Stomatal Uptake and Stomatal Deposition of Ozone in Isoprene and Monoterpene Emitting Plants

Abstract

Volatile isoprenoids were reported to protect plants against ozone. To understand whether this could be the result of a direct scavenging of ozone by these molecules, the stomatal and non-stomatal uptake of ozone was estimated in plants emitting isoprene or monoterpenes. Ozone uptake by holm oak (Quercus ilex, a monoterpene emitter) and black poplar (Populus nigra, an isoprene emitter) was studied in whole plant enclosures (continuously stirred tank reactors, CSTR). The ozone uptake by plants was estimated measuring ozone concentration at the inlet and outlet of the reactors, after correcting for the uptake of the enclosure materials. Destruction of ozone at the cuticle or at the plant stems was found to be negligible compared to the ozone uptake through the stomata. For both plant species, a relationship between stomatal conductance and ozone uptake was found. For the poplar, the measured ozone losses were explained by the uptake of ozone through the stomata only, and ozone destruction by gas phase reactions with isoprene was negligible. For the oak, gas phase reactions of ozone with the monoterpenes emitted by the plants contributed significantly to ozone destruction. This was confirmed by two different experiments showing a) that in cases of high stomatal conductance but under low CO₂ concentration, a reduction of monoterpene emission was still associated with reduced O₃ uptake; and b) that ozone losses due to the gas phase reactions only can be measured when using the exhaust from a plant chamber to determine the gas phase reactivity in an empty reaction chamber. Monoterpenes can therefore relevantly scavenge ozone at leaf level contributing to protection against ozone.

Key words

Ozone uptake - stomatal conductance - isoprene - monoterpenes - photosynthesis - reaction chambers.

References

• 1 Altimir N., Kolari P., Tuovinen J. P., Vesala T., Back J., Suni T., Kulmala M., Hari P.. Foliage surface ozone deposition: a role for surface moisture?.  Biogeosciences. (2006);  3 209-228
• 2 Asada K.. Ascorbate peroxidase – a hydrogen peroxide scavenging enzyme in plants.  Physiologia Plantarum. (1992);  85 235-241
• 3 Atkinson R., Arey J., Corchonoy S., Shu Y.. Rate constants for the gas phase reactions of cis-3-hexen-1-ol, cis-3-hexenylacetate, trans-2-hexenal, and linalool with OH and NO₃ radicals and O₃ at 296 ± 2K, and OH radical formation yields from the O₃ reactions.  International Journal of Chemical Kinetics. (1995);  27 941-955
• 4 Atkinson R.. Gas-phase tropospheric chemistry of volatile organic compounds. 1. Alkanes and alkenes.  Journal of Physical and Chemical Reference Data. (1997);  26 215-290
• 5 Beauchamp J., Wisthaler A., Hansel A., Kleist E., Miebach M., Nienemets U., Schurr U., Wildt J.. Ozone induced emissions of biogenic VOC from tobacco: relationships between ozone uptake and emission of LOX products.  Plant, Cell and Environment. (2005);  28 1334-1343
• 6 Bonn B., Moortgat G. K.. Sesquiterpene ozonolysis: origin of atmospheric new particle formation from biogenic hydrocarbons.  Geophys Research Letters. (2003);  30 1585
• 7 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
• 8 Fares S., Barta C., Ederli L., Ferranti F., Pasqualini S., Reale L., Brilli F., Tricoli D., Loreto F.. Impact of high ozone on isoprene emission and some anatomical and physiological parameters of developing Populus alba leaves directly or indirectly exposed to the pollutant.  Physiologia Plantarum. (2006);  128 456-465
• 9 Filella I., Penuelas J., Ribas A.. Using plant biomonitors and flux modelling to develop O₃ dose-response relationship in Catalogna.  Environmental Pollution. (2005);  134 145-151
• 10 Fowler D., Flechard C., Cape J. N., Storeton-West R. L., Coyle M.. Measurements of ozone deposition to vegetation quantifying the flux, the stomatal and non-stomatal components.  Water and Soil Pollution. (2001);  130 63-74
• 11 Fredericksen T. S., Kolb T. E., Skelly J. M., Steiner K. C., Joyce B. J., Savage J. E.. Light environment alters ozone uptake per net photosynthetic rate in black cherry trees.  Tree Physiology. (1996);  16 485-490
• 12 Fuhrer J., Skärby L., Ashmore M. R.. Critical levels for ozone effects on vegetation in Europe.  Environmental Pollution. (1997);  97 91-106
• 13 Guenther A. B., Hewitt C. N., Erikson D., Fall R., Geron C., Gradel 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 – Atmospheres. (1995);  100 8873-8892
• 14 Heiden A. C., Kobel K., Langebartels C., Schuh-Thomas G., Wildt J.. Emission of oxigenated volatile organic compounds from plants. Part I: Emssion from lipoxygenase activity.  Journal of Atmospheric Chemistry. (2003);  45 143-172
• 15 Heiden A. C., Kahl J., Kley D., Klockow D., Langebartels C., Melhorn H., Sanderman  Jr. H., Schraudner M., Schih G., Wildt J.. Emission of volatile organic compounds from ozone-exposed plants.  Ecological Applications. (1999);  94 1160-1167
• 16 Kurpius M. R., Goldstein A. H.. Gas-phase chemistry dominates O₃ loss to a forest, implying a source of aerosol and hydroxyl radicals to the atmosphere.  Geophysical Research Letters. (2003);  30 1371
• 17 Laisk A., Kull O., Moldau H.. Ozone concentration in leaf intercellular air spaces is close to zero.  Plant Physiology. (1989);  90 1163-1167
• 18 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
• 19 Loreto F., Pinelli P., Manes F., Kollist H.. Impact of ozone on monoterpene emission and evidence for an isoprene-like antioxidant action of monoterpens emitted by Quercus ilex leaves.  Tree Physiology. (2004);  24 361-367
• 20 Loreto F., Ferranti F., Mannozzi M., Maris C., Nascetti P., Pasqualini S.. Ozone quenching proprieties of isoprene and its antioxidant role in plants.  Plant Physiology. (2001);  126 993-1000
• 21 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
• 22 Loreto F., Ciccioli P., Cucinato A., Brancaleoni E., Frattoni F., Fabozzi C., Tricoli D.. Evidence of the photosynthetic origin of monoterpenes emitted by Quercus ilex L. leaves by ¹³C labeling.  Plant Physiology. (1996);  110 1317-1322
• 34 Loreto F., Barta C., Brilli F., Noguès I.. On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature.  Plant, Cell and Environment. (2006);  29 1820-1828
• 23 Loreto F., Fares S.. Is ozone flux inside leaves only a damage indicator? Clues from volatile isoprenoid studies.  Plant Physiology. (2007);  143 1096-1100
• 24 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
• 25 Marrero E. A., Mason T. R.. Gaseous diffusion coefficients.  Journal of Physical and Chemical Reference Data. (1972);  1 1-118
• 26 Matyssek R., Sandermann  Jr. H.. Impact of ozone on trees: an ecophysiological perspective.  Progress in Botany. (2003);  64 349-404
• 27 Musselman R. C., Minnick T. J.. Nocturnal stomatal conductance and ambient air quality standards for ozone.  Atmospheric Environment. (2000);  34 719-733
• 28 Neubert A., Kley D., Wildt J., Segschneider H. J., Förstel H.. Uptake of NO, NO₂ and O₃ by sunflower (Helianthus annuus L.) and tobacco plants (Nicotiana tabacum L.): dependence on stomatal conductance.  Atmospheric Environment. (1993);  27 1137-1145
• 29 Orlando J. J., Noziere B., Tyndall G. S., Orzechowska G. E., Paulson S. E., Rudich Y.. Product studies of the OH- and ozone-initiated oxidation of some monoterpenes.  Journal of Geophysical Research – Atmospheres. (2000);  105 (D9) 11561-11572
• 30 Pell E. J., Schlagnhaufer C. D., Arteca R. N.. Ozone induced oxidative stress: mechanisms of action and reaction.  Physiologia Plantarum. (1997);  100 264-273
• 31 Schade G. W., Goldstein A. H.. Seasonal measurements of acetone and methanol: abundances and implications for atmospheric budgets.  Global Biogeochemical Cycles. (2006);  20 No.GB1011
• 32 Velikova V., Tsonev T., Pinelli P., Alessio G. A., Loreto F.. Localized O₃-fumigation for field studies of the impact of different ozone doses on photosynthesis, respiration, electron transport rate and isoprene emission in Mediterranean species.  Tree Physiology. (2005);  25 1523-1532
• 33 Wildt J., Kley D., Rockel A., Rockel P., Segschneider H. J.. Emission of NO from several higher plant species.  Journal of Geophysical Research. (1997);  102 5919-5927

Editor: H. Rennenberg