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      Limitations to photosynthesis by proton motive force-induced photosystem II photodamage

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          Abstract

          The thylakoid proton motive force ( pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δ ψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δ ψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.

          DOI: http://dx.doi.org/10.7554/eLife.16921.001

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          Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement.

          Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chemical fuels in the case of natural photosynthesis and nonstored electrical current in the case of photovoltaics. In order to find common ground for evaluating energy-conversion efficiency, we compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. We consider opportunities in which the frontiers of synthetic biology might be used to enhance natural photosynthesis for improved solar energy conversion efficiency.
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            New fluorescence parameters for the determination of q(a) redox state and excitation energy fluxes.

            A number of useful photosynthetic parameters are commonly derived from saturation pulse-induced fluorescence analysis. We show, that q(P), an estimate of the fraction of open centers, is based on a pure 'puddle' antenna model, where each Photosystem (PS) II center possesses its own independent antenna system. This parameter is incompatible with more realistic models of the photosynthetic unit, where reaction centers are connected by shared antenna, that is, the so-called 'lake' or 'connected units' models. We thus introduce a new parameter, q(L), based on a Stern-Volmer approach using a lake model, which estimates the fraction of open PS II centers. We suggest that q(L) should be a useful parameter for terrestrial plants consistent with a high connectivity of PS II units, whereas some marine species with distinct antenna architecture, may require the use of more complex parameters based on intermediate models of the photosynthetic unit. Another useful parameter calculated from fluorescence analysis is Phi(II), the yield of PS II. In contrast to q(L), we show that the Phi(II) parameter can be derived from either a pure 'lake' or pure 'puddle' model, and is thus likely to be a robust parameter. The energy absorbed by PS II is divided between the fraction used in photochemistry, Phi(II), and that lost non-photochemically. We introduce two additional parameters that can be used to estimate the flux of excitation energy into competing non-photochemical pathways, the yield induced by downregulatory processes, Phi(NPQ), and the yield for other energy losses, Phi(NO).
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              Photoprotection and Other Responses of Plants to High Light Stress

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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                04 October 2016
                2016
                : 5
                : e16921
                Affiliations
                [1 ]deptDepartment of Energy Plant Research Laboratory , Michigan State University , East Lansing, United States
                [2 ]deptGraduate Program of Cell and Molecular Biology , Michigan State University , East Lansing, United States
                [3 ]deptDepartment of Chemistry , Michigan State University , East Lansing, United States
                [4 ]Max-Planck-Institut für Molekulare Pflanzenphysiologie , Potsdam-Golm, Germany
                [5 ]deptDepartment of Life Sciences , Imperial College London , London, United Kingdom
                [6 ]deptDepartment of Horticulture , Washington State University , Pullman, United States
                [7 ]deptDepartment of Biochemistry and Molecular Biology , Michigan State University , East Lansing, United States
                [8]University of California, Berkeley , United States
                [9]University of California, Berkeley , United States
                Author notes
                [†]

                Graduate School of Life Sciences, Tohoku University, Sendai, Japan.

                Author information
                http://orcid.org/0000-0003-2181-6888
                Article
                16921
                10.7554/eLife.16921
                5050024
                27697149
                cb1e75fe-5dd2-41db-945d-cdbc6574e3a8
                © 2016, Davis et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 14 April 2016
                : 08 September 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100006151, Basic Energy Sciences;
                Award ID: DE-FG02-91ER20021
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/K002627/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000288, Royal Society;
                Award ID: Wolfson Research Merit Award
                Award Recipient :
                Funded by: Michigan State University Center for Advanced Algal and Plant Phenotyping;
                Award Recipient :
                Funded by: Michigan State University AgBioResearch;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Biochemistry
                Plant Biology
                Research Article
                Custom metadata
                2.5
                Storage of solar energy in the thylakoid electrical field by photosynthesis in vivo can substantially destabilize charge-separated states in photosystem II, leading to singlet oxygen production and photodamage, contributing to loss of productivity, especially under fluctuating light experienced in the field.

                Life sciences
                photosynthesis,proton motive force,photoinhibition,<i>a. thaliana</i>
                Life sciences
                photosynthesis, proton motive force, photoinhibition, <i>a. thaliana</i>

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