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      Non-Stomatal Limitation to Photosynthesis in Cinnamomum camphora Seedings Exposed to Elevated O 3

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          Abstract

          Ozone (O 3) is the most phytotoxic air pollutant for global forests, with decreased photosynthesis widely regarded as one of its most common effects. However, controversy exists concerning the mechanism that underlies the depressing effects of O 3 on CO 2 assimilation. In the present study, seedlings of Cinnamomum camphora, a subtropical evergreen tree species that has rarely been studied, were exposed to ambient air (AA), ambient air plus 60 [ppb] O 3 (AA+60), or ambient air plus 120 [ppb] O 3 (AA+120) in open-top chambers (OTCs) for 2 years. Photosynthetic CO 2 exchange and chlorophyll a fluorescence were investigated in the second growing season (2010). We aim to determine whether stomatal or non-stomatal limitation is responsible for the photosynthesis reduction and to explore the potential implications for forest ecosystem functions. Results indicate that elevated O 3 (E-O 3) reduced the net photosynthetic rates ( P N) by 6.0-32.2%, with significant differences between AA+60 and AA+120 and across the four measurement campaigns (MCs). The actual photochemical efficiency of photosystem II (PSII) in saturated light (F v /F m ) was also significantly decreased by E-O 3, as was the effective quantum yield of PSII photochemistry (Φ PSII). Moreover, E-O 3 significantly and negatively impacted the maximum rates of carboxylation ( V cmax) and electron transport ( J max). Although neither the stomatal conductance ( g s) nor the intercellular CO 2 concentration ( C i) was decreased by E-O 3, P N/ g s was significantly reduced. Therefore, the observed reduction in P N in the present study should not be attributed to the unavailability of CO 2 due to stomatal limitation, but rather to the O 3-induced damage to Ribulose-1,5-bisphosphate carboxylase/oxygenase and the photochemical apparatus. This suggests that the down-regulation of stomatal conductance could fail to occur, and the biochemical processes in protoplasts would become more susceptible to injuries under long-term O 3 exposure, which may have important consequences for forest carbon and water budget.

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          Most cited references15

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          Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error.

          The principles, equipment and procedures for measuring leaf and canopy gas exchange have been described previously as has chlorophyll fluorescence. Simultaneous measurement of the responses of leaf gas exchange and modulated chlorophyll fluorescence to light and CO2 concentration now provide a means to determine a wide range of key biochemical and biophysical limitations on photo synthesis in vivo. Here the mathematical frameworks and practical procedures for determining these parameters in vivo are consolidated. Leaf CO2 uptake (A) versus intercellular CO2 concentration (Ci) curves may now be routinely obtained from commercial gas exchange systems. The potential pitfalls, and means to avoid these, are examined. Calculation of in vivo maximum rates of ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) carboxylation (Vc,max), electron transport driving regeneration of RuBP (Jmax), and triose-phosphate utilization (VTPU) are explained; these three parameters are now widely assumed to represent the major limitations to light-saturated photosynthesis. Precision in determining these in intact leaves is improved by the simultaneous measurement of electron transport via modulated chlorophyll fluorescence. The A/Ci response also provides a simple practical method for quantifying the limitation that stomata impose on CO2 assimilation. Determining the rate of photorespiratory release of oxygen (Rl) has previously only been possible by isotopic methods, now, by combining gas exchange and fluorescence measurements, Rl may be determined simply and routinely in the field. The physical diffusion of CO2 from the intercellular air space to the site of Rubisco in C3 leaves has long been suspected of being a limitation on photosynthesis, but it has commonly been ignored because of the lack of a practical method for its determination. Again combining gas exchange and fluorescence provides a means to determine mesophyll conductance. This method is described and provides insights into the magnitude and basis of this limitation.
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            Impact of ozone on Mediterranean forests: a review.

            E Paoletti (2006)
            Ozone impact on Mediterranean forests remains largely under-investigated, despite strong photochemical activity and harmful effects on crops. As representative of O3 impacts on Mediterranean vegetation, this paper reviews the current knowledge about O3 and forests in Italy. The intermediate position between Africa and European mid-latitudes creates a complex patchwork of climate and vegetation. Available data from air quality monitoring stations and passive samplers suggest O3 levels regularly exceed the critical level (CL) for forests. In contrast, relationships between O3 exposure and effects (crown transparency, radial growth and foliar visible symptoms) often fail. Despite limitations in the study design or underestimation of the CL can also affect this discrepancy, the effects of site factors and plant ecology suggest Mediterranean forest vegetation is adapted to face oxidative stress, including O3. Implications for risk assessment (flux-based CL, level III, non-stomatal deposition) are discussed.
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              Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on US forests.

              Tropospheric ozone (O(3)) was first determined to be phytotoxic to grapes in southern California in the 1950s. Investigations followed that showed O(3) to be the cause of foliar symptoms on tobacco and eastern white pine. In the 1960s, "X" disease of ponderosa pines within the San Bernardino Mountains was likewise determined to be due to O(3). Nearly 50 years of research have followed. Foliar O(3) symptoms have been verified under controlled chamber conditions. Studies have demonstrated negative growth effects on forest tree seedlings due to season-long O(3) exposures, but due to complex interactions within forest stands, evidence of similar losses within mature tree canopies remains elusive. Investigations on tree growth, O(3) flux, and stand productivity are being conducted along natural O(3) gradients and in open-air exposure systems to better understand O(3) effects on forest ecosystems. Given projected trends in demographics, economic output and climate, O(3) impacts on US forests will continue and are likely to increase.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                3 June 2014
                : 9
                : 6
                : e98572
                Affiliations
                [1 ]Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China
                [2 ]State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China
                [3 ]Key Laboratory of Black Soil Ecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, Heilongjiang, China
                Tennessee State University, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JFN ZZF. Performed the experiments: JFN WWZ. Analyzed the data: JFN. Contributed reagents/materials/analysis tools: JFN. Wrote the paper: JFN. Helpful suggestions in data analyses and manuscript preparation: XKW PZ.

                Article
                PONE-D-14-07067
                10.1371/journal.pone.0098572
                4043779
                24892748
                a5ddac25-854a-421a-a9cc-b0f94b109713
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 February 2014
                : 4 May 2014
                Page count
                Pages: 7
                Funding
                Funding for this project was provided by the National Natural Science Foundation of China (No. 31170424, No. 71003092, No. 41030638 and No. 41275169), Tiantong National Station of Forest Ecosystems (No. XT200707) and South Botanical Garden, Chinese Academy of Sciences (No. 201229). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Global Change Ecology
                Plant Ecology
                Plant Science
                Plant Physiology
                Earth Sciences
                Atmospheric Science
                Ecology and Environmental Sciences
                Ecology

                Uncategorized
                Uncategorized

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