Regulation of electron transport in C3 plant chloroplasts in situ and in silico: Short-term effects of atmospheric CO2 and O2

Edwards, 1983 Noctor, 2000, Homeostasis of adenylate status during photosynthesis in a fluctuating environment, J. Exp. Botany, 51, 347, 10.1093/jexbot/51.suppl_1.347 Haldrup, 2001, Balance of power: a view of the mechanism of photosynthetic state transitions, Trends Plant Sci., 6, 301, 10.1016/S1360-1385(01)01953-7 Allen, 2003, State transitions—a question of balance, Science, 299, 1530, 10.1126/science.1082833 Allen, 2003, Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain, Trends Plant Sci., 8, 15, 10.1016/S1360-1385(02)00006-7 Pfannschmidt, 2003, Chloroplast redox signals: how photosynthesis controls its own genes, Trends Plant Sci., 8, 33, 10.1016/S1360-1385(02)00005-5 Kramer, 2003, Balancing the central roles of the thylakoid proton gradient, Trends Plant Sci., 8, 27, 10.1016/S1360-1385(02)00010-9 Kramer, 2004, Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions, Trends Plant. Sci., 9, 349, 10.1016/j.tplants.2004.05.001 Kanervo, 2005, Functional flexibility and acclimation of the thylakoid membrane, Photochem. Photobiol. Sci., 4, 1072, 10.1039/b507866k Cruz, 2007, Plasticity in light reactions of photosynthesis for energy production and photoprotection, J. Exp. Botany, 56, 395, 10.1093/jxb/eri022 Baker, 2007, Determining the limitations and regulation of photosynthetic energy transduction in leaves, Plant, Cell & Environment, 30, 1107, 10.1111/j.1365-3040.2007.01680.x Li, 2009, Sensing and responding to excess light, Annu. Rev. Plant Biol., 60, 239, 10.1146/annurev.arplant.58.032806.103844 Werdan, 1975, The role of pH in the regulation of carbon fixation in the chloroplast stroma. Studies on CO2 fixation in the light and dark, Biochim. Biophys. Acta, 396, 276, 10.1016/0005-2728(75)90041-9 Mott, 1986, Effects of pH on activity and activation of ribulose 1, 5-biphosphate carboxylase at air level CO2, Plant Physiol., 82, 77, 10.1104/pp.82.1.77 Andersson, 2008, Catalysis and regulation in Rubisco, J. Exp. Botany, 59, 1555, 10.1093/jxb/ern091 Sage, 2002, The activation state of rubisco directly limits photosynthesis at low CO2 and low O2 partial pressure, Photosyn. Res., 71, 241, 10.1023/A:1015510005536 Bendall, 1995, Cyclic photophosorylation and electron transport, Biochim. Biophys. Acta, 1229, 23, 10.1016/0005-2728(94)00195-B Joliot, 2002, Cyclic electron transfer in plant leaf, Proc. Natl. Acad. Sci. USA, 99, 10209, 10.1073/pnas.102306999 Joët, 2002, Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex, Plant Physiol., 128, 760, 10.1104/pp.010775 Munekage, 2004, Cyclic electron flow around photosystem I is essential for photosynthesis, Nature, 429, 579, 10.1038/nature02598 Johnson, 2005, Cyclic electron transport in C3 plants: fact or artefact?, J. Exp. Bot., 56, 407, 10.1093/jxb/eri106 Joliot, 2005, Quantification of cyclic and linear flows in plants, Proc. Natl. Acad. Sci. USA, 102, 4913, 10.1073/pnas.0501268102 Iwai, 2010, Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis, Nature, 464, 1210, 10.1038/nature08885 Backhausen, 2000, Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons, Photosynth. Res., 64, 1, 10.1023/A:1026523809147 Asada, 1999, The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons, Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 601, 10.1146/annurev.arplant.50.1.601 Heber, 2002, Irrungen, wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants, Photosynth. Res., 73, 223, 10.1023/A:1020459416987 Badger, 2000, Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase, Philos. Trans. R. Soc. Lond. B, 355, 1433, 10.1098/rstb.2000.0704 Ort, 2002, A photoprotective role for O2 as an alternative electron sink in photosynthesis?, Curr. Opp. Plant Biol., 5, 193, 10.1016/S1369-5266(02)00259-5 Rumeau, 2007, Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response, Plant, Cell & Environ., 30, 1041, 10.1111/j.1365-3040.2007.01675.x Stiehl, 1969, Quantitative treatment of the function of plastoquinone in photosynthesis, Z. Naturforsch. Teil B, 24, 1588, 10.1515/znb-1969-1219 Rumberg, 1969, pH changes in the inner phase of the thylakoids during photosynthesis, Naturwissenschaften, 56, 130, 10.1007/BF00601025 Tikhonov, 1981, Electron transport control in chloroplasts. Effects of photosynthetic control monitored by the intrathylakoid pH, Biochim. Biophys. Acta, 637, 321, 10.1016/0005-2728(81)90171-7 Tikhonov, 1984, Electron transport control in chloroplasts. Effects of magnesium ions on the electron flow between two photosystems, Photobiochem. Photobiophys., 8, 261 Sigalat, 1993, Flow-force relationships in lettuce thylakoids. 1. Strict control of electron flow by internal pH, Biochemistry, 32, 10193, 10.1021/bi00089a040 Blumenfeld, 1994 Kramer, 1999, How acidic is the lumen?, Photosynth. Res., 60, 151, 10.1023/A:1006212014787 Maxwell, 2000, Chlorophyll fluorescence: a practical guide, J. Exp. Botany, 51, 659, 10.1093/jexbot/51.345.659 Müller, 2001, Non-photochemical quenching. A response to excess light energy, Plant Physiol., 125, 1558, 10.1104/pp.125.4.1558 Li, 2004, Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein, J. Biol. Chem., 279, 22866, 10.1074/jbc.M402461200 Baker, 2008, Chlorophyll fluorescence: a probe of photosynthesis in vivo, Annu. Rev. Plant Biol., 59, 89, 10.1146/annurev.arplant.59.032607.092759 Allakhverdiev, 2008, Heat stress: an overview of molecular responses in photosynthesis, Photosynth. Res., 98, 541, 10.1007/s11120-008-9331-0 Tagawa, 1963, Analysis of photosynthetic reactions by the use of monochromatic light, Nature, 199, 1247, 10.1038/1991247a0 Kobayashi, 1994, Rates of vectorial proton transport supported by cyclic electron flow during oxygen reduction by illuminated intact chloroplasts, Photosynth. Res., 41, 419, 10.1007/BF02183044 Peltier, 2002, Chlororespiration, Annu. Rev. Plant Biol., 53, 523, 10.1146/annurev.arplant.53.100301.135242 Sage, 2002, The activation state of rubisco directly limits photosynthesis at low CO2 and low O2 partial pressure, Photosynth. Res., 71, 241, 10.1023/A:1015510005536 Cornic, 1991, Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress, Planta, 183, 178, 10.1007/BF00197786 Golding, 2003, Down-regulation of linear and activation of cyclic electron transport during drought, Planta, 218, 107, 10.1007/s00425-003-1077-5 Buchanan, 1991, Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development, Arch. Biochem. Biophys., 288, 1, 10.1016/0003-9861(91)90157-E Hendrey, 1997, Can photosynthesis respond to short-term fluctuations in atmospheric carbon dioxide?, Photosynth. Res., 51, 179, 10.1023/A:1005804203928 Chow, 2004, Electron fluxes through photosystem I in cucumber leaf discs probed by far-red light, Photosynth. Res., 81, 77, 10.1023/B:PRES.0000028396.83954.36 Kuvykin, 2008, Oxygen as an alternative acceptor in the photosynthetic electron transfer chain in C3 plants, Biochemistry (Moscow), 73, 1063, 10.1134/S0006297908100027 Trubitsin, 2003, EPR study of light-induced regulation of photosynthetic electron transport in Synechocystis sp. strain PCC 6803, FEBS Letters, 544, 15, 10.1016/S0014-5793(03)00429-0 Trubitsin, 2005, EPR study of electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Oxygen-dependent interrelations between photosynthetic and respiratory electron transport chains, Biochim. Biophys. Acta, 1708, 238, 10.1016/j.bbabio.2005.03.004 E. Rabinovitch, Photosynthesis and Related Processes. 1956. V. II, part 2. Oxborough, 1997, Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components—calculation of qP and Fv'/Fm' without measuring Fo', Photosynth. Res., 54, 135, 10.1023/A:1005936823310 Dubinskii, 1994, Regulation of electron and proton transport in the chloroplasts. Kinetic model and comparison of it with the experiment, Biophysics, 39, 657 Dubinskii, 1995, Mathematical simulation of the light-induced uptake of protons by chloroplasts upon various mechanisms of proton leak through the thylakoid membrane, Biophysics, 40, 341 Dubinskii, 1997, Mathemetical model of thylakoid as the distributed heterogeneous system of electron and proton transport, Biophysics, 42, 644 Vershubskii, 2001, Electron and proton transport in chloroplasts: a mathematical model constructed with regard for the lateral heterogeneity of thylakoids, Biophysics, 46, 448 Vershubskii, 2004, Mathematical modeling of electron and proton transport coupled with ATP synthesis in chloroplasts, Biophysics, 49, 52 Vershubskii, 2004, Effects of diffusion and topological factors on the efficiency of energy coupling in chloroplasts with heterogeneous partitioning of protein complexes in thylakoids of grana and stroma. A mathematical model, Biochemistry (Moscow), 69, 1016, 10.1023/B:BIRY.0000043544.53016.8d Vershubskii, 2006, Kinetic model for electron and proton transport in chloroplasts with nonuniform distribution of protein complexes in thylakoid membranes, Russian J. Phys. Chem., 80, 467, 10.1134/S0036024406030289 Frolov, 2007, Influence of light-induced changes in stromal and lumenal pH on electron transport kinetics in chloroplasts: mathematical modeling, Biophysics, 52, 398, 10.1134/S0006350907040070 Kuvykin, 2009, Alternative routes of photoinduced electron transport in chloroplasts, Russian J. Phys. Chem. B, 3, 230, 10.1134/S1990793109020092 Kuvykin, 2009, Computer simulation study of pH-dependent regulation of electron transport in chloroplasts, Biophysics, 54, 455, 10.1134/S0006350909040101 Vershubskii, 2011, Functional and topological aspects of pH-dependent regulation of electron and proton transport in chloroplasts in silico, BioSystems, 103, 164, 10.1016/j.biosystems.2010.08.002 Sharkey, 2007, Fitting photosynthetic carbon dioxide response curves for C3 leaves, Plant, Cell & Environ., 30, 1035, 10.1111/j.1365-3040.2007.01710.x Webber, 2001, P700: the primary electron donor of photosystem I, Biochim. Biophys. Acta, 1507, 61, 10.1016/S0005-2728(01)00198-0 Heber, 1992, Chloroplast energization and oxidation of P700/plastocyanin in illuminated leaves at reduced level of CO2 or oxygen, Photosynth. Res., 34, 433, 10.1007/BF00029817 Ivanov, 1998, Photosystem I-dependent cyclic electron flow in intact spinach chloroplasts: occurrence dependence on redox conditions and electron acceptors and inhibition by antimycin A, Photosynth. Res., 57, 61, 10.1023/A:1006072230864 Breyton, 2006, Redox modulation of cyclic electron flow around photosystem I in C3 plants, Biochemistry, 45, 13465, 10.1021/bi061439s Ryzhikov, 1988, Regulation of electron transfer in photosynthetic membranes of higher plants, Biophysics, 33, 642 Björkman, 1987, Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins, Planta, 170, 489, 10.1007/BF00402983 Johnson, 1993, The dissipation of excess excitation energy in British plant species, Plant, Cell & Environ., 16, 673, 10.1111/j.1365-3040.1993.tb00485.x Karavaev, 1975, Adaptation to the dark and far red light of the leaves of higher plants in conditions of oxygen lack, Biophysics, 20, 86 Lazar, 1999, Chlorophyll a fluorescence induction, Biochim. Biophys. Acta, 1412, 1 Kanazawa, 2002, In vivo modulation of non-photochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase, Proc. Natl. Acad. Sci. USA, 99, 12789, 10.1073/pnas.182427499 Avenson, 2004, Modulation of energy dependent quenching of excitons in antenna of higher plants, Proc. Natl. Acad. Sci. USA, 101, 5530, 10.1073/pnas.0401269101 Ligeza, 1994, Oxygen production and consumption by chloroplasts in situ and in vitro as studied with microscopic spin label probes, Biochim. Biophys. Acta, 1186, 201, 10.1016/0005-2728(94)90179-1 Ligeza, 1997, In situ measurements of oxygen production and consumption using paramagnetic fusinite particles injected into a bean leaf, Biochim. Biophys. Acta, 1319, 133, 10.1016/S0005-2728(96)00122-3 Roussel, 2011, Dynamics and mechanisms of oscillatory photosynthesis, BioSystems, 103, 230, 10.1016/j.biosystems.2010.07.020 Woodrow, 1988, Enzymatic regulation of photosynthetic CO2 fixation in C3 plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 39, 533, 10.1146/annurev.pp.39.060188.002533 Jensen, 1977, Ribulose 1,5-bisphosphate carboxylase-oxygenase, Annu. Rev. Plant Physiol., 28, 379, 10.1146/annurev.pp.28.060177.002115 Pickersgill, 1986, An upper limit to the active site concentration of ribulose bisphosphate carboxylase in chloroplasts, Biochem. J., 236, 311, 10.1042/bj2360311 Trubitsin, 2003, Determination of a transmembrane pH difference in chloroplasts with a spin label tempamine, J. Magn. Res., 163, 257, 10.1016/S1090-7807(03)00110-1 Tikhonov, 2008, Spin-probes designed for measuring the intrathylakoid pH in chloroplasts, Biochim. Biophis. Acta, 1777, 285, 10.1016/j.bbabio.2007.12.002 Nishio, 1994, Dissipation of the proton electrochemical potential in intact chloroplasts. II. The pH gradient monitored by cytochrome f reduction kinetics, Plant Physiol., 101, 89, 10.1104/pp.101.1.89 Takizawa, 2007, The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf, Biochim. Biophys. Acta, 1767, 1233, 10.1016/j.bbabio.2007.07.006 Heldt, 1973, Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space, Biochim. Biophis. Acta, 314, 224, 10.1016/0005-2728(73)90137-0 Robinson, 1985, The involvement of stromal ATP in maintaining the pH gradient across the chloroplast envelope in the light, Biochim. Biophis. Acta, 806, 187, 10.1016/0005-2728(85)90096-9 Tsuyama, 2009, Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis, Photosynth. Res., 99, 37, 10.1007/s11120-008-9379-x Sivak, 1983, Some effects of CO2 concentration and decreased O2 concentration on induction fluorescence in leaves, Proc. R. Soc. Lond. B, 217, 377, 10.1098/rspb.1983.0016 Sivak, 1983, Some effects of changes in gas phase on the steady-state chlorophyll a fluorescence exhibited by illuminated leaves, Proc. R. Soc. Lond. B, 217, 393, 10.1098/rspb.1983.0017 Bradbury, 1985, An analysis of the chlorophyll-fluorescence transients from pea leaves generated by changes in atmospheric concentrations of CO2 and O2, Biochim. Biophis. Acta, 806, 357, 10.1016/0005-2728(85)90243-9