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      Effect of Leaf Water Potential on Internal Humidity and CO 2 Dissolution: Reverse Transpiration and Improved Water Use Efficiency under Negative Pressure

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          Abstract

          The pull of water from the soil to the leaves causes water in the transpiration stream to be under negative pressure decreasing the water potential below zero. The osmotic concentration also contributes to the decrease in leaf water potential but with much lesser extent. Thus, the surface tension force is approximately balanced by a force induced by negative water potential resulting in concavely curved water-air interfaces in leaves. The lowered water potential causes a reduction in the equilibrium water vapor pressure in internal (sub-stomatal/intercellular) cavities in relation to that over water with the potential of zero, i.e., over the flat surface. The curved surface causes a reduction also in the equilibrium vapor pressure of dissolved CO 2, thus enhancing its physical solubility to water. Although the water vapor reduction is acknowledged by plant physiologists its consequences for water vapor exchange at low water potential values have received very little attention. Consequences of the enhanced CO 2 solubility to a leaf water-carbon budget have not been considered at all before this study. We use theoretical calculations and modeling to show how the reduction in the vapor pressures affects transpiration and carbon assimilation rates. Our results indicate that the reduction in vapor pressures of water and CO 2 could enhance plant water use efficiency up to about 10% at a leaf water potential of −2 MPa, and much more when water potential decreases further. The low water potential allows for a direct stomatal water vapor uptake from the ambient air even at sub-100% relative humidity values. This alone could explain the observed rates of foliar water uptake by e.g., the coastal redwood in the fog belt region of coastal California provided the stomata are sufficiently open. The omission of the reduction in the water vapor pressure causes a bias in the estimates of the stomatal conductance and leaf internal CO 2 concentration based on leaf gas exchange measurements. Manufactures of leaf gas exchange measurement systems should incorporate leaf water potentials in measurement set-ups.

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          Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.

          A series of experiments is presented investigating short term and long term changes of the nature of the response of rate of CO2 assimilation to intercellular p(CO2). The relationships between CO2 assimilation rate and biochemical components of leaf photosynthesis, such as ribulose-bisphosphate (RuP2) carboxylase-oxygenase activity and electron transport capacity are examined and related to current theory of CO2 assimilation in leaves of C3 species. It was found that the response of the rate of CO2 assimilation to irradiance, partial pressure of O2, p(O2), and temperature was different at low and high intercellular p(CO2), suggesting that CO2 assimilation rate is governed by different processes at low and high intercellular p(CO2). In longer term changes in CO2 assimilation rate, induced by different growth conditions, the initial slope of the response of CO2 assimilation rate to intercellular p(CO2) could be correlated to in vitro measurements of RuP2 carboxylase activity. Also, CO2 assimilation rate at high p(CO2) could be correlated to in vitro measurements of electron transport rate. These results are consistent with the hypothesis that CO2 assimilation rate is limited by the RuP2 saturated rate of the RuP2 carboxylase-oxygenase at low intercellular p(CO2) and by the rate allowed by RuP2 regeneration capacity at high intercellular p(CO2).
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            Vulnerability of Xylem to Cavitation and Embolism

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              Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited.

              J Flexas (2002)
              There is a long-standing controversy as to whether drought limits photosynthetic CO2 assimilation through stomatal closure or by metabolic impairment in C3 plants. Comparing results from different studies is difficult due to interspecific differences in the response of photosynthesis to leaf water potential and/or relative water content (RWC), the most commonly used parameters to assess the severity of drought. Therefore, we have used stomatal conductance (g) as a basis for comparison of metabolic processes in different studies. The logic is that, as there is a strong link between g and photosynthesis (perhaps co-regulation between them), so different relationships between RWC or water potential and photosynthetic rate and changes in metabolism in different species and studies may be 'normalized' by relating them to g. Re-analysing data from the literature using light-saturated g as a parameter indicative of water deficits in plants shows that there is good correspondence between the onset of drought-induced inhibition of different photosynthetic sub-processes and g. Contents of ribulose bisphosphate (RuBP) and adenosine triphosphate (ATP) decrease early in drought development, at still relatively high g (higher than 150 mmol H20 m(-2) s(-1)). This suggests that RuBP regeneration and ATP synthesis are impaired. Decreased photochemistry and Rubisco activity typically occur at lower g (<100 mmol H20 m(-2) s(-1)), whereas permanent photoinhibition is only occasional, occurring at very low g (<50 mmol H20 m(-2) s(-1)). Sub-stomatal CO2 concentration decreases as g becomes smaller, but increases again at small g. The analysis suggests that stomatal closure is the earliest response to drought and the dominant limitation to photosynthesis at mild to moderate drought. However, in parallel, progressive down-regulation or inhibition of metabolic processes leads to decreased RuBP content, which becomes the dominant limitation at severe drought, and thereby inhibits photosynthetic CO2 assimilation.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                06 February 2017
                2017
                : 8
                : 54
                Affiliations
                [1] 1Department of Physics, University of Helsinki Helsinki, Finland
                [2] 2Department of Forest Sciences, University of Helsinki Helsinki, Finland
                [3] 3Viikki Plant Science Centre, University of Helsinki Helsinki, Finland
                [4] 4Earth and Environmental Sciences Division, Los Alamos National Laboratory Los Alamos, NM, USA
                Author notes

                Edited by: Yoel Forterre, Centre National de la Recherche Scientifique (CNRS), France

                Reviewed by: H. Jochen Schenk, California State University, Fullerton, USA; Todd Edwin Dawson, University of California - Berkeley, USA

                *Correspondence: Tiia Grönholm tiia.gronholm@ 123456helsinki.fi

                This article was submitted to Plant Biophysics and Modeling, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2017.00054
                5292819
                28220128
                43355628-13a8-45ab-9fe0-d8ac3259deae
                Copyright © 2017 Vesala, Sevanto, Grönholm, Salmon, Nikinmaa, Hari and Hölttä.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 July 2016
                : 10 January 2017
                Page count
                Figures: 6, Tables: 1, Equations: 18, References: 55, Pages: 10, Words: 7104
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                water potential,co2 assimilation,carbon uptake,water uptake,kelvin effect,water use efficiency,redwood

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