Skip to main content

Advertisement

SpringerLink
Log in

Early Responses to Acute Ozone Exposure in Two Fagus Sylvatica Clones Differing in Xeromorphic Adaptations: Photosynthetic and Stomatal Processes, Membrane and Epicuticular Characteristics

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Two Fagus sylvatica L. clones were used to investigate the early responses to acute O3 exposure (150 nL L−1, i.e., 1.35× ambient hourly peak in rural Italy) and whether xeromorphic adaptations affect gas exchange, membrane, and epicuticular responses. One clone originated in a wet and temperate climate in Central Italy (Tuscany); the other clone originated in a warmer and drier climate in the southern-most part of the F. sylvatica distribution (Sicily). Because of higher base gas exchange rates, the most negative effects of O3 exposure (gas exchange impairment, uncoupling between net photosynthesis and stomatal conductance, increased membrane lipid peroxidation) were found in the southern clone. Xeromorphic adaptations (higher epicuticular waxes and stomatal density, lower leaf wettability and size) were found in this clone. Our results suggest that xeromorphism may increase O3 sensitivity in species not adapted to face water stress, like the mesophilic F. sylvatica, when experiments are carried out with full irrigation. We present evidence describing the relationship between gas exchange and number and status of stomata. Stomatal density and the structural damage to stomata resulting from O3 exposure did not affect gas exchange: In fact, non-stomatal limitations to photosynthesis prevailed over stomatal limitations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baker, E. A. (1982). Chemistry and morphology of plant epicuticular waxes. In: D. F. Cutler, K. L. Alvin, & C. E. Price (Eds.), The plant cuticle (pp. 139–165). New York: Academic.

    Google Scholar 

  • Barnes, J. D., & Brown, K. A. (1990). The influence of ozone and acid mist on the amount and wettability of the surface waxes in Norway spruce (Picea abies (L.) Karst.). New Phytologist, 114, 531–535.

    Article  CAS  Google Scholar 

  • Barnes, J. D., Davison, A. W., & Booth, T. A. (1988). Ozone accelerates structural degradation of epicuticular wax on Norway spruce needles. New Phytologist, 110, 309–318.

    Article  CAS  Google Scholar 

  • Barnes, J. D., Eamus, D., Davison, A. W., Ro-Poulsen, H., & Mortensen, L. (1990). Persistent effects of ozone on needle water loss and wettability in Norway spruce. Environmental Pollution, 63, 345–363.

    Article  CAS  Google Scholar 

  • Beckerson, D. W., & Hofstra, G. (1980). Effects of sulphur dioxide and ozone, singly or in combination, on membrane permeability. Canadian Journal of Botany, 58, 451–457.

    CAS  Google Scholar 

  • Bennett, J. P., Rassat P., Berrang P., & Karnosky, D. F. (1992) Relationships between leaf anatomy and ozone sensitivity of Fraxinus pennsylvanica Marsh. and Prunus serotina Ehrh. Environmental and Experimental Botany, 32, 33–41.

    Article  CAS  Google Scholar 

  • Bortier, K., Ceulemans, R., & De Temmerman, L. (2000). Effects of ozone exposure on growth and photosynthesis of beech seedlings (Fagus sylvatica). New Phytologist, 146, 271–280.

    Article  CAS  Google Scholar 

  • Bortier, K., Vandermeiren, K., De Temmerman, L., & Ceulemans, R. (2001). Growth, photosynthesis and ozone uptake of young beech (Fagus sylvatica L.) in response to different ozone exposures. Trees, 15, 75–82.

    Article  CAS  Google Scholar 

  • Braun, S., & Flückiger, W. (1995). Effects of ambient ozone on seedlings of Fagus sylvatica L. and Picea abies (L.). New Phytologist, 129, 33–44.

    Article  CAS  Google Scholar 

  • Brewer, C. A., & Smith, W. K. (1994). Influence of simulated dewfall on photosynthesis and yield in soybean isolines (Glycine max [L.] Merr. cv Williams) with different trichome densities. International Journal of Plant Science, 155, 460–466.

    Article  Google Scholar 

  • Cape, J. N. (1983). Contact angles of water droplets on needle of scots pine (Pinus sylvestris) growing in polluted atmospheres. New Phytologist, 93, 293–299.

    Article  Google Scholar 

  • Cape, J. N., Paterson, I. S., & Wolfenden, J. (1989). Regional variation in surface properties of Norway spruce and Scots pine needles in relation to forest decline. Environmental Pollution, 58, 325–342.

    Article  CAS  Google Scholar 

  • Cape, J. N., & Percy, K. E. (1993). Environmental influences on the development of spruce needle cuticles. New Phytologist, 125, 787–799.

    Article  Google Scholar 

  • Cape, J. N., Sheppard, L. J., & Binnie, J. (1995). Leaf surface properties of Norway spruce needles exposed to sulphur dioxide and ozone in an open-air fumigation system at Liphook. Plant Cell & Environment, 18, 285–289.

    Article  CAS  Google Scholar 

  • Crossley, A., & Fowler, D. (1986). The weathering of Scots pine epicuticular wax in polluted and clean air. New Phytologist, 103, 207–218.

    Article  Google Scholar 

  • Dexter, S. T., Tottingham, W. E., & Graber, L. F. (1932). Investigations of the hardiness of plants by measurement of electrical conductivity. Plant Physiology, 7, 63–78.

    CAS  Google Scholar 

  • Dixon, M., Le Thiec, D., & Garrec, J. P. (1997). An investigation into the effects of ozone and drought, applied singly and in combination, on the quantity and quality of the epicuticular wax of Norway spruce. Plant Physiology and Biochemistry, Paris, 35, 447–454.

    CAS  Google Scholar 

  • Dixon, M., Le Thiec, D., & Garrec, J. P. (1998). Reactions of Norway spruce and beech trees to 2 years of ozone exposure and episodic drought. Environmental and Experimental Botany, 40, 77–91.

    Article  Google Scholar 

  • Draper, N., & Smith, H. (1981). Applied regression analysis (p. 209). New York: Wiley.

    Google Scholar 

  • Farage, P. K., Long, S. P., Lechner, E. G., & Baker, N. R. (1991). The sequence of changes within the photosynthetic apparatus of wheat following short term exposure to ozone. Plant Physiology, 95, 529–535.

    CAS  Google Scholar 

  • Farquhar, G. D., & Sharkey, T. D. (1982). Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33, 317–345.

    Article  CAS  Google Scholar 

  • Farquhar, G. D., von Caemmerer, S., & Berry, J. A. (1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149, 78–90.

    Article  CAS  Google Scholar 

  • Ferdinand, J. A., Fredericksen, T. S., Kouterick, K. B., & Skelly, J. M. (2000). Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings. Environmental Pollution, 108, 297–302.

    Article  CAS  Google Scholar 

  • García-Plazaola, J. I., & Becerril, J. M. (2000). Effects of drought on photoprotective mechanisms in European beech (Fagus sylvatica L.) seedlings from different provenances. Trees, 14, 485–490.

    Article  Google Scholar 

  • Grams, T. E. E., Anegg, S., Häberle, K.-H., Langebartels, C., & Matyssek, R. (1999). Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica). New Phytologist, 144, 95–107.

    Article  CAS  Google Scholar 

  • Grantz, D. A., Zhang, X. J., Massman, W. J., Delany, A., & Pederson, J. R. (1997). Ozone deposition to a cotton (Gossypium hirsutum L.) field: Stomatal and surface wetness effects during the California ozone deposition experiment. Agricultural and Forest Meteorology, 85, 19–31.

    Article  Google Scholar 

  • Grossoni, P., Bussotti, F., Tani, C., Gravano, E., Santarelli, S., & Bottacci, A. (1998). Morpho-anatomical alterations in leaves of Fagus sylvatica L. and Quercus ilex L. in different environmental stress conditions. Chemosphere, 36, 919–924.

    Article  CAS  Google Scholar 

  • Gunthardt-Goerg, M. S., & Keller, T. (1987). Some effects of long-term ozone fumigation on Norway spruce. II. Epicuticular wax and stomata. Trees, 1, 145–150.

    Article  Google Scholar 

  • Heath, R. L. (1996). The modification of photosynthetic capacity induced by ozone exposure. In N. R. Baker (Ed.), Photosynthesis and the environment (pp. 409–433). Dordrecht, The Netherlands: Kluwer.

    Google Scholar 

  • Hodges, D. M., Delong, J. M., Forney, C. F., & Prange, R. K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta, 207, 604–611.

    Article  CAS  Google Scholar 

  • ICP (2004). Manual on Methodologies and Criteria for Modelling and Mapping Critical Loads & Levels and Air Pollution Effects, Risks and Trends.

  • Jetter, R., Riederer, M., & Lendzian, K. J. (1996). The effects of dry O3, SO2 and NO2 on reconstituted epicuticular wax tubules. New Phytologist, 133, 207–216.

    Article  CAS  Google Scholar 

  • Kellomäki, S., & Wang, K.-Y. (1997). Effects of elevated O3 and CO2 concentrations on photosynthesis and stomatal conductance in Scots pine. Plant Cell & Environment, 20, 995–1006.

    Article  Google Scholar 

  • Kerstiens, G., & Lendzian, K. J. (1989). Interactions between ozone and plant cuticles. I. Ozone deposition and permeability. New Phytologist, 112, 13–19.

    Article  CAS  Google Scholar 

  • Krause, G. H. M., & Höckel, F.-E. (1995). Long-term effects of ozone on Fagus sylvatica L.—An open-top chamber exposure study. Water Air and Soil Pollution, 85, 1337–1342.

    Article  CAS  Google Scholar 

  • Krause, C. R., & Jensen, K. F. (1979). Surface changes on hybrid poplar leaves exposed to ozone and sulfur dioxide. Scanning Electron Microscopy, 3, 77–86.

    Google Scholar 

  • Langebartels, C., Ernst, D., Heller, W., Lütz, C., Payer, H.-D., & Sandermann, H. Jr. (1997). Ozone responses of trees: results from controlled chamber exposures at the GSF phytotron. In H. Sandermann, A. R. Wellburn, & R. L. Heath (Eds.), Forest decline and ozone: A comparison of controlled chamber and field experiments (Vol. 127, pp. 163–200). Berlin Heidelberg New York: Ecological Studies, Springer.

    Google Scholar 

  • Leonardi, S., Langebartels, C., & Sandermann, H. (1990). Fall exposure of beech trees (Fagus sylvatica L.) to ozone and simulated acidic mist: Immediate and post-treatment effects on whole plant physiology. In H. D. Payer, T. Pfirrmann, & P. Mathy (Eds.), Environmental research with plants in closed chamber, Air Pollution Research Reports (Vol. 26, pp. 369–380). Brussels: CEC.

    Google Scholar 

  • Lippert, M., Steiner, K., Payer, H. D., Simons, S., Langebartels, C., & Sandermann, H. (1996). Assessing the impact of ozone on photosynthesis of European beech (Fagus sylvatica L.) in environmental chambers. Trees, 10, 268–275.

    Google Scholar 

  • Long, S. P., & Bernacchi, C. J. (2003). Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany, 54, 2393–2401.

    Article  CAS  Google Scholar 

  • Lorenzini, G., Medeghini Bonatti, P., Nali, C., & Baroni Fornasiero, R. (1994). The protective effect of rust infection against ozone, sulphur dioxide and paraquat toxicity symptoms in broad bean. Physiological and Molecular Plant Pathology, 45, 263–279.

    Article  CAS  Google Scholar 

  • Lutz, C., Heinzmann, U., & Gulz, P. G. (1990). Surface structures and epicuticular wax composition of spruce needles after long-term treatment with ozone and acid mist. Environmental Pollution, 64, 3–4.

    Article  Google Scholar 

  • Matyssek, R., Gunthardt-Goerg, M. S., Keller, T., & Scheidegger, C. (1991). Impairment of gas exchange and structure in birch leaves (Betula pendula) caused by low ozone concentrations. Trees, 5, 5–13.

    Article  Google Scholar 

  • Mikkelsen, T. N. (1995). Physiological responses of Fagus sylvatica L. exposed to two levels of ozone in open-top chambers. Trees, 9, 355–361.

    Article  Google Scholar 

  • Mikkelsen, T. N., & Heide-Jorgensen, H. S. (1996). Acceleration of leaf senescence in Fagus sylvatica L. by low levels of tropospheric ozone demonstrated by leaf colour, chlorophyll fluorescence and chloroplast ultrastructure. Trees, 10, 145–156.

    Google Scholar 

  • Minotta, G., & Pinzauti, S. (1994). Influenza della radiazione luminosa sulle prime fasi di sviluppo di semenzali di faggio (Fagus sylvatica L.). Monti e Boschi, 45, 44–52.

    Google Scholar 

  • Mortensen, L., Bastrup-Birk, A., & Ro-Poulsen, H. (1995). Critical levels of O3 for wood production of European beech (Fagus sylvatica L.). Water Air and Soil Pollution, 85, 1349–1354.

    Article  CAS  Google Scholar 

  • Nali, C., Guidi, L., Filippi, F., Soldatini, G. F., & Lorenzini, G. (1998). Photosynthesis of two poplar clones contrasting in O3 sensitivity. Trees, 12, 196–200.

    Google Scholar 

  • Nali, C., Paoletti, E., Marabottini, R., Della Rocca, G., Lorenzini, G., Paolacci, A. R., et al. (2004). Ecophysiological and biochemical strategies of response to ozone in Mediterranean evergreen broadleaf species. Atmospheric Environment, 38, 2247–2257.

    Article  CAS  Google Scholar 

  • Nali, C., Pucciariello, C., & Lorenzini, G. (2002). Ozone distribution in central Italy and its effects on crop productivity. Agriculture, Ecosystem & Environment, 90, 277–289.

    Article  CAS  Google Scholar 

  • Neinhuis, C., Koch, K., & Barthlott, W. (2001). Movement and regeneration of epicuticular waxes through plant cuticles. Planta, 213, 427–434.

    Article  CAS  Google Scholar 

  • Pääkkönen, E., Gunthardt-Goerg, M. S., & Holopainen, T. (1998). Responses of leaf processes in a sensitive birch (Betula pendula Roth) clone to ozone combined with drought. Annals of Botany, 82, 49–59.

    Article  Google Scholar 

  • Pääkkönen, E., Holopainen, T., & Karenlampi, L. (1997). Variation in ozone sensitivity among clones of Betula pendula and Betula pubescens. Environmental Pollution, 95, 37–44.

    Article  Google Scholar 

  • Pääkkönen, E., Paasisalo, S., Holopainen, T., & Kärenlampi, L. (1993). Growth and stomatal responses of birch (Betula pendula Roth.) clones to ozone in open-air and chamber fumigations. New Phytologist, 125, 615–623.

    Article  Google Scholar 

  • Pääkkönen, E., Vahala, J., Pohjolai, M., Holopainen, T., & Karenlampi, L. (1998). Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress. Plant Cell & Environment, 21, 671–684.

    Article  Google Scholar 

  • Paludan-Müller, G., Saxe, H., & Leverenz, J. W. (1999). Responses to ozone in 12 provenances of European beech (Fagus sylvatica): Genotypic variation and chamber effects on photosynthesis and dry-matter partitioning. New Phytologist, 144, 261–273.

    Article  Google Scholar 

  • Paoletti, E., De Marco, A., & Racalbuto, R. (in press). Why should we calculate complex indices of ozone exposure? Results from Mediterranean background sites. Environmental Monitoring and Assessment.

  • Paoletti, E., & Grulke, N. E. (2005). Does living in elevated CO2 ameliorate tree response to ozone? A review on stomatal responses. Environmental Pollution, 137, 483–493.

    Article  CAS  Google Scholar 

  • Paoletti, E., Nali, C., & Lorenzini, G. (2002). Photosynthetic behavior of two Italian clones of European beech (Fagus sylvatica Mill.) exposed to ozone. Phyton, 42, 149–155.

    CAS  Google Scholar 

  • Paoletti, E., Raddi, P., & La Scala, S. (1998). Relationships between transpiration, stomatal damage and leaf wettability in declining beech trees. Chemosphere, 36, 907–912.

    Article  CAS  Google Scholar 

  • Pearson, M., & Mansfield, T. A. (1994). Effects of exposure to ozone and water stress on the following season’s growth of beech (Fagus sylvatica L.). New Phytologist, 126, 511–515.

    Article  CAS  Google Scholar 

  • Percy, K. E., Awmack, C. S., Lindroth, R. L., Kubiske, M. E., Kopper, B. J., Isebrands, J. G., et al. (2002). Altered performance of forest pests under atmospheres enriched by CO2 and O3. Nature, 420, 403–407.

    Article  CAS  Google Scholar 

  • Percy, K. E., Jensen, K. F., & McQuattie, C. J. (1992). Effects of ozone and acidic fog on red spruce needle epicuticular wax production, chemical composition, cuticular membrane ultrastructure and needle wettability. New Phytologist, 122, 71–80.

    Article  CAS  Google Scholar 

  • Percy, K. E., Krause, C. R., & Jensen, K. F. (1990). Effects of ozone and acidic fog on red spruce needle epicuticular wax ultrastructure. Canadian Journal of Forest Research, 20, 117–120.

    CAS  Google Scholar 

  • Reich, P. B. (1983). Effects of low concentrations of O3 on net photosynthesis, dark respiration, and chlorophyll contents in aging hybrid poplar leaves. Plant Physiology, 73, 291–296.

    Article  CAS  Google Scholar 

  • Reichenauer, T., Bolhar-Nordenkampf, H. R., Ehrlich, U., Soja, G., Postl, W. F., & Halbwachs, F. (1997). The influence of ambient and elevated ozone concentrations on photosynthesis in Populus nigra. Plant Cell & Environment, 20, 1061–1069.

    Article  CAS  Google Scholar 

  • Sakaki, T., & Kondo, N. (1985). Lipid changes in higher plant leaves with ozone fumigation (research report). National Institute for Environmental Studies, 82, 179–186.

    CAS  Google Scholar 

  • Sasek, T. W., & Richardson, C. J. (1989). Effects of chronic doses of ozone on loblolly pine: Photosynthetic characteristics in the third growing season. Forest Science, 35, 745–755.

    Google Scholar 

  • Schraudner, M., Langebartels, C., & Sandermann, H. (1997).Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiologia Plantarum, 100, 274–280.

    Article  CAS  Google Scholar 

  • Schreuder, M. D. J., van Hove, L. W. A., & Brewer, C. A. (2001). Ozone exposure affects leaf wettability and tree water balance. New Phytologist, 152, 443–454.

    Article  CAS  Google Scholar 

  • Steubing, L., Fangmeier, A., Both, R., & Frankenfeld, M. (1989). Effects of SO2, NO2, and O3 on population development and morphological and physiological parameters of native herb layer species in a beech forest. Environmental Pollution, 58, 281–302.

    Article  CAS  Google Scholar 

  • Strasser, R. J., & Stirbet, A. D. (2000). Energetic connectivity creates heterogeneity of PSII centres in plants probed by the fluorescence rise 0-J-I-P. Fitting of experimental data to three different PSII models. In H. Greppin, C. Penel, W. Broughton, & R. J. Strasser (Eds.), Integrated plant systems (pp. 81–94). Switzerland: University of Geneva.

    Google Scholar 

  • Taylor, G., & Dobson, M. C. (1989). Photosynthetic characteristics, stomatal responses and water relations of Fagus sylvatica: Impact of air quality at a site in southern Britain. New Phytologist, 113, 265–273.

    Article  Google Scholar 

  • Ticha, I. (1982). Photosynthetic characteristics during ontogenesis of leaves 7. Stomata density and sizes. Photosynthetica, 16, 375–471.

    Google Scholar 

  • Tognetti, R., Minotta, G., Pinzauti, S., Michelozzi, M., & Borghetti, M. (1998). Acclimation to changing light conditions of long-term shade-grown beech (Fagus sylvatica L.) seedlings of different geographic origins. Trees, 12, 326–333.

    Google Scholar 

  • Trimble, J. L., Skelly, J. M., Tolin, S. A., & Orcutt, D. M. (1982). Chemical and structural characterization of the needle epicuticular wax of two clones of Pinus strobus differing in sensitivity to ozone. Phytopathology, 72, 652–656.

    CAS  Google Scholar 

  • Turunen, M., & Huttunen, S. (1990). A review of the response of epicuticular wax of conifer needles to air pollution. Journal of Environmental Quality, 19, 35–45.

    Article  CAS  Google Scholar 

  • Vingarzan, R. (2004). A review of surface O3 background levels and trends. Atmospheric Environment, 38, 3431–3442.

    Article  CAS  Google Scholar 

  • Vollenweider, P., Ottiger, M., & Günthardt-Goerg, M. S. (2003). Validation of leaf ozone symptoms in natural vegetation using microscopical methods. Environmental Pollution, 124, 101–118.

    Article  CAS  Google Scholar 

  • Wilson, J. (1984). Microscopic features of wind damage to leaves of Acer pseudoplatanus L. Annals of Botany, 53, 73–82.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Istituto Protezione Piante-Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, I-50019, Sesto Fiorentino, Italy

    Elena Paoletti

  2. Dipartimento G. Scaramuzzi, Università di Pisa, Via del Borghetto 80, Pisa, Italy

    Cristina Nali & Giacomo Lorenzini

Authors
  1. Elena Paoletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina Nali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giacomo Lorenzini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elena Paoletti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paoletti, E., Nali, C. & Lorenzini, G. Early Responses to Acute Ozone Exposure in Two Fagus Sylvatica Clones Differing in Xeromorphic Adaptations: Photosynthetic and Stomatal Processes, Membrane and Epicuticular Characteristics. Environ Monit Assess 128, 93–108 (2007). https://doi.org/10.1007/s10661-006-9418-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-006-9418-z

Keywords

Search

Navigation