Flux-Based Response of Sucrose and Starch in Leaves of Adult Beech Trees (Fagus sylvatica L.) under Chronic Free-Air O₃ Fumigation

Abstract

Investigations on sucrose and starch contents in leaves of 60-year-old beech trees (Fagus sylvatica L.) are the focus of the present study. Five trees were exposed to a twice ambient ozone regime (2 × O₃) with a free-air canopy exposure system throughout the seasons and five trees under the prevailing ambient ozone regime served as controls (1 × O₃). In order to examine chronic ozone (O₃) effects, Ieaf samples from the sun and shade crowns of the trees were analyzed five times throughout the growing seasons in 2003 and 2004. Sucrose concentrations of leaves collected in 2004 were consistently lower than those taken in 2003, regardless of the O₃ treatment and crown position. However, the opposite was found for starch. O₃ caused a reduction of sucrose and starch contents of sun leaves in both years. Due to the fact that O₃-responsiveness depends on the O₃ uptake through stomata during the season, all carbohydrate data were related to the cumulative O₃ uptake (COU). Little differences were found comparing sucrose and starch contents in leaves of trees grown under ambient or elevated O₃ regimes, possibly indicating the high capacity of leaves of adult beech to cope with rising O₃ exposure. Even under 2 × O₃, leaves were still able to regulate the O₃ intake by narrowing their stomata at the cost of CO₂-uptake and sugar synthesis. In order to clarify whole-tree response patterns carbohydrate data were compared with photosynthesis, stomatal conductance and electron transport rates. In 2004 all parameters revealed a significant common response pattern to COU that indicated a reduction for all parameters under 2 × O₃.

Fagus sylvatica - chronic ozone exposure - starch - sucrose - cumulative ozone uptake - sun and shade crown.

References

• 1 Bahnweg G., Heller W., Stich S., Knappe C., Betz G., Heerdt C., Kehr R. D., Ernst D., Langebartels C., Nunn A. J., Rothenburger J., Schubert R., Wallis P., Müller-Starck G., Werner H., Matyssek R., Sandermann H.. Beech leaf colonization by the endophyte Apiognomonia errabunda dramatically depends on light exposure and climatic conditions.  Plant Biology. (2005);  7 659-669
• 2 Bortier K., De Temmerman L., Ceulemans R.. Effects of ozone exposure in open-top chambers on poplar (Populus nigra) and beech (Fagus sylvatica): a comparison.  Environmental Pollution. (2000);  109 509-516
• 3 Bortier K., Vandermeiren K., De T. 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
• 4 Braun S., Zugmaier U., Thomas V., Flückiger W.. Carbohydrate concentrations in different plant parts of young beech and spruce along a gradient of ozone pollution.  Atmospheric Environment. (2004);  38 2399-2407
• 5 Bytnerowicz A., Godzik B., Grodzinska K., Fraczek W., Musselman R., Manning W., Badea O., Popescu F., Fleischer P.. Ambient ozone in forests of the Central and Eastern European mountains.  Environmental Pollution. (2004);  130 5-16
• 6 Ciais Ph., Reichstein M., Viovy N., Granier A., Ogée J., Allard V., Aubinet M., Buchmann N., Bernhofer Chr., Carrara A., Chevallier F., De Noblet N., Friend A. D., Friedlingstein P., Grünwald T., Heinesch B., Keronen P., Knohl A., Krinner G., Loustau D., Manca G., Matteucci G., Miglietta F., Ourcival J. M., Papale D., Pilegaard K., Rambal S., Seufert G., Soussana J. F., Sanz M. J., Schulze E. D., Vesala T., Valentini R.. Europe-wide reduction in primary productivity caused by the heat and drought in 2003.  Nature. (2005);  437 529-534
• 7 Dizengremel P., Sasek T. W., Brown K. J., Richardson C. J.. Ozone-induced changes in primary carbon metabolism enzymes of loblolly pine needles.  Journal of Plant Physiology. (1994);  144 300-306
• 8 Dizengremel P.. Effects of ozone on the carbon metabolism of forest trees.  Plant Physiology and Biochemistry. (2001);  39 729-742
• 9 Emberson L., Ashmore M., Cambridge H., Simpson D., Tuovinen J.. Modelling stomatal ozone flux across Europe.  Environmental Pollution. (2000);  109 403-413
• 10 Fowler D., Cape J. N., Coyle M., Flechard C., Kuylenstierna J., Hicks K., Derwent D., Johnson C., Stevenson D.. The global exposure of forests to air pollutants.  Water, Air, and Soil Pollution. (1999);  116 5-32
• 11 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
• 12 Herbinger K., Then C., Löw M., Haberer K., Alexous M., Koch N., Remele K., Heerdt C., Grill D., Rennenberg H.. 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);  137 476-482
• 13 Hoch G., Richter A., Körner C.. Non-structural carbon compounds in temperate forest trees.  Plant, Cell and Environment. (2003);  26 1067-1081
• 14 Kaakinen S., Kostiainen K., Ek F., Saranpaa P., Kubiske M. E., Sober J., Karnosky D. F., Vapaavuori E.. Stem wood properties of Populus tremuloides, Betula papyrifera and Acer saccharum saplings after 3 years of treatments to elevated carbon dioxide and ozone.  Global Change Biology. (2004);  10 1513-1525
• 15 Karlsson P. E., Medin E. L., Wickstrom H., Sellden G., Wallin G., Ottosson S., Skärby L.. Ozone and drought stress - interactive effects on the growth and physiology of Norway spruce (Picea abies [L.] Karst).  Water, Air, and Soil Pollution. (1995);  85 1325-1330
• 16 Karlsson P. E., Uddling J., Skärby L., Wallin G., Sellden G.. Impact of ozone on the growth of birch (Betula pendula) saplings.  Environmental Pollution. (2003);  124 485-495
• 17 Karnosky D. F., Percy K. E., Xiang B. X., Callan B., Noormets A., Mankovska B., Hopkin A., Sober J., Jones W., Dickson R. E., Isebrands J. G.. Interacting elevated CO₂ and tropospheric O₃ predisposes aspen (Populus tremuloides Michx.) to infection by rust (Melampsora medusae f. sp tremuloidae).  Global Change Biology. (2002);  8 329-338
• 18 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 forests to elevated CO₂: a synthesis of molecular to ecosystem results from the Aspen FACE project.  Functional Ecology. (2003);  17 289-304
• 19 Karnosky D. F., Pregitzer K. S., Zak D. R., Kubiske M. E., Hendrey G. R., Weinstein D., Nosal M., Percy K. E.. Scaling ozone responses of forest trees to the ecosystem level in a changing climate.  Plant, Cell and Environment. (2005);  28 965-981
• 20 Kolb T. E., Fredericksen T. W., Steiner K. C., Skelly J. M.. Issues in scaling tree size and age responses to ozone: a review.  Environmental Pollution. (1997);  98 195-208
• 21 Kolb T. E., Matyssek R.. Limitations and perspectives about scaling ozone impacts in trees.  Environmental Pollution. (2001);  115 373-393
• 22 Körner C.. Carbon limitation in trees.  Journal of Ecology. (2003);  91 4-17
• 23 Kosola K. R., Dickmann D. I., Paul E. A., Parry D.. Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars.  Oecologia. (2001);  129 65-74
• 24 Kozovits A. R., Matyssek R., Blaschke H., Göttlein A., Grams T. E. E.. Competition increasingly dominates the responsiveness of juvenile beech and spruce to elevated CO₂ and/or O₃ concentrations throughout two subsequent growing seasons.  Global Change Biology. (2005);  11 1387-1401
• 25 Landolt W., Buhlmann U., Bleuler P., Bucher J. B.. Ozone exposure-response relationships for biomass and root/shoot ratio of beech (Fagus sylvatica), ash (Fraxinus excelsior), Norway spruce (Picea abies) and Scots pine (Pinus sylvestris). .  Environmental Pollution. (2000);  109 473-478
• 26 Le Thiec D., Dixon M., Garrec J. P.. The effects of slightly elevated ozone concentrations and mild drought stress on the physiology and growth of norway spruce, (Picea abies [L.] Karst) and Beech, (Fagus sylvatica L.) in open-top chambers.  New Phytologist. (1994);  128 671-678
• 27 Liu W. 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
• 28 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);  DOI: 10.1007/s00468-006-0069-z
• 48 Löw M., Häberle K.-H., Warren C. R., Matyssek R.. O₃ flux-related responsiveness of photosynthesis, respiration, and stomatal conductance of adult Fagus sylvatica to experimentally enhanced free-air O₃ exposure.  Plant Biology. (2007);  9 197-206
• 29 Matyssek R., Innes J. L.. Ozone - a risk factor for trees and forests in Europe?.  Water, Air, and Soil Pollution. (1999);  116 199-226
• 30 Matyssek R., Sandermann H.. Impact of ozone on trees: an ecophysiological perspective.  Progress in Botany. (2003);  64 349-404
• 31 Matyssek R., Wieser G., Nunn A. J., Kozovits A. R., Reiter I. M., Heerdt C., Winkler J. B., Baumgarten M., Häberle K.-H., Grams T. E. E.. Comparison between AOT40 and ozone uptake in forest trees of different species, age and site conditions.  Atmospheric Environment. (2004);  38 2271-2281
• 32 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
• 33 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
• 34 Nunn A. J., Kozovits A. R., Reiter I. M., Heerdt C., Leuchner M., Lütz C., Liu X., Löw M., Winkler J. B., Grams T. E. E., Matyssek R.. Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech (Fagus sylvatica). .  Environmental Pollution. (2005);  137 494-506
• 35 Oßwald W. F., Kraus R., Hippeli S., Benz B., Volpert R., Elstner E. F.. Comparison of the enzymatic activities of dehydroascorbic acid reductase, glutathione reductase, catalase, peroxidase and superoxide dismutase of healthy and damaged spruce needles.  Journal of Plant Physiology. (1992);  139 742-748
• 36 Pääkkonen E., Vahala J., Pohjolai M., Holopainen T., Kärenlampi L.. Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress.  Plant, Cell and Environment. (1998);  21 671-684
• 37 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
• 38 Percy K. E., Awmack C. S., Lindroth R. L., Kubiske M. E., Kopper B. J., Isebrands J. G., Pregitzer K. S., Hendrey G. R., Dickson R. E., Zak D. R., Oksanen E., Sober J., Harrington R., Karnosky D. F.. Altered performance of forest pests under atmospheres enriched by CO₂ and O₃.  Nature. (2002);  420 403-407
• 39 Polle A., Schwanz P., Rudolf C.. Developmental and seasonal changes of stress responsiveness in beech leaves (Fagus sylvatica L.).  Plant, Cell and Environment. (2001);  24 821-829
• 40 Pretzsch H., Kahn M., Grote R.. Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches „Wachstum oder Parasitenabwehr?“ im Kranzberger Forst.  Forstwissenschaftliches Centralblatt. (1998);  117 241-257
• 41 Reichenbacker R. R., Schultz R. C., Hart E. R.. Artificial defoliation effect on Populus growth, biomass production, and total nonstructural carbohydrate concentration.  Environmental Entomology. (1996);  25 632-642
• 42 Saxe H.. Physiological responses of trees to ozone - interactions and mechanisms.  Current Topics in Plant Biology. (2000);  3 27-55
• 43 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
• 44 Smirnoff N.. The function and metabolism of ascorbic acid in plants.  Annals of Botany. (1996);  78 661-669
• 45 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
• 46 Werner H., Fabian P.. Free-air fumigation of adult trees: a novel system for controlled ozone enrichment in grown-up beech and spruce canopies.  Environmental Science and Pollution Research International. (2002);  9 117-121
• 47 Wipfler P., Seifert T., Heerdt C., Werner H., Pretzsch H.. Growth of adult Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica L.) under free-air ozone fumigation.  Plant Biology. (2005);  7 611-618

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