Physiological Responses of Forest Trees to Heat and Drought

H. Rennenberg; F. Loreto; A. Polle; F. Brilli; S. Fares; R. S. Beniwal; A. Gessler

doi:10.1055/s-2006-924084

Plant Biology, Inhaltsverzeichnis

Plant Biol (Stuttg) 2006; 8(5): 556-571
DOI: 10.1055/s-2006-924084

Review Article

Georg Thieme Verlag Stuttgart KG · New York

Physiological Responses of Forest Trees to Heat and Drought

H. Rennenberg¹ , F. Loreto² , A. Polle³ , F. Brilli² , S. Fares² , R. S. Beniwal³ ^, ⁴ , A. Gessler¹

¹Institute of Forest Botany and Tree Physiology, Chair of Tree Physiology, Albert Ludwigs University Freiburg, Georges-Köhler-Allee 53/54, 79110 Freiburg, Germany
²CNR - Istituto di Biologia Agroambientale e Forestale, Via Salaria Km. 29 300, 00016 Monterotondo Scalo (Roma), Italy
³Forstbotanisches Institut, Georg-August-Universität Göttingen, Büsgenweg 2, 37077 Göttingen, Germany
⁴On leave from the Department of Forestry, CCS Haryana Agricultural University, Hisar, Haryana, India

Abstract

The heat wave of summer 2003 was the largest and the most persistent ever experienced in Central Europe and has fuelled concern about the effects of climate change on European ecosystems. Since forests constitute the most important European ecosystems, in this review article we assess current knowledge on the effects of heat and drought on key metabolic processes for growth and productivity of forest trees. In particular, the general consequences of heat and drought on (1) photosynthesis and respiration at the cellular and community level, and (2) on nutrient uptake, partitioning and competition for nutrients are summarized. The latter are a major sink for photosynthetic energy and, therefore, are indirectly but strongly connected to the performance of photosynthesis. In addition, the interaction of heat and drought with stress compensation mechanisms and emission of biogenic volatile organic compounds (BVOC) are discussed, since these processes are directly connected to carbon metabolism. Effects on the emission of BVOC are also included because they constitute an important feedback mechanism on ozone formation and, thus, on atmospheric pollution. As far as available, data collected during the 2003 heat wave are included and discussed.

Key words

Antioxidant systems - competition - global change - nitrogen assimilation - nitrogen uptake - photosynthesis - respiration - stress compensation - volatile organic compounds.

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References

1 Apel K., Hirt H.. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology. (2004); 55 373-399
2 Backes K., Leuschner C.. Leaf water relations of competitive Fagus sylvatica and Quercus petraea trees during 4 years differing in soil drought. Canadian Journal of Forest Research. (2000); 30 335-346
3 Baldi M., Meneguzzo F., Dalu G. A., Maracchi G., Pasqui M., Capecchi V., Crisci A., Piani F.. Guinea Gulf SST and Mediterranean summer climate: analysis of the interannual variability. Proceedings of the 84th AMS Conference, Seattle, WA, USA. (2004)
4 BassiriRad H.. Kinetics of nutrient uptake by roots: responses to global change. New Phytologist. (2000); 147 155-169
5 BassiriRad H., Caldwell M. M., Bilbrough C.. Effects of soil-temperature and nitrogen status on kinetics of ¹⁵NO₃ ^- uptake by roots of field-grown Agropyron-desertorum (Fisch ex Link) Schult. New Phytologist. (1993); 123 485-489
6 BassiriRad H., Radin J. W., Matsuda K.. Temperature-dependent water and ion-transport properties of barley and Sorghum roots. 1. Relationship to leaf growth. Plant Physiology. (1991); 97 426-432
7 BassiriRad H., Thomas R. B., Reynolds J. F., Strain B. R.. Differential responses of root uptake kinetics of NH₄ ⁺ and NO₃ ^- to enriched atmospheric CO₂ concentration in field-grown loblolly pine. Plant, Cell and Environment. (1996); 19 367-371
8 BEMA . A European Commission project on biogenic emissions in the Mediterranean area. Atmospheric Environment. (1997); 31 1-256
9 Bernacchi C. J., Portis A. R., Nakano H., von Caemmerer S., Long S. P.. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology. (2002); 130 1992-1998
10 Berry J., Bjorkman O.. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology. (1980); 31 491-543
11 Bertin N., Staudt M.. Effect of water stress on monoterpene emission from young potted holm oak (Quercus ilex L.) trees. Oecologia. (1996); 107 456-462
12 Bingham I. J., Cumbus I. P.. Influence of root temperature on the potassium requirements of young tomato plants. Plant and Soil. (1991); 133 227-237
13 Bota J., Medrano H., Flexas J.. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress?. New Phytologist. (2004); 162 671-681
14 Brasseur G. P., Chatfield R. B.. The fate of biogenic trace gases in the atmosphere. Sharkey, T. D., Holland, B., and Mooney, H. A., eds. Trace Gas Emissions by Plants. New York; Academic Press (1991): 1-28
15 Bray E.. Classification of genes differentially expressed during water deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Annals of Botany. (2002); 89 803-811
16 Brooks A., Farquhar G. D.. Effects of temperature on the O₂/CO₂ specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Estimates from gas exchange measurements on spinach. Planta. (1985); 165 397-406
17 Buljovcic Z., Engels C.. Nitrate uptake ability by maize roots during and after drought stress. Plant and Soil. (2001); 229 125-135
18 Centritto M., Nascetti P., Petrilli L., Raschi A., Loreto F.. Profiles of isoprene emission and photosynthetic parameters in hybrid exposed to free-air CO₂ enrichment. Plant, Cell and Environment. (2004); 27 403-412
19 Chameides W. L., Lindsay R. W., Richardson J., Kiang C. S.. The role of biogenic hydrocarbons in urban photochemical smog: Atlanta as a case-study. Science. (1988); 241 1473-1475
20 Chapin F. S.. Temperature compensation in phosphate absorption occurring over diverse time scales. Arctic and Alpine Research. (1977); 9 139-148
21 Chapin F. S., Schulze E. D., Mooney H. A.. The ecology and economics of storage in plants. Annual Review of Ecology and Systematics. (1990); 21 423-447
22 Chapin F. S., Vancleve K., Tryon P. R.. Relationship of ion absorption to growth rate in taiga trees. Oecologia. (1986); 69 238-242
23 Chapin F. S. III., Shaver G. R., Giblin A. E., Nadelhoffer K. J., Laundre J. A.. Response of arctic tundra to experimental and observed changes in climate. Ecology. (1995); 76 694-711
24 Ciais P., Viovy N., Reichstein M., Granier A., Ogée J., Allard V., Aubinet M., Bernhofer C., Carrara A., Chevallier F., De Noblet N., Friend A., Grünwald T., Heinesch B., Keronen P., Knohl A., Loustau D., Manca G., Matteucci G., Miglietta F., Ourcival J. M., Pilegaard K., Rambal S., Seufert G., Soussana J.-F., Sanz M.-J., Schulze E. D., Vesala T., Valentini R.. An unprecedented reduction in the primary productivity of Europe during 2003 caused by heat and drought. Nature. (2005); 437 529-533
25 Crafts-Brandner S. J., Salvucci M. E.. Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO₂. Proceedings of the National Academy of Sciences of the USA. (2000); 97 13430-13435
26 Crutzen P. J., Fall R., Galbally I., Lindinger W.. Parameters for global ecosystem models. Nature. (1999); 399 535
27 Cumbus I. P., Nye P. H.. Root zone temperature effects on growth and phosphate absorption in rape Brassica-Napus cv Emerald. Journal of Experimental Botany. (1985); 36 219-227
28 Di Carlo P., Brune W. H., Martinez M., Harder H., Lesher R., Ren X. R., Thornberry T., Carroll M. A., Young V., Shepson P. B., Riemer D., Apel E., Campbell C.. Missing OH reactivity in a forest: evidence for unknown reactive biogenic VOCs. Science. (2004); 304 722-725
29 Dindorf T., Kuhn U., Ganzeveld L., Schebeske G., Ciccioli P., Holke C., Koble R., Seufert G., Kesselmeier J.. Emission of monoterpenes from European beech (Fagus sylvatica L.) as a function of light and temperature. Biogeoscience Discussions. (2005); 2 137-182
30 Dise N. B., Matzner E., Gundersen P.. Synthesis of nitrogen pools and fluxes from European forest ecosystems. Water, Air and Soil Pollution. (1998); 105 143-154
31 Domisch T., Finer L., Lehto T.. Growth, carbohydrate and nutrient allocation of Scots pine seedlings after exposure to simulated low soil temperature in spring. Plant and Soil. (2002 a); 246 75-86
32 Domisch T., Finer L., Lehto T., Smolander A.. Effect of soil temperature on nutrient allocation and mycorrhizas in Scots pine seedlings. Plant and Soil. (2002 b); 239 173-185
33 Feller U., Crafts-Brandner S. J., Salvucci M. E.. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiology. (1998); 116 539-546
34 Flexas J., Bota J., Escalona J. M., Sampol B., Medrano H.. Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology. (2002); 29 461-471
35 Flexas J., Bota J., Loreto F., Cornic G., Sharkey T. D.. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology. (2004); 6 269-279
36 Fotelli M. N., Gessler A., Peuke A. D., Rennenberg H.. Drought affects the competitive interactions between Fagus sylvatica seedlings and an early successional species, Rubus fruticosus: responses of growth, water status and delta C‐13 composition. New Phytologist. (2001); 151 427-435
37 Fotelli M. N., Nahm M., Heidenfelder A., Papen H., Rennenberg H., Gessler A.. Soluble nonprotein nitrogen compounds indicate changes in the nitrogen status of beech seedlings due to climate and thinning. New Phytologist. (2002 a); 154 85-97
38 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 b); 4 311-320
39 Fotelli M. N., Rienks M., Rennenberg H., Gessler A.. Climate and forest management affect N‐15-uptake, N balance and biomass of European beech seedlings. Trees. (2004); 18 157-166
40 Fotelli M. N., Rudolph P., Rennenberg H., Gessler A.. Irradiance and temperature affect the competitive interference of blackberry on the physiology of European beech seedlings. New Phytologist. (2005); 165 453-462
41 Foyer C., Descourvieres P., Kunert K. J.. Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant, Cell and Environment. (1994); 17 507-523
42 Franke W.. Über den Vitamin C Gehalt der Herbstblätter. I. Der Vitamin C Gehalt bis zum Laubabwurf. Zeitschrift für Pflanzenphysiologie. (1965); 53 289-310
43 Garcia-Plazaola J. I., Artetxe U., Becerril J. M.. Diurnal changes in antioxidant and carotenoid composition in the Mediterranean schlerophyll tree Quercus ilex (L) during winter. Plant Science. (1999); 143 125-133
44 Garcia-Plazaola J. I., Becerril J. M.. Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings from diverse climatic origins. Trees. (2000); 14 339-343
45 Garcia-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
46 Gasche R., Papen H.. A 3-year continuous record of nitrogen trace gas fluxes from untreated and limed soil of a N-saturated spruce and beech forest ecosystem in Germany. 2. NO and NO₂ fluxes. Journal of Geophysical Research. (1999); 104 18505-18520
47 Genty B., Briantais J. M., Baker N. R.. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta. (1989); 990 87-92
48 Gessler A., Jung K., Gasche R., Papen H., Heidenfelder A., Börner 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
49 Gessler A., Keitel C., Nahm M., Rennenberg H.. Water shortage affects the water and nitrogen balance in central European beech forests. Plant Biology. (2004 a); 6 289-298
50 Gessler A., Kopriva S., Rennenberg H.. Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiology. (2004 b); 24 1313-1321
51 Gessler A., Kreuzwieser J., Dopatka T., Rennenberg H.. Diurnal courses of ammonium net uptake by the roots of adult beech (Fagus sylvatica) and spruce (Picea abies) trees. Plant and Soil. (2002); 240 23-32
52 Gessler A., Schneider S., Von Sengbusch D., Weber P., Hanemann U., Huber C., Rothe A., Kreutzer K., Rennenberg H.. Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist. (1998 a); 138 275-285
53 Gessler A., Schneider S., Weber P., Hanemann U., Rennenberg H.. Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce (Picea abies) and beech (Fagus sylvatica) trees grown under field conditions. New Phytologist. (1998 b); 138 385-399
54 Godde M., Conrad R.. Influence of soil properties on the turnover of nitric oxide and nitrous oxide by nitrification and denitrification at constant temperature and moisture. Biology and Fertility of Soils. (2000); 32 120-128
55 Grassi G., Millard P., Gioacchini P., Tagliavini M.. Recycling of nitrogen in the xylem of Prunus avium trees starts when spring remobilization of internal reserves declines. Tree Physiology. (2003); 23 1061-1068
56 Guenther A. B., Zimmermann P. R., Harley P. C., Monson R. K., Fall R.. Isoprene and monoterpene emission rate variability: model evaluations and sensitivity analysis. Journal of Geophysical Research. (1993); 98 12609-12617
57 Guenther A., Hewitt C. N., Erickson D., Fall R., Geron C., Graedel T., Harley P., Klinger L., Lerdau M., McKay W. A., Pierce T., Scholes B., Steinbrecher R., Tallamraju R., Taylor J., Zimmerman P.. A global model of natural volatile organic compound emissions. Journal of Geophysical Research. (1995); 100 8873-8892
58 Gunderson C. A., Norby R. J., Wullschleger S. D.. Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field experiments. Tree Physiology. (2000); 20 87-96
59 Haldimann P., Feller U.. Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant, Cell and Environment. (2004); 27 1169-1183
60 Hansen U., Fiedler B., Rank B.. Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees. (2002); 16 354-364
61 Hare P. D., Cress W. A., Van Staden J. V.. Dissecting the roles of osmolyte accumulation during stress. Plant, Cell and Environment. (1998); 21 535-553
62 Havaux M.. Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science. (1998); 3 147-151
63 Holopainen J. K.. Multiple functions of inducible plant volatiles. Trends in Plant Science. (2004); 9 529-533
64 IPCC .Climate change 2001: IPCC third assessment report. Intergovernmental Panel on Climate Change. http://www.grida.no/climate/ipcc_tar/ Cambridge; Cambridge University Press (2001)
65 Kavouras L. G., Mihalopoulos N., Stephanou E. G.. Formation of atmospheric particles from organic acids produced by forests. Nature. (1998); 395 683-686
66 Kesselmeier J., Staudt M.. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. Journal of Atmospheric Chemistry. (1999); 33 23-88
67 Kobza J., Edwards G. E.. Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology. (1987); 83 69-74
68 Kunert K., Ederer M.. Leaf ageing and lipid peroxidation: the role of the antioxidants vitamin C and E. Plant Physiology. (1986); 65 85-88
69 Labeke M. C., van Degeyter L., Fernandez T., Davidson C. G.. Non-structural carbohydrate content as an aid for interpreting quality testing of nursery stock plants. Acta Horticulturae. (2004); 630 191-198
70 Laine P., Bigot J., Ourry A., Boucaud J.. Effects of low-temperature on nitrate uptake, and xylem and phloem flows of nitrogen in Secale cereale L. and Brassica napus L. New Phytologist. (1994); 127 675-683
71 Laine P., Ourry A., Macduff J., Boucaud J., Salette J.. Kinetic parameters of nitrate uptake by different catch crop species - effects of low temperatures or previous nitrate starvation. Physiologia Plantarum. (1993); 88 85-92
72 Lal R.. World soils and the greenhouse effect. IGBP Newsletter. (1999); 37 4-5
73 Law R., Crafts-Brandner S. J.. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology. (1999); 120 173-182
74 Lea P. J., Leegood R. C.. Plant Biochemistry and Molecular Biology. Chichester, UK; Wiley (1999)
75 Lichtenthaler H. K., Schwendler J., Disch A., Rohmer M.. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Letters. (1997); 400 271-274
76 Long S. P., Ainsworth E. A., Rogers A., Ort D. R.. Rising atmospheric carbon dioxide: plants FACE the future. Annual Reviews in Plant Biology. (2004); 55 591-628
77 Loreto F., Sharkey T. D.. A gas exchange study of photosynthesis and isoprene emission in red oak (Quercus rubra L.). Planta. (1990); 182 523-531
78 Loreto F., Ciccioli P., Cecinato A., Brancaleoni E., Frattoni M., Tricoli D.. Influence of environmental factors and air composition on the emission of α-pinene from Quercus ilex leaves. Plant Physiology. (1996); 110 267-275
79 Loreto F., Velikova V., Di Marco G.. Respiration in the light measured by ¹²CO₂ emission in ¹³CO₂ atmosphere in maize leaves. Austalian Journal of Plant Physiology. (2001 a); 28 1103-1108
80 Loreto F., Fischbach R. J., Schnitzler J.-P., Ciccioli P., Brancaleoni E., Calfapietra C., Seufert G.. Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L. grown at elevated CO₂ concentrations. Global Change Biology. (2001 b); 7 709-717
81 Loreto F., Velikova V.. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology. (2001); 127 1781-1787
82 Loreto F.. Distribution of isoprenoid emitters in the Quercus genus around the world: chemo-taxonomical implications and evolutionary considerations based on the ecological function of the trait. Perspectives in Plant Ecology, Evolution and Systematics. (2002); 5 185-192
83 Loreto F., Pinelli P., Manes F., Kollist H.. Impact of ozone on monoterpene emissions and evidences for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex (L.) leaves. Tree Physiology. (2004); 24 361-367
84 Loreto F., Centritto M.. Photosynthesis in a changing world. Plant Biology. (2004); 6 239-241
85 Luwe M.. Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentrations in air. Plant, Cell and Environment. (1996); 19 321-328
86 Marschner H., Haussling M., George E.. Ammonium and nitrate uptake rates and rhizosphere pH in nonmycorrhizal roots of Norway spruce (Picea abies [L] Karst). Trees. (1991); 5 14-21
87 McNeil S. D., Nuccio M. L., Hanson A. D.. Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiology. (1999); 120 945-949
88 Munné-Bosch S., Alegre L.. Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta. (2000 a); 210 925-931
89 Munné-Bosch S., Alegre L.. The significance of β-carotene, α-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Australian Journal of Plant Physiology. (2000 b); 27 139-146
90 Munné-Bosch S., Peñuelas J.. Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Science. (2004); 166 1105-1110
91 Nahm M., Matzarakis A., Rennenberg H., Gessler A.. Seasonal courses of key parameters of nitrogen, carbon and water balance in European beech (Fagus sylvatica L.) grown on four different study sites along a European North-South climate gradient during the 2003 drought. Trees. (2006); in press
92 Niyogi K. K.. Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology. (1999); 50 333-359
93 Norby R. J.. Interactions between increasing CO₂ and temperature in terrestrial ecosystems: a conceptual framework. TERACC Workshop Interactions Between Increasing CO₂ and Temperature in Terrestrial Ecosystems. Lake Tahoe, CA, USA, April, 2003. http://www.esd.ornl.gov/facilities/ORNL-FACE/pubs.html. (2003)
94 Nordin A., Uggla C., Nasholm T.. Nitrogen forms in bark, wood and foliage of nitrogen-fertilized Pinus sylvestris. Tree Physiology. (2001); 21 59-64
95 Osmond B., Badger M., Maxwell K., Bjorkman O., Leegood R.. Too many photons: photorespiration, photoinhibition and photooxidation. Trends in Plant Science. (1997); 2 119-121
96 Peltzer D.. Anpassung antioxidativer Systeme an Licht und Temperatur: holzige und krautige Pflanzen im Vergleich. Online-Dissertation. Institut für Forstbotanik, Universität Göttingen (2001)
97 Peltzer D., Dreyer E., Polle A.. Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiology and Biochemistry. (2002); 40 141-150
98 Peltzer D., Polle A.. Diurnal fluctuations of antioxidative systems in leaves of field-grown beech trees (Fagus sylvatica): responses to light and temperature. Physiologia Plantarum. (2001); 111 158-163
99 Peñuelas J., Llusià J.. Linking photorespiration, monoterpenes and thermotolerance in Quercus. New Phytologist. (2002); 155 227-237
100 Perry M. A., Mitchell R. J., Zutter B. R., Glover G. R., Gjerstad D. H.. Seasonal variation in competitive effects on water-stress and pine responses. Canadian Journal of Forest Research. (1994); 24 1440-1449
101 Peuke A. D., Schraml C., Hartung W., Rennenberg H.. Identification of drought sensitive beech ecotype by physiological parameters. New Phytologist. (2002); 154 373-387
102 Pinelli P., Loreto F.. ¹²CO₂ emission from different metabolic pathways measured in illuminated and darkened C3 and C4 leaves at low, atmospheric, and elevated CO₂ concentration. Journal of Experimental Botany. (2003); 54 1761-1769
103 Polle A.. Defense against photooxidative damage in plants. Scandalios, J., ed. Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Cold Spring Harbour; Cold Spring Harbour Laboratory Press (1997): 623-666
104 Polle A.. Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiology. (2001); 126 445-462
105 Polle A., Morawe B.. Properties of ascorbate-related enzyme activities in foliar extracts from beech (Fagus sylvatica, L.). Phyton. (1995 a); 35 117-129
106 Polle A., Morawe B.. Seasonal changes of antioxidative systems in foliar buds and leaves of field grown beech trees (Fagus sylvatica L.) in a stressful climate. Botanica Acta. (1995 b); 108 314-320
107 Polle A., Rennenberg H.. Photo-oxidative stress in plants: causes and amelioration. Foyer, C. and Mullineaux, P., eds. Photooxidative Stresses in Trees. Boca Raton; CRC Press Inc. (1994): 199-218
108 Polle A., Altman A., Jiang X.. Towards genetic engineering for drought tolerance in trees. Fladung, M. and Ewald, D., eds. Recent Developments in Tree Transgenesis. Heidelberg; Springer Verlag, in press (2006)
109 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
110 Rapparini F., Baraldi R., Miglietta F., Loreto F.. Isoprenoid emission in trees of Quercus pubescens and Quercus ilex with lifetime exposure to naturally high CO₂ environment. Plant, Cell and Environment. (2004); 27 381-391
111 Rennenberg H., Kreutzer K., Papen H., Weber P.. Consequences of high loads of nitrogen for spruce (Picea abies) and beech (Fagus sylvatica) forests. New Phytologist. (1998); 139 71-86
112 Robertson K., Klemedtsson L.. Assessment of denitrification in organogenic forest soil by regulating factors. Plant and Soil. (1996); 178 49-57
113 Rosenstiel T. N., Potosnak M. J., Griffin K. L., Fall R., Monson R. K.. Increased CO₂ uncouples growth from isoprene emission in an agriforest ecosystem. Nature. (2003); 421 256-259
114 Salvucci M. E., Crafts-Brandner S. J.. Mechanisms for deactivation of Rubisco under moderate heat stress. Physiologia Plantarum. (2004); 122 513-519
115 Schaer C., Vidale P. L., Luethi D., Frei C., Haeberli C., Liniger M. A., Appenzeller C.. Variability in European summer heatwaves. Nature. (2004); 427 332-336
116 Schmidt S., Stewart G. R.. Transport, storage and mobilization of nitrogen by trees and shrubs in the wet/dry tropics of northern Australia. Tree Physiology. (1998); 18 403-410
117 Schönwiese C.-D., Staeger T., Trömel S.. The hot summer 2003 in Germany. Some preliminary results of a statistical time series analysis. Meteorologische Zeitschrift. (2004); 13 323-327
118 Scholefield P. A., Doick K. J., Herbert B., Hewitt C. N., Schnitzler J.-P., Pinelli P., Loreto F.. Impact of rising CO₂ on VOC emissions: isoprene emission from Phragmites australis growing at elevated CO₂ in a natural carbon dioxide spring. Plant, Cell and Environment. (2004); 27 393-401
119 Schrader S. M., Wise R. R., Wacholtz W. F., Ort D. R., Sharkey T. D.. Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant, Cell and Environment. (2004); 27 725-735
120 Schraml C., Rennenberg H.. Sensitivity of different ecotypes of beech (Fagus sylvatica) to drought stress. Forstwissenschaftliches Centralblatt. (2000); 119 51-61
121 Sharkey T. D., Loreto F., Delwiche C. F.. The biochemistry of isoprene emission from leaves during photosynthesis. Sharkey, T. D., Holland, B., and Mooney, H. A., eds. Trace Gas Emissions by Plants. New York; Academic Press Publ. (1991): 153-184
122 Sharkey T. D., Loreto F.. Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia. (1993); 95 328-333
123 Sharkey T. D.. Isoprene synthesis by plants and animals. Endeavour. (1996); 2 74-78
124 Shi L., Guttenberger M., Kottke I., Hampp R.. The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza. (2002); 12 303-311
125 Singsaas E. L., Lerdau M., Winter K., Sharkey T. D.. Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiology. (1997); 115 1413-1420
126 Smart D. R., Bloom A. J.. Influence of root NH₄ ⁺ and NO₃ ^- content on the temperature response of net NH₄ ⁺ and NO₃ ^- uptake in chilling sensitive and chilling resistant lycopersicon taxa. Journal of Experimental Botany. (1991); 42 331-338
127 Steinbrecher R., Hauff K., Rabong R., Steinbrecher J.. Isoprenoid emission of oak species typical for the Mediterranean area: Source strength and controlling variables. Atmospheric Environment. (1997); 31 (Suppl. 1) 79-88
128 Sunkar R., Bartels D., Kirch H. H.. Overexpression of a stress-induced aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. The Plant Journal. (2003); 35 452-464
129 Tezara W., Mitchell V. J., Driscoll S. D., Lawlor D. W.. Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature. (1999); 401 914-917
130 Tognetti R., Johnson J. D., Michelozzi M.. The response of European beech (Fagus sylvatica L.) seedlings from two Italian populations to drought and recovery. Trees. (1995); 9 348-354
131 Valentini R., Matteucci G., Dolman A. J., Schulze E. D., Rebmann C., Moors E. J., Granier A., Gross P., Jensen N. O., Pilegaard K., Lindroth A., Grelle A., Bernhofer C., Grunwald T., Aubinet M., Ceulemans R., Kowalski A. S., Vesala T., Rannik U., Berbigier P., Loustau D., Guomundsson J., Thorgeirsson H., Ibrom A., Morgenstern K., Clement R., Moncrieff J., Montagnani L., Minerbi S., Jarvis P. G.. Respiration as the main determinant of carbon balance in European forests. Nature. (2000); 404 861-865
132 Vassey T. L., Sharkey T. D.. Mild water stress of Phaseolus vulgaris plants leads to reduced starch synthesis and extractable sucrose phosphate activity. Plant Physiology. (1989); 89 1066-1070
133 Wang W. X., Pelah D., Alergand T., Shoseyov O., Altman A.. Characterisation of SP1, a stress-responsive, boiling soluble, homo-oligomeric protein from aspen. Plant Physiology. (2002); 130 865-875
134 Yordanov I., Dilova S., Petkova R., Pangelova T., Goltsev V., Suess K. H.. Mechanisms of the temperature damage and accliation of the photosynthetic apparatus. Photobiochemistry and Photobiophysics. (1986); 12 147-155

H. Rennenberg

Institute of Forest Botany and Tree Physiology
Chair of Tree Physiology
Albert Ludwigs University Freiburg

Georges-Köhler-Allee 53/54

79110 Freiburg

Germany

eMail: heinz.rennenberg@ctp.uni-freiburg.de

Editor: J. T. M. Elzenga