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Carbon Isotope Composition, Macronutrient Concentrations, and Carboxylating Enzymes in Relation to the Growth of Pinus halepensis Mill. When Subject to Ozone Stress

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Abstract

We present here the effects of ambient ozone (O3)-induced decline in carbon availability, accelerated foliar senescence, and a decrease in aboveground biomass accumulation in the Aleppo pine (Pinus halepensis Mill.). Aleppo pine seedlings were continuously exposed in open-top chambers for 39 months to three different types of O3 treatments, which are as follows: charcoal-filtered air, nonfiltered air (NFA), and nonfiltered air supplemented with 40 ppb O3 (NFA+). Stable carbon isotope discrimination (Δ) and derived time-integrated c i/c a ratios were reduced after an accumulated ozone exposure over a threshold of 40 ppb (AOT40) value from April to September of around 20,000 ppb·h. An AOT40 of above 67,000 ppb·h induced reductions in ribulose-1,5-biphosphate carboxylase/oxygenase activity, aboveground C and needle N and K concentrations, the C/N ratio, Ca concentrations in twigs under 3 mm, and the aerial biomass, as well as increases in needle P concentrations and phosphoenolpyruvate carboxylase (PEPC) activity and the N and K concentrations in twigs under 3 mm. Macronutrients losses, the limitations placed on carbon uptake, and increases in catabolic processes may be the causes of carbon gain diminution in leaves which was reflected as a reduction in aboveground biomass at tree level. Stimulation of PEPC activity, the consequent decreased Δ, and compensation processes in nutrient distribution may increase O3 tolerance and might be interpreted as part of Aleppo pine acclimation response to O3.

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Abbreviations

Rubisco:

ribulose-1,5-biphosphate carboxylase/oxygenase

PEPC:

phosphoenolpyruvate carboxylase

Δ:

stable carbon isotope discrimination

ci/ca:

ratio of internal CO2 concentration to ambient CO2 concentration

References

  • Alonso, R., Elvira, S., Inclán, R., Bermejo, V., Castillo, F. J., & Gimeno, B. S. (2003). Responses of Aleppo pine to ozone. In D. F. Karnosky, K. E. Percy, A. H. Chappelka, C. Simpson, & J. Pikkarainen (Eds.), Air pollution, global change and forests in the new millenium (pp. 359–374). Oxford: Elsevier.

    Google Scholar 

  • Andersen, C. P. (2003). Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytolosist, 157, 213–228.

    Article  CAS  Google Scholar 

  • Anttonen, S., Kittilä, M., & Kärenlampi, L. (1998). Impacts of ozone on Aleppo pine needles: Visible symptoms, starch concentrations and stomatal responses. Chemosphere, 36, 663–668.

    Article  CAS  Google Scholar 

  • Baker, T. R., Allen, H. L., Schoeneberger, M. M., & Kress, L. W. (1994). Nutritional response of loblolly pine exposed to ozone and simulated acid rain. Canadian Journal of Forest Research, 24, 453–461.

    Article  CAS  Google Scholar 

  • Barnes, J., Gimeno, B., Davison, A., Dizengremel, P., Gerant, D., Bussotti, F., et al. (2000). Air pollution impacts on pine forests in the Mediterranean Basin. In G. Ne‘emana & L. Trabaud (Eds.), Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean Basin (pp. 391–404). Leiden: Backhuys Publishers.

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  Google Scholar 

  • Bussoti, F., & Gerosa, G. (2002). Are the Mediterranean forests in southern Europe threatened from ozone? Journal of Mediterranean Ecology, 3, 23–34.

    Google Scholar 

  • Chappelka, A. H., & Chevone, B. I. (1992). Trees responses to ozone. In A. S. Lefhon (Ed.), Surface level ozone exposure and their effects on vegetation (pp. 271–309). Chelsea: Lewis Publishers.

    Google Scholar 

  • Chapin, F. S. I. I. I., & Kedrowski, R. A. (1983). Seasonal changes in nitrogen and phosphorus fractions and autumnal retranslocation in evergreen and deciduous taiga trees. Ecology, 64, 76–391.

    Google Scholar 

  • Damesin, C., & Lelarge, C. (2003). Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant, Cell & Environment, 26, 207–219.

    Article  Google Scholar 

  • De Temmerman, L., Vandermeiren, K., & D’Haese, D. (2002). Ozone effects on trees, where uptake and detoxification meet. Dendrobiology, 47, 9–19.

    Google Scholar 

  • Dizengremel, P. (2001). Effects of ozone on the carbon metabolism of forest trees. Plant Physiology and Biochemistry, 39(9), 729–742.

    Article  CAS  Google Scholar 

  • Dizengremel, P., Le Thiec, D., Hasenfratz-Sauder, M. P., Vaultier, M. N., Bagard, M., & Jolivet, Y. (2009). Metabolic-dependent changes in plant cell redox power after ozone exposure. Plant Biology, 11(1), 35–42.

    Article  CAS  Google Scholar 

  • Elvira, S., Alonso, R., Inclán, R., Bermejo, V., Castillo, F. J., & Gimeno, B. S. (1995). Ozone effects on Aleppo pine seedling (Pinus halepensis Mill.) grown in open-top chambers. Water, Air, and Soil Pollution, 85, 1387–1392.

    Article  CAS  Google Scholar 

  • Farquhar, G. D., O’Leary, M. H., & Berry, A. (1982). On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology, 9, 121–137.

    Article  CAS  Google Scholar 

  • Farquhar, G. D., Hubick, K. T., Cordon, A. G., & Richards, R. A. (1989). Carbon isotope fractionation and plant water-use efficiency. In P. W. Rundel, J. R. Ehleringer, & K. A. Nagy (Eds.), Stabe isotopes in ecological research (pp. 21–40). Berlin: Springer.

    Google Scholar 

  • FFCC. (1997). Forest foliar condition in Europe results of large-scale foliar chemistry surveys (survey 1995 and from previous years). Brussels, Belgium: Forest Foliar Co-ordinating Center. United Nations Economic Commission for Europe. European Commission.

    Google Scholar 

  • Fontaine, V., Pelloux, J., Podor, M., Afif, D., Gerant, D., Grieu, P., et al. (1999). Carbon fixation in Pinus halepensis submitted to ozone. Opposite response of ribulose-1, 5-biphosphate carboxylase/oxygenase and phosphoenolpyruvate carboxylase. Physiologia Plantarum, 105, 87–192.

    Article  Google Scholar 

  • Fontaine, V., Cabané, M., & Dizengremel, P. (2003). Regulation of phosphoenolpyruvate carboxylase in Pinus halepensis needles submitted to ozone and water stress. Physiologia Plantarum, 117, 45–452.

    Article  Google Scholar 

  • Gerant, D., Podor, M., Grieu, O., Afif, D., Cornu, S., Morabito, D., et al. (1996). Carbon metabolism enzyme activities and carbon partitioning in Pinus halepensis Mill. exposed to mild drought and ozone. Journal of Plant Physiology, 148, 142–147.

    CAS  Google Scholar 

  • Gimeno, B. S., Velissariou, D., Barnes, J. D., Inclán, R., Peña, J. M., & Davison, A. W. (1992). Daños visibles por ozono en acículas de Pinus halepensis Mill. en Grecia y España. Ecología, 6, 131–134.

    Google Scholar 

  • Gimeno, B. S., Bermejo, V., Reinert, R. A., Zheng, Y., & Barnes, J. D. (1999). Adverse effects of ambient ozone on watermelon yield and physiology at a rural site in Eastern Spain. The New Phytologist, 144, 245–260.

    Article  CAS  Google Scholar 

  • Grams, T. E. E., Kozovits, A. R., Häberle, K. H., Matyssek, R., & Dawson, T. E. (2007). Combining delta C-13 and delta O-18 analyses to unravel competition, CO2 and O3 effects on the physiological performance of different-aged trees. Plant, Cell & Environment, 30, 1023–1034.

    Article  CAS  Google Scholar 

  • Heath, R. L. (2008). Modification of the biochemical pathways of plants induced by ozone: what are the varied routes to change? Environmental Pollution, 155, 453–463.

    Article  CAS  Google Scholar 

  • Inclán, R., Alonso, R., Pujadas, M., Terés, J., & Gimeno, B. S. (1998). Ozone and drought stress: interactive effects on gas exchange in Aleppo pine (Pinus halepensis Mill.). Chemosphere, 675, 685–690.

    Article  Google Scholar 

  • Inclán, R., Gimeno, B. S., Dizengremel, P., & Sanchez, M. (2005). Compensation processes of Aleppo pine (Pinus halepensis Mill) to ozone exposure and drought stress. Environmental Pollution, 137, 517–524.

    Article  Google Scholar 

  • Kärenlampi, L. (1987). Visible symptoms and mesophyll cell structural responses to air pollution in two lowland pines (Pinus radiata and P. halepensis) in Southern California. Savonia, 9, 1–12.

    Google Scholar 

  • Karlsson, P. E., Uddling, J., Braun, S., Broadmeadow, M., Elvira, S., Gimeno, B. S., et al. (2004). New critical levels for ozone effects on young trees based on AOT40 and simulated cumulative leaf uptake of ozone. Atmospheric Environment, 38, 2283–2294.

    Article  CAS  Google Scholar 

  • Karlsson, P. E., Braun, S., Broadmeadow, M., Elvira, S., Emberson, L., Gimeno, B. S., et al. (2007). Risk assessments for forest trees: the performance of the ozone flux versus the AOT concepts. Environmental Pollution, 146, 608–616.

    Article  CAS  Google Scholar 

  • Karnosky, D. F., Skelly, J. M., Percy, K. E., & Chappelka, A. H. (2007). Perspectives regarding 50 years of research of effects of tropospheric ozone air pollution on US forests. Environmental Pollution, 147, 489–506.

    Article  CAS  Google Scholar 

  • Kytöviita, M. M., Le Thiec, D., & Dizengremel, P. (2001). Elevated CO2 and ozone reduce nitrogen acquisition by Pinus halepensis from its mycorrhizal symbiont. Physiologia Plantarum, 111, 305–312.

    Article  Google Scholar 

  • Kolb, T. E., & Matyssek, R. (2001). Limitations and perspectives about scaling ozone impacts in trees. Environmental Pollution, 115, 373–393.

    Article  CAS  Google Scholar 

  • Le Thiec, D., & Manninen, S. (2003). Ozone and water deficit reduced growth of Aleppo pine seedlings. Plant Physiology and Biochemistry, 41(1), 55–63.

    Article  Google Scholar 

  • Lindroth, R. L., Kopper, B. J., Parsons, W. F. J., Bockheim, J. G., Karnosky, D. F., Hendrey, G. R., et al. (2001). Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environmental Pollution, 115, 395–404.

    Article  CAS  Google Scholar 

  • Lucas, P. W., & Diggle, P. J. (1997). The use of longitudinal data analysis to study the multi-seasonal growth responses of Norway and Sitka spruce to summer exposure to ozone: implications for the determination of critical levels. The New Phytologist, 137, 315–323.

    Article  CAS  Google Scholar 

  • Manning, W. J. (2005). Establishing a cause and effect relationship for ambient ozone exposure and tree growth in the forest: progress and an experimental approach. Environmental Pollution, 137, 443–454.

    Article  CAS  Google Scholar 

  • Marschner, H. (2002). Mineral nutrition of higher plants. San Diego: Academic.

    Google Scholar 

  • Matyssek, R., Günthardt-Goerg, M. S., Landolt, W., & Keller, T. (1992). Seasonal growth, δ13C in leaves and stem, and phloem structure of birch (Betula pendula) under low ozone concentrations. Trees, 6, 69–76.

    Article  Google Scholar 

  • Matyssek, R., & Innes, J. L. (1999). Ozone—a risk factor for trees and forests in Europe? Water, Air, and Soil Pollution, 116, 199–226.

    Article  CAS  Google Scholar 

  • Matyssek, R., Bytnerowicz, A., Karlsson, P. E., Paoletti, E., Sanz, M., Schaub, M., et al. (2007). Promoting the O3-flux concept for European forest trees. Environmental Pollution, 146, 587–607.

    Article  CAS  Google Scholar 

  • Matyssek, R., Sandermann, H., Wieser, G., Booker, F., Cieslik, S., Musselman, R., et al. (2008). The challenge of making ozone risk assessment for forest trees more mechanistic. Environmental Pollution, 156, 567–582.

    Article  CAS  Google Scholar 

  • Matyssek, R., Karnosky, D., Kubiske, M., Oksanen, E., & Wieser, G. (2010). Advances in understanding ozone impact on forest trees:messages from novel phytotron and free-air fumigation studies. Environmental Pollution 158, 1990–2006.

  • Noodén, L. D., & Leopold, A. C. (1988). Senescence and aging in plants. San Diego: Academic.

    Google Scholar 

  • Nussbaum, S., Geissmann, M., Saurer, M., Siegwolf, R., & Fuhrer, J. (2000). Ozone and low concentrations of nitric oxide have similar effects on carbon isotope discrimination and gas exchange in leaves of wheat (Triticum aestivum L.). Journal of Plant Physiology, 156, 741–745.

    CAS  Google Scholar 

  • Paoletti, E. (2006). Impact of ozone on Mediterranean forests: a review. Environmental Pollution, 144, 463–474.

    Article  CAS  Google Scholar 

  • Paoletti, E., & Manning, W. J. (2007). Toward a biologically significant and usable standard for ozone that will also protect plants. Environmental Pollution, 150, 85–95.

    Article  CAS  Google Scholar 

  • Pell, E. J., Schlagnhaufer, C. D., & Arteca, R. N. (1997). Ozone-induced oxidative stress: Mechanisms of action and reaction. Physiologia Plantarum, 100, 264–273.

    Article  CAS  Google Scholar 

  • Pelloux, J., Jolivet, Y., Fontaine, V., Banvoy, J., & Dizengremel, P. (2001). Changes in Rubisco and Rubisco activase gene expression and polypeptide content in Pinus halepensis M. subjected to ozone and drought. Plant, Cell & Environment, 24, 123–131.

    Article  CAS  Google Scholar 

  • Peñuelas, J., Llusià, J., & Gimeno, B. S. (1999). Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region. Environmental Pollution, 105, 17–23.

    Article  Google Scholar 

  • Ribas, A., & Peñuelas, J. (2004). Temporal patterns of surface ozone levels in different habitats of the North Western Mediterranean basin. Atmospheric Environment, 38, 985–992.

    Article  CAS  Google Scholar 

  • Ribas, A., Peñuelas, J., Elvira, S., & Gimeno, B. S. (2005). Ozone exposure induces the activation of leaf senescence-related processes and morphological and growth changes in seedlings of Mediterranean tree species. Environmental Pollution, 134, 291–300.

    Article  CAS  Google Scholar 

  • Samuelson, L. J., & Kelly, J. M. (1996). Carbon partitioning and allocation in northern red oak seedlings and mature trees in response to ozone. Tree Physiology, 16, 853–858.

    CAS  Google Scholar 

  • Sanz, M. J., Calatayud, V., & Calvo, E. (2000). Spatial pattern of ozone injury in Aleppo pine related to air pollution dynamics in a coastal-mountain region of eastern Spain. Environmental Pollution, 108, 239–247.

    Article  CAS  Google Scholar 

  • Saurer, M., Fuhrer, J., & Siegenthaler, U. (1991). Influence of ozone on the stable C isotope composition, δ13C, of leaves and grain of spring wheat (Triticum aestivum L.). Plant Physiology, 97, 313–316.

    Article  CAS  Google Scholar 

  • Saurer, M., Maurer, S., Matyssek, R., Landolt, W., Günthardt-Goerg, M. S., & Siegenthaler, U. (1995). The influence of ozone and nutrition on δ13C in Betula pendula. Oecologia, 103, 397–406.

    Article  Google Scholar 

  • Tietz, S., & Wild, A. (1991). Investigation on the phosphoenolpyruvate carboxylase activity of spruce needles relative to the occurrence of novel forest decline. Journal of Plant Physiology, 137, 327–331.

    CAS  Google Scholar 

  • UNECE (2009). Manual on methodologies and criteria for modelling and mapping critical loads and levels and air pollution effects, risks and trends. Convention on Long-range Transboundary Air Pollution. http://www.icpmapping.org.

  • Utriainen, J., & Holopainen, T. (2001). Influence of nitrogen and phosphorus availability and ozone stress on Norway spruce seedlings. Tree Physiology, 21, 447–456.

    CAS  Google Scholar 

  • Ward, D. A., & Keys, A. J. (1989). A comparison between the coupled spectrophotometric and the uncoupled radiometric assay for RUBP carboxylase. Photosynthesis Research, 22, 167–171.

    Article  CAS  Google Scholar 

  • Wieser, G., & Matyssek, R. (2007). Linking ozone uptake and defense towards a mechanistic risk assessment for forest trees. The New Phytologist, 174, 7–9.

    Article  CAS  Google Scholar 

  • Zheng, Y., Shimizu, H., & Barnes, J. D. (2002). Limitations to CO2 assimilation in ozone-exposed leaves of Plantago major. The New Phytologist, 155, 67–78.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the EU EV5V-CT93-0263 project. We are also grateful for the partial funding from Spanish Government projects CGL2006-02922/CLI, CGL2009-07031/CLI, CGL2006-04025/BOS and Consolider Montes (CSD2008-00040) and Catalan Government project SGR 2009-458. We gratefully acknowledge Victoria Bermejo, Rocio Alonso, Susana Elvira, Sonia Sanchez, José Manuel Gil, and Modesto Mendoza for their help in the fieldwork.

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Authors and Affiliations

  1. Ecotoxicology of Air pollution, Ciemat. Ed 70. Avda. Complutense 22, Madrid, 28040, Spain

    Rosa Inclán & Benjamín S. Gimeno

  2. Plant Ecophysiology Unit, Csic-Ceab-Creaf. Edifici c, Universitat Autonoma de Barcelona, 08193, Bellaterra, Spain

    Josep Peñuelas

  3. University Nancy, BP 239, 54506, Vandoeuvre, France

    Dominique Gerant

  4. Chemistry Division, Ciemat. Ed 3. Avda. Complutense 22, Madrid, 28040, Spain

    Alberto Quejido

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  1. Rosa Inclán
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  2. Benjamín S. Gimeno
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Correspondence to Benjamín S. Gimeno.

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Inclán, R., Gimeno, B.S., Peñuelas, J. et al. Carbon Isotope Composition, Macronutrient Concentrations, and Carboxylating Enzymes in Relation to the Growth of Pinus halepensis Mill. When Subject to Ozone Stress. Water Air Soil Pollut 214, 587–598 (2011). https://doi.org/10.1007/s11270-010-0448-3

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