Comparison of Isoprene Emission, Intercellular Isoprene Concentration and Photosynthetic Performance in Water-Limited Oak (Quercus pubescens Willd. and Quercus robur L.) Saplings

Abstract

The influence of prolonged water limitation on leaf gas exchange, isoprene emission, isoprene synthase activities and intercellular isoprene concentrations was investigated under standard conditions (30 °C leaf temperature and 1000 μmol photons m^-2 s^-1 PPFD) in greenhouse experiments with five-year-old pubescent oak (Quercus pubescens Willd.) and four-year-old pedunculate oak (Quercus robur L.) saplings. Net assimilation rates proved to be highly sensitive to moderate drought in both oak species, and were virtually zero at water potentials (Ψ_pd) below - 1.3 MPa in Q. robur and below - 2.5 MPa in Q. pubescens. The response of stomatal conductance to water stress was slightly less distinct. Isoprene emission was much more resistant to drought and declined significantly only at Ψ_pd below - 2 MPa in Q. robur and below - 3.5 MPa in Q. pubescens. Even during the most severe water stress, isoprene emission of drought-stressed saplings was still approximately one-third of the control in Q. robur and one-fifth in Q. pubescens. Isoprene synthase activities were virtually unaffected by drought stress. Re-watering led to partial recovery of leaf gas exchange and isoprene emission. Intercellular isoprene concentrations were remarkably enhanced in water-limited saplings of both oak species during the first half of the respective drought periods with maximum mean values up to ca. 16 μl l^-1 isoprene for Q. pubescens and ca. 11 μl l^-1 isoprene for pedunculate oak, supporting the hypothesis that isoprene serves as a short-term thermoprotective agent in isoprene-emitting plant species.

Drought - isoprene emission - isoprene synthase - oak - photosynthesis - Quercus pubescens - Quercus robur

References

• 1 Bertin,  N., and Staudt,  M.. (1996);  Effect of water stress on monoterpene emissions from young potted holm oak (Quercus ilex L.) trees.  Oecologia. 107 456-462
• 2 Biesenthal,  T. A.,, Wu,  Q.,, Shepson,  P. B.,, Wiebe,  H. A.,, Anlauf,  K. G.,, and MacKay,  G. I.. (1997);  A study of relationships between isoprene, its oxidation products, and ozone, in the lower Fraser valley, BC.  Atmos. Environ.. 31 2049-2058
• 3 Bradford,  M. M.. (1976);  A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.  Analyt. Biochem.. 72 248-254
• 4 Brüggemann,  N.. (2002) Untersuchungen zur Regulation der Isoprenbildung bei Eichen. PhD-Thesis, University of Freiburg, Schriftenreihe des Fraunhofer-Instituts Atmosphärische Umweltforschung. Garmisch-Partenkirchen, Band 70-2002, ISBN 3-8265-9848-2. Aachen, Germany; Shaker Verlag
• 5 Brüggemann,  N., and Schnitzler,  J.-P.. (2001);  Influence of powdery mildew (Microsphaera alphitoides) on isoprene biosynthesis and emission of pedunculate oak (Quercus robur L.) leaves.  J. Appl. Bot.. 75 91-96
• 6 Damesin,  C., and Rambal,  S.. (1995);  Field study of leaf photosynthetic performance by a Mediterranean deciduous oak tree (Quercus pubescens) during a severe summer drought.  New Phytol.. 131 159-167
• 7 Fall,  R., and Monson,  R. K.. (1992);  Isoprene emission rate and intercellular isoprene concentration as influenced by stomatal distribution and conductance.  Plant Physiol. . 100 987-992
• 8 Fang,  C.,, Monson,  R. K.,, and Cowling,  E. B.. (1996);  Isoprene emission, photosynthesis, and growth in sweetgum (Liquidambar styraciflua) seedlings exposed to short- and long-term drying cycles.  Tree Physiol.. 16 441-446
• 9 Fehsenfeld,  F.,, Calvert,  J.,, Fall,  R.,, Goldan,  P.,, Guenther,  A. B.,, Hewitt,  C. N.,, Lamb,  B.,, Liu,  S.,, Trainer,  M.,, Westberg,  H., et al.. (1992);  Emissions of volatile organic compounds from vegetation and the implications for atmospheric chemistry.  Global. Biogeochem. Cycl.. 6 389-430
• 10 Filella,  I.,, Llusià,  J.,, Piñol,  J.,, and Peñuelas,  J.. (1998);  Leaf gas exchange of Phillyrea latifolia, Pistacia lentiscus and Quercus ilex saplings in severe drought and high light conditions.  Environ. Exper. Bot.. 39 213-220
• 11 Hills,  A. J., and Zimmermann,  P. R.. (1990);  Isoprene measurement by ozone induced chemiluminescence.  Analyt. Chem.. 62 1055-1060
• 12 Ingestad,  T.. (1959);  Studies on the nutrition of forest tree seedlings. II. Mineral nutrition of spruce.  Physiol. Plant.. 12 568-593
• 13 IPCC .(2001) Climate change 2001: The scientific basis. IPCC Third Assessment Report. Geneva, Switzerland; IPCC Secretariat
• 14 Kesselmeier,  J., and Staudt,  M.. (1999);  Biogenic volatile organic compounds (VOCs): An overview on emission, physiology, and ecology.  J. Atmos. Chem.. 33 23-88
• 15 Lehning,  A.,, Zimmer,  I.,, Steinbrecher,  R.,, Brüggemann,  N.,, and Schnitzler,  J.-P.. (1999);  Isoprene synthase activity and its relation to isoprene emission in Quercus robur L. leaves.  Plant Cell Environ.. 22 495-504
• 16 Lichtenthaler,  H. K.. (1999);  The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 50 47-66
• 17 Loreto,  F.,, Förster,  A.,, Dürr,  M.,, Csiky,  O.,, and Seufert,  G.. (1998);  On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes.  Plant Cell Environ.. 21 101-107
• 18 Loreto,  F.,, Mannozzi,  M.,, Maris,  C.,, Nascetti,  P.,, Ferranti,  F.,, and Pasqualini,  S.. (2001);  Ozone quenching properties of isoprene and its antioxidant role in leaves.  Plant Physiol.. 126 993-1000
• 19 Méthy,  M.,, Damesin,  C.,, and Rambal,  S.. (1996);  Drought and photosystem II activity in two Mediterranean oaks.  Ann. Sci. For.. 53 255-262
• 20 Monson,  R. K.,, Jaeger,  C. H.,, Adams III,  W. W.,, Driggers,  E. M.,, Silver,  G. M.,, and Fall,  R.. (1992);  Relationship among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature.  Plant Physiol.. 98 1175-1180
• 21 Peñuelas,  J.. (1996);  Overview on current and past global changes in the Mediterranean ecosystems.  Orsis. 11 165-176
• 22 Picon,  C.,, Fehri,  A.,, and Guehl,  J. M.. (1997);  Concentration and delta C-13 of leaf carbohydrates in relation to gas exchange in Quercus robur under elevated CO₂ and drought.  J. Exp. Bot.. 48 1547-1556
• 23 Rohmer,  M.,, Knani,  M.,, Simonin,  P.,, Sutter,  B.,, and Sahm,  H.. (1993);  Isoprenoid biosynthesis in bacteria: a novel pathway for early steps leading to isopentenyl diphosphate.  Biochem. J.. 295 517-524
• 24 Scholander,  P. F.,, Hammel,  H. F.,, Bradstreet,  E.,, and Hemmingsen,  E. A.. (1965);  Sap pressure in plants.  Science. 148 339-346
• 25 Schwarz,  O.. (1936) Monographie der Eichen Europas und des Mittelmeergebietes. Feddes Repertorium regni vegetabilis.  Berlin-Dahlem, Germany; Sonderbeiheft D
• 26 Schwender,  J.,, Zeidler,  J.,, Gröner,  R.,, Müller,  C.,, Frocke,  M.,, Braun,  S.,, Lichtenthaler,  F. W.,, and Lichtenthaler,  H. K.. (1997);  Incorporation of 1-deoxy-D-xylulose into isoprene and phytol by higher plants and algae.  FEBS Lett.. 414 129-134
• 27 Seegmüller,  S.,, Schulte,  M.,, Herschbach,  C.,, and Rennenberg,  H.. (1998);  Interactive effects of mycorrhization and elevated atmospheric CO₂ on sulphur nutrition of young pedunculate oak (Quercus robur L.) trees.  Plant Cell Environ. . 19 418-426
• 28 Sharkey,  T. D.,, Chen,  X.,, and Yeh,  S.. (2001);  Isoprene increases thermotolerance of fosmidomycin-fed leaves.  Plant Physiol.. 125 2001-2006
• 29 Sharkey,  T. D., and Loreto,  F.. (1993);  Water stress, temperature and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves.  Oecologia. 343 1-6
• 30 Sharkey,  T. D., and Yeh,  S.. (2001);  Isoprene emission from plants.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 52 407-436
• 31 Silver,  G. M., and Fall,  R.. (1991);  Enzymatic synthesis of isoprene from dimethylallyl diphosphate in aspen leaf extracts.  Plant Physiol.. 97 1588-1591
• 32 Simpson,  D.,, Guenther,  A.,, Hewitt,  C. N.,, and Steinbrecher,  R.. (1995);  Biogenic emissions in Europe. 1. Estimates and uncertainties.  J. Geophys. Res.. 100 22875-22890
• 33 Singsaas,  E. L.,, Lerdau,  M.,, Winter,  K.,, and Sharkey,  T. D.. (1997);  Isoprene increases thermotolerance of isoprene-emitting species.  Plant Physiol.. 115 1413-1420
• 34 Singsaas,  E. L., and Sharkey,  T. D.. (1998);  The regulation of isoprene emission responses to rapid leaf temperature fluctuations.  Plant Cell Environ.. 21 1181-1188
• 35 Singsaas,  E. L., and Sharkey,  T. D.. (2000);  The effect of high temperature on isoprene synthesis in oak leaves.  Plant Cell Environ.. 23 751-757
• 36 Thompson,  A. M.. (1992);  The oxidizing capacity of the Earth's atmosphere: probable past and future changes.  Science. 256 1157-1165
• 37 Tingey,  D. T.,, Evans,  R.,, and Gumpertz,  M.. (1981);  Effects of environmental conditions on isoprene emission from live oak.  Planta. 152 565-570
• 38 Trainer,  M.,, Williams,  E. J.,, Parrish,  D. D.,, Buhr,  M. P.,, Allwine,  E. J.,, Westberg,  H. H.,, Fehsenfeld,  F. C.,, and Liu,  S. C.. (1987);  Models and observations of the impact of natural hydrocarbons on rural ozone.  Nature. 329 705-707
• 39 Tyree,  M. T., and Ewers,  F. W.. (1991);  Tansley Review No. 34: The hydraulic architecture of trees and other woody plants.  New Phytol.. 119 345-360
• 40 von Caemmerer,  S., and Farquhar,  G. D.. (1981);  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.  Planta. 153 376-387
• 41 Wildermuth,  M. C., and Fall,  R.. (1996);  Light-dependent isoprene emission. Characterization of a thylakoid-bound isoprene synthase in Salix discolor chloroplasts.  Plant Physiol.. 112 171-182
• 42 Wildermuth,  M. C., and Fall,  R.. (1998);  Biochemical characterization of stromal and thylakoid-bound isoforms of isoprene synthase in willow leaves.  Plant Physiol.. 116 1111-1123
• 43 Zimmer,  W.,, Brüggemann,  N.,, Emeis,  S.,, Giersch,  C.,, Lehning,  A., , Steinbrecher,  R., , and Schnitzler,  J.-P.. (2000);  Process-based modelling of isoprene emission by oak leaves.  Plant Cell Environ.. 23 585-595

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