. (2003);  60 131-135
    CrossrefPubMedGoogle Scholar
  • 52 Wonisch A., Tausz M., Müller M., Soja G., Grill D.. Ozone-induced long-term effects on chromosomal aberration rates in root-tip meristems of spruce trees do not correspond to changes in tissue antioxidant status.  Phyton. (2003);  43 147-160
    PubMedGoogle Scholar
  • 53 Wustman B. A., Oksanen E., Karnosky D. F., Noormets A., Isebrands J. G., Pregitzer K. S., Hendrey G. R., Sober J., Podila G. K.. Effects of elevated CO2 and O3 on aspen clones varying in O3 sensitivity: can CO2 ameliorate the harmful effects of O3?.  Environmental Pollution. (2001);  115 473-481
    CrossrefPubMedGoogle Scholar

K. Herbinger

Institut für Pflanzenwissenschaften
Universität Graz

Schuberstraße 51

8010 Graz

Austria

Email: karin.herbinger@uni-graz.at

Editor: J. T. M. Elzenga