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      Fagaceae tree species allocate higher fraction of nitrogen to photosynthetic apparatus than Leguminosae in Jianfengling tropical montane rain forest, China

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          Abstract

          Variation in photosynthetic-nitrogen use efficiency (PNUE) is generally affected by several factors such as leaf nitrogen allocation and leaf diffusional conductances to CO 2, although it is still unclear which factors significantly affect PNUE in tropical montane rain forest trees. In this study, comparison of PNUE, photosynthetic capacity, leaf nitrogen allocation, and diffusional conductances to CO 2 between five Fagaceae tree species and five Leguminosae tree species were analyzed in Jianfengling tropical montane rain forest, Hainan Island, China. The result showed that PNUE of Fagaceae was significantly higher than that of Leguminosae (+35.5%), attributed to lower leaf nitrogen content per area ( N area, –29.4%). The difference in nitrogen allocation was the main biochemical factor that influenced interspecific variation in PNUE of these tree species. Fagaceae species allocated a higher fraction of leaf nitrogen to the photosynthetic apparatus ( P P, +43.8%), especially to Rubisco ( P R, +50.0%) and bioenergetics ( P B +33.3%) in comparison with Leguminosae species. Leaf mass per area (LMA) of Leguminosae species was lower than that of Fagaceae species (-15.4%). While there was no significant difference shown for mesophyll conductance ( g m), Fagaceae tree species may have greater chloroplast to total leaf surface area ratios and that offset the action of thicker cell walls on g m. Furthermore, weak negative relationship between nitrogen allocation in cell walls and in Rubisco was found for Castanopsis hystrix, Cyclobalanopsis phanera and Cy. patelliformis, which might imply that nitrogen in the leaves was insufficient for both Rubisco and cell walls. In summary, our study concluded that higher PNUE might contribute to the dominance of most Fagaceae tree species in Jianfengling tropical montane rain forest.

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          A biochemical model of photosynthetic CO2 assimilation in leaves of C 3 species.

          Various aspects of the biochemistry of photosynthetic carbon assimilation in C3 plants are integrated into a form compatible with studies of gas exchange in leaves. These aspects include the kinetic properties of ribulose bisphosphate carboxylase-oxygenase; the requirements of the photosynthetic carbon reduction and photorespiratory carbon oxidation cycles for reduced pyridine nucleotides; the dependence of electron transport on photon flux and the presence of a temperature dependent upper limit to electron transport. The measurements of gas exchange with which the model outputs may be compared include those of the temperature and partial pressure of CO2(p(CO2)) dependencies of quantum yield, the variation of compensation point with temperature and partial pressure of O2(p(O2)), the dependence of net CO2 assimilation rate on p(CO2) and irradiance, and the influence of p(CO2) and irradiance on the temperature dependence of assimilation rate.
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            Photosynthesis and nitrogen relationships in leaves of C3 plants

            The photosynthetic capacity of leaves is related to the nitrogen content primarily bacause the proteins of the Calvin cycle and thylakoids represent the majority of leaf nitrogen. To a first approximation, thylakoid nitrogen is proportional to the chlorophyll content (50 mol thylakoid N mol-1 Chl). Within species there are strong linear relationships between nitrogen and both RuBP carboxylase and chlorophyll. With increasing nitrogen per unit leaf area, the proportion of total leaf nitrogen in the thylakoids remains the same while the proportion in soluble protein increases. In many species, growth under lower irradiance greatly increases the partitioning of nitrogen into chlorophyll and the thylakoids, while the electron transport capacity per unit of chlorophyll declines. If growth irradiance influences the relationship between photosynthetic capacity and nitrogen content, predicting nitrogen distribution between leaves in a canopy becomes more complicated. When both photosynthetic capacity and leaf nitrogen content are expressed on the basis of leaf area, considerable variation in the photosynthetic capacity for a given leaf nitrogen content is found between species. The variation reflects different strategies of nitrogen partitioning, the electron transport capacity per unit of chlorophyll and the specific activity of RuBP carboxylase. Survival in certain environments clearly does not require maximising photosynthetic capacity for a given leaf nitrogen content. Species that flourish in the shade partition relatively more nitrogen into the thylakoids, although this is associated with lower photosynthetic capacity per unit of nitrogen.
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              Fitting photosynthetic carbon dioxide response curves for C(3) leaves.

              Photosynthetic responses to carbon dioxide concentration can provide data on a number of important parameters related to leaf physiology. Methods for fitting a model to such data are briefly described. The method will fit the following parameters: V(cmax), J, TPU, R(d) and g(m)[maximum carboxylation rate allowed by ribulose 1.5-bisphosphate carboxylase/oxygenase (Rubisco), rate of photosynthetic electron transport (based on NADPH requirement), triose phosphate use, day respiration and mesophyll conductance, respectively]. The method requires at least five data pairs of net CO(2) assimilation (A) and [CO(2)] in the intercellular airspaces of the leaf (C(i)) and requires users to indicate the presumed limiting factor. The output is (1) calculated CO(2) partial pressure at the sites of carboxylation, C(c), (2) values for the five parameters at the measurement temperature and (3) values adjusted to 25 degrees C to facilitate comparisons. Fitting this model is a way of exploring leaf level photosynthesis. However, interpreting leaf level photosynthesis in terms of underlying biochemistry and biophysics is subject to assumptions that hold to a greater or lesser degree, a major assumption being that all parts of the leaf are behaving in the same way at each instant.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: SupervisionRole: Validation
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Investigation
                Role: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 February 2018
                2018
                : 13
                : 2
                : e0192040
                Affiliations
                [1 ] Key Laboratory on Forest Ecology and Environmental Sciences of State Forestry Administration, Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, China
                [2 ] Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China
                [3 ] Tree and Timber Institute, National Research Council of Italy Sesto, Fiorentino, Italy
                Universidade Federal de Viçosa, BRAZIL
                Author notes

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

                Author information
                http://orcid.org/0000-0003-4233-3228
                Article
                PONE-D-17-11091
                10.1371/journal.pone.0192040
                5794133
                29390007
                24c0dbcd-bc7f-46e0-a2d0-ac433943b330
                © 2018 Tang et al

                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
                : 2 April 2017
                : 16 January 2018
                Page count
                Figures: 4, Tables: 5, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31290223
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31570240
                Award Recipient :
                This research was supported by projects of the National Natural Science Foundation of China, http://www.nsfc.gov.cn/ (funder: Ministry of National Science and Technology, China, no. 31290223 and 31570240, received by ZS). 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
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Legumes
                Fabaceae
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Trees
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Ribulose-1,5-Bisphosphate Carboxylase Oxygenase
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Ribulose-1,5-Bisphosphate Carboxylase Oxygenase
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Walls
                Plant Cell Walls
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Plant Cells
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                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Cells
                Plant Cell Walls
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                Plant Science
                Plant Cell Biology
                Plant Cells
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                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Rainforests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Rainforests
                Ecology and Environmental Sciences
                Terrestrial Environments
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                Biology and Life Sciences
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