The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways

Adams, 2013, May photoinhibition be a consequence, rather than a cause, of limited plant productivity?, Photosyn. Res., 117, 31, 10.1007/s11120-013-9849-7 Albertsson, 2001, A quantitative model of the domain structure of the photosynthetic membrane, Trends Plant Sci., 6, 349, 10.1016/S1360-1385(01)02021-0 Allakhverdiev, 2004, Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803, Biochim. Biophys. Acta, 1657, 23, 10.1016/j.bbabio.2004.03.003 Allen, 1992, Protein phosphorylation in regulation of photosynthesis, Biochim. Biophys. Acta, 1098, 275, 10.1016/S0005-2728(09)91014-3 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 Alric, 2010, Cyclic electron flow around photosystem I in unicellular green algae, Photosyn. Res., 106, 47, 10.1007/s11120-010-9566-4 Alric, 2005, Spectral and redox characterization of the heme ci of the cytochrome b6f complex, Proc. Natl. Acad. Sci. U S A, 102, 15860, 10.1073/pnas.0508102102 Andersson, 2008, Catalysis and regulation in Rubisco, J. Exp. Bot., 59, 1555, 10.1093/jxb/ern091 Asada, 1999, The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 601, 10.1146/annurev.arplant.50.1.601 Barber, 2008, Crystal structure of the oxygen-evolving complex of photosystem II, Inorg. Chem., 47, 1700, 10.1021/ic701835r Battchikova, 2011, Cyanobacterial NDH-1 complexes: Novel insights and remaining puzzles, Biochim. Biophys. Acta, 1807, 935, 10.1016/j.bbabio.2010.10.017 Bellafiore, 2005, State transitions and light adaptation require chloroplast thylakoid protein kinase STN7, Nature, 433, 892, 10.1038/nature03286 Bendall, 1995, Cyclic photophosphorylation and electron transport, Biochim. Biophys. Acta, 1229, 23, 10.1016/0005-2728(94)00195-B Bennett, 1977, Phosphorylation of chloroplast membrane polypeptides, Nature, 269, 344, 10.1038/269344a0 Benz, 2010, A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids, Trends Plant Sci., 15, 608, 10.1016/j.tplants.2010.08.008 Berry, 2003, Observations concerning the quinol oxidation site of the cytochrome bc1 complex, FEBS Lett., 555, 13, 10.1016/S0014-5793(03)01099-8 Berry, 2011, Conformationally linked interaction in the cytochrome bc1 complex between inhibitors of the Qo site and the Rieske iron–sulfur protein, Biochim. Biophys. Acta, 1807, 1349, 10.1016/j.bbabio.2011.04.005 Berry, 2000, Structure and function of cytochrome bc complexes, Annu. Rev. Biochem., 69, 1005, 10.1146/annurev.biochem.69.1.1005 Blackwell, 1990, Effect of integral membrane proteins on the lateral mobility of plastoquinone in phosphatidylcholine proteoliposomes, Biophys. J., 58, 1259, 10.1016/S0006-3495(90)82466-8 Bleier, 2013, Superoxide generation by complex III: from mechanistic rationales to functional consequences, Biochim. Biophys. Acta, 1827, 1320, 10.1016/j.bbabio.2012.12.002 Blumenfeld, 1994, Biophysical Thermodynamics of Intracellular Processes, 10.1007/978-1-4612-2630-7 Brandt, 1996, Bifurcated ubihydroquinone oxidation in the cytochrome bc1 complex by proton-gated charge transfer, FEBS Lett., 387, 1, 10.1016/0014-5793(96)00436-X Brandt, 1997, Role of deprotonation events in ubihydroquinone: cytochrome c oxidoreductase from bovine heart and yeast mitochondria, Biochemistry, 36, 11234, 10.1021/bi970968g Brettel, 1997, Electron transfer and arrangement of the redox cofactors in photosystem I, Biochim. Biophys. Acta, 1318, 322, 10.1016/S0005-2728(96)00112-0 Breyton, 2000, Conformational changes in the cytochrome b6f complex induced by inhibitor binding, J. Biol. Chem., 275, 13195, 10.1074/jbc.275.18.13195 Breyton, 2006, Redox modulation of cyclic electron flow around photosystem I in C3 plants, Biochemistry, 45, 13465, 10.1021/bi061439s Buchanan, 1980, Role of light in the regulation of chloroplast enzymes, Annu. Rev. Plant Physiol., 31, 341, 10.1146/annurev.pp.31.060180.002013 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 Burrows, 1998, Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes, EMBO J., 17, 868, 10.1093/emboj/17.4.868 Cape, 2006, Understanding the cytochrome bc complexes by what they don’t do. The Q-cycle at 30, Trends Plant Sci., 11, 46, 10.1016/j.tplants.2005.11.007 Cape, 2007, A semiquinone intermediate generated at the Qo site of the cytochrome bc1 complex: importance for the Q-cycle and superoxide production, Proc. Natl. Acad. Sci. U S A, 104, 7887, 10.1073/pnas.0702621104 Cardona, 2012, Charge separation in Photosystem II: A comparative and evolutionary overview, Biochim. Biophys. Acta, 1817, 26, 10.1016/j.bbabio.2011.07.012 Chance, 1956, The respiratory chain and oxidative phosphorylation, Adv. Enzymol., 17, 65 Chobot, 2008, Breaking the Q-cycle: finding new ways to study Qo through thermodynamic manipulations, J. Bioenerg. Biomembr., 40, 501, 10.1007/s10863-008-9175-5 Chovancová, 2012, CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures, PloS Comput. Biol., 8, e1002708, 10.1371/journal.pcbi.1002708 Cohen, 2004, Evidence for asymmetric electron transfer in cyanobacterial photosystem I: analysis of a methionine to leucine mutation of the ligand to the primary electron acceptor A0, Biochemistry, 43, 4741, 10.1021/bi035633f Covian, 2008, Regulatory interactions in the dimeric cytochrome bc1 complex: the advantages of being a twin, Biochim. Biophys. Acta, 1777, 1079, 10.1016/j.bbabio.2008.04.022 Cramer, 2006, Transmembrane traffic in the cytochrome b6f complex, Annu. Rev. Biochem., 75, 769, 10.1146/annurev.biochem.75.103004.142756 Cramer, 2011, The Q cycle of cytochrome bc complexes: a structure perspectives, Biochim. Biophys. Acta, 1807, 788, 10.1016/j.bbabio.2011.02.006 Crofts, 2004, The cytochrome bc1 complex: function in the context of structure, Annu. Rev. Physiol., 66, 689, 10.1146/annurev.physiol.66.032102.150251 Crofts, 2004, Proton-coupled electron transfer at the Qo-site of the bc1 complex controls the rate of ubihydroquinone oxidation, Biochim. Biophys. Acta, 1655, 77, 10.1016/j.bbabio.2003.10.012 Crofts, 1999, Mechanism of ubiquinol oxidation by the bc1 complex: role of the iron sulfur protein and its mobility, Biochemistry, 38, 15791, 10.1021/bi990961u Crofts, 1999, Physicochemical aspects of the movement of the Rieske iron sulfur protein during quinol oxidation by the bc1 complex from mitochondria and photosynthetic bacteria, Biochemistry, 38, 15827, 10.1021/bi990963e Crofts, 2000, Proton-coupled electron transfer at the Qo-site: what type of mechanism can account for the high activation barrier?, Biochim. Biophys. Acta, 1459, 456, 10.1016/S0005-2728(00)00184-5 Crofts, 2006, Proton pumping in the bc1 complex: A new gating mechanism that prevents short circuits, Biochim. Biophys. Acta, 1757, 1019, 10.1016/j.bbabio.2006.02.009 Crofts, 2013, The mechanism of ubihydroquinone oxidation at the Qo-site of the cytochrome bc1 complex, Biochim. Biophys. Acta, 1827, 1362, 10.1016/j.bbabio.2013.01.009 Cruz, 2005, Plasticity in light reactions of photosynthesis for energy production and photoprotection, J. Exp. Bot., 56, 395, 10.1093/jxb/eri022 DalCorso, 2008, A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis, Cell, 132, 273, 10.1016/j.cell.2007.12.028 Darrouzet, 2001, Large scale domain movement in cytochrome bc1: a new device for electron transfer in proteins, Trends Biochem. Sci., 26, 445, 10.1016/S0968-0004(01)01897-7 Dashdorj, 2005, Asymmetric electron transfer in cyanobacterial photosystem I: charge separation and secondary electron transfer dynamics of mutations near the primary electron acceptor A0, Biophys. J., 88, 1238, 10.1529/biophysj.104.050963 de Vitry, 2004, The chloroplast Rieske iron-sulfur protein: at the crossroad of electron transport and signal transduction, J. Biol. Chem., 279, 44621, 10.1074/jbc.M406955200 Delosme, 1996, Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii, Biochim. Biophys. Acta, 1273, 150, 10.1016/0005-2728(95)00143-3 Demmig-Adams, 1990, Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin, Biochim. Biophys. Acta, 1020, 1, 10.1016/0005-2728(90)90088-L Demmig-Adams, 2012, Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons, Photosyn. Res., 113, 75, 10.1007/s11120-012-9761-6 Dietz, 2011, Novel regulators in photosynthetic redox control of plant metabolism and gene expression, Plant Physiol., 155, 1477, 10.1104/pp.110.170043 Eberhard, 2008, The dynamics of photosynthesis, Annu. Rev. Genet., 42, 463, 10.1146/annurev.genet.42.110807.091452 Edwards, 1983 Endo, 1998, NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron donation to plastoquinone in tobacco chloroplasts, Plant Cell Physiol., 39, 1226, 10.1093/oxfordjournals.pcp.a029324 Ferreira, 2004, Architecture of the photosynthetic oxygen-evolving center, Science, 303, 1831, 10.1126/science.1093087 Finazzi, 2002, Redox-coupled proton pumping activity in cytochrome b6f, as evidenced by the pH dependence of electron transfer in whole cells of Chlamydomonas reinhardtii, Biochemistry, 41, 7475, 10.1021/bi025714w Finazzi, 1999, State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii, Biochim. Biophys. Acta, 1413, 117, 10.1016/S0005-2728(99)00089-4 Finazzi, 2001, Contrasted effects of inhibitors of cytochrome b6f complex on state transitions in Chlamydomonas reinhardtii: the role of Qo site occupancy in LHCII kinase activation, J. Biol. Chem., 276, 9770, 10.1074/jbc.M010092200 Finazzi, 2002, Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii, EMBO Rep., 3, 280, 10.1093/embo-reports/kvf047 Foyer, 2012, Photosynthetic control of electron transport and the regulation of gene expression, J. Exp. Bot., 63, 1637, 10.1093/jxb/ers013 Forti, 2003, In vivo changes of the oxidation-reduction state of NADP and the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii, Plant Physiol., 132, 1464, 10.1104/pp.102.018861 Frolov, 2009, The oxidation of plastoquinol by a cytochrome b6f complex: a density functional theory study, Russian J. Phys. Chem. A, 83, 506, 10.1134/S0036024409030315 Fromme, 2001, Structure of photosystem I, Biochim. Biophys. Acta, 1507, 5, 10.1016/S0005-2728(01)00195-5 Galka, 2012, Functional analyses of the plant photosystem I–light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II, Plant Cell, 24, 2963, 10.1105/tpc.112.100339 Gill, 2010, Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 48, 909, 10.1016/j.plaphy.2010.08.016 Gins, 1982, Peculiarities of the functioning of two molecular forms of pea ferredoxin in chloroplast electron transport chain, Biochemistry (Moscow), 47, 1581 Gong, 2001, Electron transfer and stability of the cytochrome b6f complex in a small domain deletion mutant of cytochrome f, J. Biol. Chem., 276, 24365, 10.1074/jbc.M010721200 Haehnel, 1976, The reduction kinetics of chlorophyll a1 as an indicator of for proton uptake between the light reactions in chloroplasts, Biochim. Biophys. Acta, 440, 506, 10.1016/0005-2728(76)90038-4 Haehnel, 1984, Photosynthetic electron transport in higher plants, Annu. Rev. Plant Physiol., 35, 659, 10.1146/annurev.pp.35.060184.003303 Hald, 2008, Feedback regulation of photosynthetic electron transport by NADP(H) redox poise, Biochim. Biophys. Acta, 1777, 433, 10.1016/j.bbabio.2008.02.007 Hald, 2008, Competition between linear and cyclic electron flow in plants deficient in Photosystem I, Biochim. Biophys. Acta, 1777, 1173, 10.1016/j.bbabio.2008.04.041 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 Hasan, 2013, Transmembrane signaling and assembly of the cytochrome b6f-lipidic charge transfer complex, Biochim. Biophys. Acta, 1827, 1295, 10.1016/j.bbabio.2013.03.002 Hasan, 2013, Lipid-induced conformational changes within the cytochrome b6f complex of oxygenic photosynthesis, Biochemistry, 52, 2649, 10.1021/bi301638h Hasan, 2013, Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b6f complex, Proc. Natl. Acad. Sci. U. S. A., 110, 4293, 10.1073/pnas.1222248110 Heimann, 2000, Movement of the Rieske iron-sulfur protein in the p-side bulk aqueous phase: effect of lumenal viscosity on redox reactions of the cytochrome b6f complex, Biochemistry, 39, 2692, 10.1021/bi9921992 Heldt, 1973, Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space, Biochim. Biophys. Acta, 314, 224, 10.1016/0005-2728(73)90137-0 Hertle, 2013, PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow, Mol. Cell, 49, 511, 10.1016/j.molcel.2012.11.030 Hofmann, 2012, A refined model of state transitions in plant thylakoid membranes, Plant Cell, 24, 2708, 10.1105/tpc.112.240711 Holzwarth, 2006, Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2: Mutations around the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor, Biophys. J., 90, 552, 10.1529/biophysj.105.059824 Hong, 1999, The energy landscape for ubihydroquinone oxidation at the Qo-site of the bc1 complex in Rhodobacter sphaeroides, J. Biol. Chem., 274, 33931, 10.1074/jbc.274.48.33931 Hong, 2012, Inter-monomer electron transfer is too slow to compete with monomeric turnover in bc1 complex, Biochim. Biophys. Acta, 1817, 1053, 10.1016/j.bbabio.2012.03.012 Hope, 1994, Effects of pH on the kinetics of redox reactions in and around the cytochrome bf complex in an isolated system, Photosyn. Res., 42, 111, 10.1007/BF02187122 Hsueh, 2010, NMR investigations of the Rieske protein from Thermus thermophilus support a coupled proton and electron transfer mechanism, J. Am. Chem. Soc., 132, 7908, 10.1021/ja1026387 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, Photosyn. Res., 57, 61, 10.1023/A:1006072230864 Iwai, 2010, Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis, Nature, 464, 1210, 10.1038/nature08885 Iwaki, 2005, Direct observation of redox-linked histidine protonation changes in the iron–sulfur protein of the cytochrome bc1 complex by ATR-FTIR spectroscopy, Biochemistry, 44, 4230, 10.1021/bi047533v Iwata, 1998, Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex, Science, 281, 64, 10.1126/science.281.5373.64 Izrailev, 1999, Steered molecular dynamics simulation of the Rieske subunit motion in the cytochrome bc1 complex, Biophys. J., 77, 1753, 10.1016/S0006-3495(99)77022-0 Jahns, 2012, The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II, Biochim. Biophys. Acta, 1817, 182, 10.1016/j.bbabio.2011.04.012 Joët, 2001, Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I, Plant Physiol., 125, 1919, 10.1104/pp.125.4.1919 Johnson, 2011, Physiology of PSI cyclic electron transport in higher plants, Biochim. Biophys. Acta, 1807, 906, 10.1016/j.bbabio.2011.05.008 Joliot, 2005, Quantification of cyclic and linear flows in plants, Proc. Natl. Acad. Sci. U S A, 102, 4913, 10.1073/pnas.0501268102 Jünemann, 1998, On the mechanism of quinol oxidation in the bc1 complex, J. Biol. Chem., 273, 21603, 10.1074/jbc.273.34.21603 Kim, 1998, Inhibitor binding changes domain mobility in the iron–sulphur protein of the mitochondrial bc1 complex from bovine heart, Proc. Natl. Acad. Sci. U S A, 95, 8026, 10.1073/pnas.95.14.8026 Kouril, 2005, Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana, Biochemistry, 44, 10935, 10.1021/bi051097a Kramer, 1999, How acidic is the lumen?, Photosyn. Res., 60, 151, 10.1023/A:1006212014787 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 Krieger, 1993, The role of calcium in the pH-dependent control of photosystem II, Photosyn. Res., 37, 117, 10.1007/BF02187470 Kubicki, 1996, Differential expression of plastome-encoded ndh genes in mesophyll and bundlesheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport, Planta, 199, 276, 10.1007/BF00196569 Kubota, 2010, Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits, Biochim. Biophys. Acta, 1797, 98, 10.1016/j.bbabio.2009.09.001 Kurisu, 2003, Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity, Science, 302, 1009, 10.1126/science.1090165 Kuvykin, 2008, Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants, Biochemistry (Moscow), 73, 1063, 10.1134/S0006297908100027 Kuvykin, 2011, Regulation of electron transport in C3 plant chloroplasts in situ and in silico, short-term effects of atmospheric CO2 and O2, Biochim. Biophys. Acta, 1807, 336, 10.1016/j.bbabio.2010.12.012 Leister, 2013, Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants, Front. Plant Sci., 4, 10.3389/fpls.2013.00161 Lemeille, 2010, State transitions at the crossroad of thylakoid signaling pathways, Photosyn. Res., 106, 33, 10.1007/s11120-010-9538-8 Lemeille, 2009, Analysis of the chloroplasts protein kinase Stt7 during state transition, PLoS Biol., 7, e1000045, 10.1371/journal.pbio.1000045 Lennartz, 2001, HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b6f complex in Arabidopsis, Plant Cell, 13, 2539, 10.1105/tpc.010245 Lhee, 2010, Modifications of protein environment of the [2Fe-2S] cluster of the bc1 complex: effects on the biophysical properties of the Rieske iron-sulfur protein and on the kinetics of the complex, J. Biol. Chem., 285, 9233, 10.1074/jbc.M109.043505 Li, 2000, A pigment-binding protein essential for regulation of photosynthetic light harvesting, Nature, 403, 391, 10.1038/35000131 Li, 2002, PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition, Proc. Natl. Acad. Sci. U S A, 99, 15222, 10.1073/pnas.232447699 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 Li, 2009, Sensing and responding to excess light, Annu. Rev. Plant Biol., 60, 239, 10.1146/annurev.arplant.58.032806.103844 Lin, 2006, Rieske protein from Thermus thermophilus: 15N NMR titration study demonstrates the role of iron-ligated histidines in the pH dependence of the reduction potential, J. Am. Chem. Soc., 128, 10672, 10.1021/ja0627388 Link, 1997, The role of the “Rieske” iron sulfur protein in the hydroquinone oxidation (Qp-) site of the cytochrome bc1 complex. The “proton-gated affinity change” mechanism, FEBS Lett., 412, 257, 10.1016/S0014-5793(97)00772-2 Mayer, 2004, Thermodynamics and kinetics of proton-coupled electron transfer: stepwise vs. concerted pathways, Biochim. Biophys. Acta, 1655, 51, 10.1016/j.bbabio.2003.07.002 Mehler, 1951, Studies on reactions of illuminated chloroplasts. I. Mechanisms of the reduction of oxygen and other Hill reagents, Arch. Biochem. Biophys., 33, 65, 10.1016/0003-9861(51)90082-3 Michelet, 2013, Redox regulation of the Calvin-Benson cycle: something old, something new, Front. Plant Sci., 4, 10.3389/fpls.2013.00470 Minagawa, 2011, State transitions—The molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast, Biochim. Biophys. Acta, 1807, 897, 10.1016/j.bbabio.2010.11.005 Mitchell, 1966, Chemiosmotic coupling in oxidative and photosynthetic phosphorylation, Biol. Rev., 41, 445, 10.1111/j.1469-185X.1966.tb01501.x Mitchell, 1976, Possible molecular mechanisms of the protonmotive function of cytochrome systems, J. Theor. Biol., 62, 327, 10.1016/0022-5193(76)90124-7 Mitchell, 1990, Plastoquinol diffusion in linear photosynthetic electron transport, Biophys. J., 58, 1011, 10.1016/S0006-3495(90)82445-0 Miyake, 2010, Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions, Plant Cell Physiol., 51, 1951, 10.1093/pcp/pcq173 Miyake, 2000, Determination of the rate of photoreduction of O2 in the water-water cycle in watermelon leaves and enhancement of the rate by limitation of photosynthesis, Plant Cell Physiol., 41, 335, 10.1093/pcp/41.3.335 Moser, 1997, Biological electron tunnelling through native protein media, J. Biol. Inorg. Chem., 2, 393, 10.1007/s007750050149 Motohashi, 2006, HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen, J. Biol. Chem., 281, 35039, 10.1074/jbc.M605938200 Müh, 2012, Light-induced quinone reduction in photosystem II, Biochim. Biophys. Acta, 1817, 44, 10.1016/j.bbabio.2011.05.021 Mula, 2012, Incorporation of a high potential quinone reveals that electron transfer in photosystem I becomes highly asymmetric at low temperature, Photochem. Photobiol. Sci., 11, 946, 10.1039/c2pp05340c Mulkidjanian, 2005, Ubiquinol oxidation in the cytochrome bc1 complex: reaction mechanism and prevention of short-circuiting, Biochim. Biophys. Acta, 1709, 5, 10.1016/j.bbabio.2005.03.009 Müller, 2001, Non-photochemical quenching. A response to excess light energy, Plant Physiol., 125, 1558, 10.1104/pp.125.4.1558 Müller, 2003, Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in photosystem I, Biophys. J., 85, 3899, 10.1016/S0006-3495(03)74804-8 Munekage, 2002, PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis, Cell, 110, 361, 10.1016/S0092-8674(02)00867-X Munekage, 2004, Cyclic electron flow around photosystem I is essential for photosynthesis, Nature, 429, 579, 10.1038/nature02598 Munekage, 2008, Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana, Plant Cell Physiol., 49, 1688, 10.1093/pcp/pcn140 Murata, 2009, The discovery of state transitions in photosynthesis 40 years ago, Photosyn. Res., 99, 155, 10.1007/s11120-008-9389-8 Murata, 2007, Photoinhibition of photosystem II under environmental stress, Biochim. Biophys. Acta, 1767, 414, 10.1016/j.bbabio.2006.11.019 Murata, 2012, The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport, Biochim. Biophys. Acta, 1817, 1127, 10.1016/j.bbabio.2012.02.020 Nakamura, 2011, Species dependence of the redox potential of the primary electron donor P700 in photosystem I of oxygenic photosynthetic organisms revealed by spectoelectrochemistry, Plant Cell Physiol., 52, 815, 10.1093/pcp/pcr034 Nelson, 2006, Structure and function of photosystems I and II, Annu. Rev. Plant Biol., 57, 521, 10.1146/annurev.arplant.57.032905.105350 Nitscke, 1992, The pH dependence of the redox midpoint of the 2Fe2S cluster from cytochrome b6f complex (the ‘Rieske centre’), Biochim. Biophys. Acta, 1102, 266, 10.1016/0005-2728(92)90109-F Ogawa, 2007, Cyanobacterial NADPH dehydrogenase complexes, Photosyn. Res., 93, 69, 10.1007/s11120-006-9128-y Ohyama, 1986, Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA, Nature, 322, 572, 10.1038/322572a0 Okegawa, 2008, Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts, Plant Cell Physiol., 49, 825, 10.1093/pcp/pcn055 Osyczka, 2004, Reversible redox energy coupling in electron transfer chains, Science, 427, 607 Osyczka, 2005, Fixing the Q cycle, Trends Biochem. Sci., 30, 176, 10.1016/j.tibs.2005.02.001 Page, 1999, Natural engineering principles of electron tunnelling in biological oxidation–reduction, Nature, 402, 47, 10.1038/46972 Peng, 2008, The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis, J. Biol. Chem., 283, 34873, 10.1074/jbc.M803207200 Peng, 2009, Efficient operation of NAD(P)H dehydrogenase requires the supercomplex formation with photosystem I via minor LHCI in Arabidopsis, Plant Cell, 21, 3623, 10.1105/tpc.109.068791 Peng, 2011, Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex, Biochim. Biophys. Acta, 1807, 945, 10.1016/j.bbabio.2010.10.015 Pfündel, 1993, The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts, Plant Physiol., 101, 65, 10.1104/pp.101.1.65 Pfündel, 1994, Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin deepoxidation, Plant Physiol., 106, 1647, 10.1104/pp.106.4.1647 Pierre, 1995, Purification and characterization of the cytochrome b6f complex from Chlamydomonas reinhardtii, J. Biol. Chem., 270, 29342, 10.1074/jbc.270.49.29342 Ponamarev, 1998, Perturbation of internal water chain in cytochrome f of oxygenic photosynthesis: loss of the concerted reduction of cytochromes f and b6, Biochemistry, 37, 17199, 10.1021/bi981814j Postila, 2013, Key role of water in proton transfer at the Qo-site of the cytochrome bc1 complex predicted by atomistic molecular dynamics simulations, Biochim. Biophys. Acta, 1827, 761, 10.1016/j.bbabio.2013.02.005 Rich, 2004, The quinone chemistry of bc complexes, Biochim. Biophys. Acta, 1658, 165, 10.1016/j.bbabio.2004.04.021 Roberts, 2002, Certain metal ions are inhibitors of cytochrome b6f complex ‘Rieske’ iron-sulfur protein domain movements, Biochemistry, 41, 4070, 10.1021/bi015996k Robinson, 1985, The involvement of stromal ATP in maintaining the pH gradient across the chloroplast envelope in the light, Biochim. Biophys. Acta, 806, 187, 10.1016/0005-2728(85)90096-9 Ruban, 2012, The photoprotective molecular switch in the photosystem II antenna, Biochim. Biophys. Acta, 1817, 167, 10.1016/j.bbabio.2011.04.007 Rumberg, 1969, pH changes in the inner phase of the thylakoids during photosynthesis, Naturwissenschaften, 56, 130, 10.1007/BF00601025 Ryzhikov, 1988, Regulation of electron transfer in photosynthetic membranes of higher plants, Biophysics (Moscow), 33, 642 Sainz, 2000, Interruption of the internal water chain of cytochrome f impairs photosynthetic function, Biochemistry, 39, 9164, 10.1021/bi0004596 Samoilova, 2002, The interaction of the Rieske iron sulfur protein with occupants of the Qo-site of the bc1 complex, probed by 1D and 2D electron spin echo envelope modulation, J. Biol. Chem., 277, 4605, 10.1074/jbc.C100664200 Savitsky, 2010, Alteration of the axial Met ligand to electron acceptor A0 in photosystem I: effect on the generation of P700·+A1·− radical pairs as studied by W-band transient EPR, Appl. Magn. Reson., 37, 85, 10.1007/s00723-009-0052-0 Sazanov, 1996, Detection and characterization of a complex I-like NADH-specific dehydrogenase from pea thylakoids, Biochem. Soc. Trans., 24, 739, 10.1042/bst0240739 Sazanov, 1998, The plastid ndh genes code for an NADH-specific dehydrogenase: Isolation of a complex I analogue from pea thylakoid membranes, Proc. Natl. Acad. Sci. U S A, 95, 1319, 10.1073/pnas.95.3.1319 Schönknecht, 1995, Relationship between photosynthetic electron transport and pH gradient across the thylakoid membrane in intact leaves, Proc. Natl. Acad. Sci. U S A, 92, 12185, 10.1073/pnas.92.26.12185 Semenov, 2008, Electrogenic reactions and dielectric properties of photosystem II, Photosyn. Res., 98, 121, 10.1007/s11120-008-9377-z Shelaev, 2010, Femtosecond primary charge separation in photosystem I, Biochim. Biophys. Acta, 1797, 1410, 10.1016/j.bbabio.2010.02.026 Shikanai, 2007, Cyclic electron transport around photosystem I: Genetic approaches, Annu. Rev. Plant Biol., 58, 199, 10.1146/annurev.arplant.58.091406.110525 Shikanai, 1998, Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I, Proc. Natl. Acad. Sci. U S A, 95, 9705, 10.1073/pnas.95.16.9705 Shinozaki, 1986, The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression, EMBO J., 5, 2043, 10.1002/j.1460-2075.1986.tb04464.x Siggel, 1976, The function of plastoquinone as electron and proton carrier in photosynthesis, Bioelectrochem. Bioenerg., 3, 302, 10.1016/0302-4598(76)80012-8 Snyder, 2000, Evidence for a concerted mechanism of ubiquinol oxidation by the cytochrome bc1 complex, J. Biol. Chem., 275, 13535, 10.1074/jbc.275.18.13535 Solovchenko, 2010, Photoprotection in Plants, 14 Soriano, 2002, Electron transfer from the Rieske iron-sulfur protein (ISP) to cytochrome f in vitro. Is a guided trajectory of the ISP necessary for competent docking?, J. Biol. Chem., 277, 41865, 10.1074/jbc.M205772200 Spetea, 1997, Low pH accelerates light-induced damage of photosystem II by enhancing the probability of the donor-side mechanism of photoinhibition, Biochim. Biophys. Acta, 1318, 275, 10.1016/S0005-2728(96)00145-4 Stiehl, 1969, Quantitative treatment of the function of plastoquinone in photosynthesis, Z. Naturforsch. Teil. B, 24, 1588, 10.1515/znb-1969-1219 Stroebel, 2003, An atypical heam in the cytochrome b6f complex, Nature, 426, 413, 10.1038/nature02155 Suorsa, 2012, PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions, Plant Cell, 24, 2934, 10.1105/tpc.112.097162 Swierczek, 2010, An electronic bus bar lies in the core of cytochrome bc1, Science, 329, 451, 10.1126/science.1190899 Tagawa, 1963, Role of chloroplast ferredoxin in the energy conversion process of photosynthesis, Proc. Natl. Acad. Sci. U S A, 49, 567, 10.1073/pnas.49.4.567 Takahashi, 2011, Photoprotection in plants: a new light on photosystem II damage, Trends Plant Sci., 16, 53, 10.1016/j.tplants.2010.10.001 Tikhonov, 2012, Energetic and regulatory role of proton potential in chloroplasts, Biochemistry (Moscow), 77, 956, 10.1134/S0006297912090027 Tikhonov, 2013, pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts, Photosyn. Res., 116, 511, 10.1007/s11120-013-9845-y Tikhonov, 1985, Electron transport, proton translocation, and their relation to photophosphorylation in chloroplasts. II. Spin label tempamine as the indicator of the light-induced uptake of protons by chloroplasts, Biol. Membr. (Moscow), 2, 608 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 Tikhonov, 2008, Spin-probes designed for measuring the intrathylakoid pH in chloroplasts, Biochim. Biophys. Acta, 1777, 285, 10.1016/j.bbabio.2007.12.002 Tikkanen, 2012, Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants, Biochim. Biophys. Acta, 1817, 232, 10.1016/j.bbabio.2011.05.005 Tikkanen, 2014, Integrative regulatory network of plant thylakoid energy transduction, Trends Plant Sci., 19, 10, 10.1016/j.tplants.2013.09.003 Tikkanen, 2011, Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’, Trends Plant Sci., 16, 126, 10.1016/j.tplants.2010.11.006 Tikkanen, 2012, Regulation of the photosynthetic apparatus under fluctuating growth light, Philos. Trans. R. Soc. Lond. B Biol. Sci., 367, 3486, 10.1098/rstb.2012.0067 Tremmel, 2003, Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins, Biochim. Biophys. Acta, 1603, 97, 10.1016/j.bbabio.2003.09.004 Trubitsin, 2003, Determination of a transmembrane pH difference in chloroplasts with a spin label Tempamine, J. Magn. Reson., 163, 257, 10.1016/S1090-7807(03)00110-1 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 Umena, 2011, Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å, Nature, 473, 55, 10.1038/nature09913 Vallon, 1991, Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions, Proc. Natl. Acad. Sci. U S A, 88, 8262, 10.1073/pnas.88.18.8262 Vener, 1997, Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: Thylakoid protein kinase deactivation by a single-turnover flash, Proc. Natl. Acad. Sci. U S A, 94, 1585, 10.1073/pnas.94.4.1585 Victoria, 2013, Role of the –PEWY-glutamate in catalysis at the Qo-site of the Cyt bc1 complex, Biochim. Biophys. Acta, 1827, 365, 10.1016/j.bbabio.2012.10.012 Witt, 1979, Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods, Biochim. Biophys. Acta, 505, 355, 10.1016/0304-4173(79)90008-9 Wollman, 2001, State transitions reveal the dynamics and flexibility of the photosynthetic apparatus, EMBO J., 20, 3623, 10.1093/emboj/20.14.3623 Wood, 1988, The potential diagram for oxygen at pH 7, Biochem. J., 253, 287, 10.1042/bj2530287 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 Xia, 1997, Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria, Science, 277, 60, 10.1126/science.277.5322.60 Xia, 2013, Structural analysis of cytochrome bc1 complexes: implications to the mechanism of function, Biochim. Biophys. Acta, 1827, 1278, 10.1016/j.bbabio.2012.11.008 Yamamoto, 2006, Ferredoxin limits cyclic electron flow around PSI (CEF-PSI) in higher plants–Stimulation of CEF-PSI enhances nonphotochemical quenching of Chl fluorescence in transplastomic tobacco, Plant Cell Physiol., 47, 1355, 10.1093/pcp/pcl005 Yamamoto, 2011, An Src homology 3 domain-like fold protein forms a ferredoxin-binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis, Plant Cell, 23, 1480, 10.1105/tpc.110.080291 Yan, 2003, Functional insensitivity of the cytochrome b6f complex to structure changes in the hinge region of the Rieske iron-sulfur protein, J. Biol. Chem., 278, 20925, 10.1074/jbc.M212616200 Zhang, 2004, Light-harvesting complex II binds to several small subunits of photosystem I, J. Biol. Chem., 279, 3180, 10.1074/jbc.M311640200 Zhang, 1996, Characterization and crystallization of the lumen side domain of the chloroplast Rieske iron-sulfur protein, J. Biol. Chem., 271, 31360, 10.1074/jbc.271.49.31360 Zhang, 1998, Electron transfer by domain movement in cytochrome bc1, Nature, 392, 677, 10.1038/33612 Zhu, 2007, Simultaneous reduction of iron-sulfur protein and cytochrome bL during ubiquinol oxidation in cytochrome bc1 complex, Proc. Natl. Acad. Sci. U S A, 104, 4864, 10.1073/pnas.0607812104 Zito, 1998, Glu78, from the conserved PEWY sequence of subunit IV, has a key function in the cytochrome b6f turnover, Biochemistry, 37, 10395, 10.1021/bi980238o Zito, 1999, The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase, EMBO J., 18, 2961, 10.1093/emboj/18.11.2961 Zouni, 2001, Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution, Nature, 409, 739, 10.1038/35055589 Zu, 2003, Reduction potentials of Rieske clusters: Importance of the coupling between oxidation state and histidine protonation state, Biochemistry, 42, 12400, 10.1021/bi0350957