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Bioenergetic Pathways in the Chloroplast: Photosynthetic Electron Transfer

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Chlamydomonas: Molecular Genetics and Physiology

Part of the book series: Microbiology Monographs ((MICROMONO,volume 30))

Abstract

In this review, we address bioenergetic pathways in the chloroplast of Chlamydomonas reinhardtii, with a focus on photosynthetic electron transfer. The conversion of solar energy into chemical energy by oxygenic photosynthesis, as performed by plants, green algae and cyanobacteria, supports the life on this planet. The production of oxygen (O2) and the assimilation of carbon dioxide (CO2) into organic matter determine, to a large extent, the composition of our atmosphere. Plant photosynthesis is conducted by a series of reactions that occur mainly in the chloroplast, resulting in light-dependent H2O oxidation, NADP+ reduction and ATP formation. NADPH and ATP, produced by linear electron flow (LEF), are required for carbon fixation via the Calvin-Benson-Bassham (CBB) cycle. Besides, photosynthetic electron transfer may operate in a cyclic electron flow (CEF) mode to satisfy the cellular ATP demand. Electrons derived from LEF may also be diverted to various other metabolic pathways, e.g. via ferredoxin (FDX). In addition, photosynthesis evolved to maximize its outcome while minimizing photooxidative stress. In this regard, mechanisms such as non-photochemical quenching (NPQ) and state transitions regulate energy influx at different light availabilities, which feedback to the proton-motive force (pmf) and the redox state of the plastoquinone/plastoquinol (PQ) pool, thereby also regulating LEF and CEF. To overcome possible limitations in electron transfer at the acceptor side of photosystem (PSI), alternative electron transfer pathways evolved, including flavodiiron proteins (FDPs), allowing safe utilization of O2 as alternative electron acceptor, as well as the hydrogenase, which utilizes two electrons and two protons to produce H2. Nevertheless, reactive oxygen species (ROS) may be formed, e.g. via the Mehler reaction at the acceptor side of PSI, which is why photosynthetic electrons are also utilized in detoxification mechanisms to prevent excessive damage. In conclusion, photosynthetic electron transfer is interwoven in a regulatory network that is aimed at adjusting ATP and NADPH production in a way that electron transfer is not harmful to the cell.

Authors Philipp Gäbelein and Laura Mosebach contributed equally to the work.

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References

  • Ahmad N, Michoux F, Nixon PJ (2012) Investigating the production of foreign membrane proteins in tobacco chloroplasts: expression of an algal plastid terminal oxidase. PLoS One. doi:10.1371/journal.pone.0041722

  • Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro E-M (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci U S A 110:4111–4116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen JF (2002) Photosynthesis of ATP – electrons, proton pumps, rotors, and poise. Cell 110:273–276

    Article  CAS  PubMed  Google Scholar 

  • Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, Petroutsos D, Kuntz M, Breyton C et al (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allorent G, Lefebvre-legendre L, Chappuis R, Kuntz M, Truong TB (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. 1–6

    Google Scholar 

  • Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106:47–56

    Article  CAS  PubMed  Google Scholar 

  • Alric J (2014) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii: (II) involvement of the PGR5-PGRL1 pathway under anaerobic conditions. Biochim Biophys Acta 1837:825–834

    Article  CAS  PubMed  Google Scholar 

  • Alric J, Lavergne J, Rappaport F (2010) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim Biophys Acta 1797:44–51

    Article  CAS  PubMed  Google Scholar 

  • Aran M, Caporaletti D, Senn AM, Tellez De Iñon MT, Girotti MR, Llera AS, Wolosiuk RA (2008) ATP-dependent modulation and autophosphorylation of rapeseed 2-Cys peroxiredoxin. FEBS J 275:1450–1463

    Article  CAS  PubMed  Google Scholar 

  • Armbruster U, Carrillo RL, Venema K, Pavlovic L, Schmidtmann E, Kornfeld A, Jahns P, Berry JA, Kramer DM, Jonikas MC (2014) Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat Commun 5:5439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armbruster U, Leonelli L, Galvis VC, Strand D, Quinn EH, Jonikas MC, Niyogi KK (2016) Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light. Plant Cell Physiol 57:1557–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond Ser B Biol Sci 355:1419–1431

    Article  CAS  Google Scholar 

  • Asada K, Kanematsu S, Uchida K (1977) Superoxide dismutases in photosynthetic organisms: absence of the cuprozinc enzyme in eukaryotic algae. Arch Biochem Biophys 179:243–256

    Article  CAS  PubMed  Google Scholar 

  • Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci 102(27):9709–9713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Ballottari M, Truong TB, De Re E, Erickson E, Stella GR, Fleming GR, Bassi R, Niyogi KK (2016) Identification of pH-sensing sites in the light harvesting complex stress-related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J Biol Chem 291(14):7334–7346. doi:10.1074/jbc.M115.704601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baltz A, Dang K-V, Beyly A, Auroy P, Richaud P, Cournac L, Peltier G (2014) Plastidial expression of type II NAD(P)H dehydrogenase increases the reducing state of plastoquinones and hydrogen photoproduction rate by the indirect pathway in Chlamydomonas reinhardtii1. Plant Physiol 165:1344–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Review structure–function of the cytochrome b 6 f complex. Photochem Photobiol 84:1349–1358

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci U S A 79:4352–4356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635

    Article  CAS  PubMed  Google Scholar 

  • Bergner SV, Scholz M, Trompelt K, Barth J, Gäbelein P, Steinbeck J, Xue H, Clowez S, Fucile G, Goldschmidt-Clermont M et al (2015) State transition7-dependent phosphorylation is modulated by changing environmental conditions and its absence triggers remodeling of photosynthetic protein complexes. Plant Physiol 168:615–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta Biomembr 1758:994–1003

    Article  CAS  Google Scholar 

  • Boehm M, Alahuhta M, Mulder DW, Peden EA, Long H, Brunecky R, Lunin VV, King PW, Ghirardi ML, Dubini A (2015) Crystal structure and biochemical characterization of Chlamydomonas FDX2 reveal two residues that, when mutated, partially confer FDX2 the redox potential and catalytic properties of FDX1. Photosynth Res 128:45–57

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008) The occurrence of the psbs gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370

    Article  CAS  PubMed  Google Scholar 

  • Breyton C, Nandha B, Johnson GN, Joliot P, Finazzi G (2006) Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45:13465–13475

    Article  CAS  PubMed  Google Scholar 

  • Busch A, Hippler M (2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807:864–877

    Article  CAS  PubMed  Google Scholar 

  • Cardol P, Bailleul B, Rappaport F, Derelle E, Béal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H et al (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci U S A 105:7881–7886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardol P, Alric J, Girard-Bascou J, Franck F, Wollman FA, Finazzi G (2009) Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc Natl Acad Sci U S A 106:15979–15984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Regul Electron Transp Chloroplasts 1807:912–918

    CAS  Google Scholar 

  • Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carraretto L, Formentin E, Teardo E, Checchetto V, Tomizioli M, Morosinotto T, Giacometti GM, Finazzi G, Szabó I (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants. Science 342:114–118

    Article  CAS  PubMed  Google Scholar 

  • Chaux F, Peltier G, Johnson X (2015) A security network in PSI photoprotection: regulation of photosynthetic control, NPQ and O2 photoreduction by cyclic electron flow. Front Plant Sci 6:1–7

    Article  Google Scholar 

  • Chen G, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    Article  CAS  Google Scholar 

  • Chen H, Hu J, Qiao Y, Chen W, Rong J, Zhang Y, He C, Wang Q (2015) Ca2+-regulated cyclic electron flow supplies ATP for nitrogen starvation-induced lipid biosynthesis in green alga. Sci Rep 5:15117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Zhang J, Zhao L, Xing J, Peng L, Kuang T, Rochaix J-D, Huang F (2016) Loss of algal proton gradient regulation 5 increases ROS scavenging an H2 evolution. J Integr Plant Biol:6772–6772

    Google Scholar 

  • Clark RD, Hawkesford MJ, Coughlan SJ, Bennett J, Hind G (1984) Association of ferredoxin-NADP+ oxidoreductase with the chloroplast cytochrome b-f complex. FEBS Lett 174:137–142

    Article  CAS  Google Scholar 

  • Clowez S, Godaux D, Cardol P, Wollman F-A, Rappaport F (2015) The involvement of hydrogen-producing and ATP-dependent NADPH consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia. J Biol Chem 290:8666–8676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa-Galvis V, Redekop P, Guan K, Grieß A, Truong TB, Wakao S, Niyogi KK, Jahns P (2016) Photosystem II subunit PsbS is involved in the induction of LHCSR-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem jbc.M116.737312

    Google Scholar 

  • DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285

    Article  CAS  PubMed  Google Scholar 

  • Dang K-V, Plet J, Tolleter D, Jokel M, Cuiné S, Carrier P, Auroy P, Richaud P, Johnson X, Alric J et al (2014) Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 26:1–16

    Article  CAS  Google Scholar 

  • Davis GA, Kanazawa A, Schöttler MA, Kohzuma K, Froehlich JE, Rutherford AW, Satoh-Cruz M, Minhas D, Tietz S, Dhingra A et al (2016) Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. elife 5:1–27

    Google Scholar 

  • Dayer R, Fischer BB, Eggen RIL, Lemaire SD (2008) The peroxiredoxin and glutathione peroxidase families in Chlamydomonas reinhardtii. Genetics 179:41–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delosme R, Olive J, Wollman F-A (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 Bioenerg 1273:150–158

    Article  Google Scholar 

  • Depège N, Bellafiore S, Rochaix J-D (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Desplats C, Mus F, Cuiné S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in chlamydomonas chloroplasts. J Biol Chem 284:4148–4157

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz K-J (2016) Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cells 39:20–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz K-J, Stork T, Finkemeier I, Lamkemeyer P, Li W-X, El-Tayeb MA, Michel K-P, Pistorius E, Baier M (2006) Photoprotection, photoinhibition, gene regulation, and environment. In: Demmig-Adams B, Adams WW, Mattoo AK (eds) Advances in photosynthesis and respiration. Springer Netherlands, Dordrecht, pp 303–319

    Google Scholar 

  • Drop B, Webber-Birungi M, Fusetti F, Kourǐl R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286:44878–44887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drop B, Webber-Birungi M, Yadav SKN, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, Croce R (2014a) Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta 1837:63–72

    Article  CAS  PubMed  Google Scholar 

  • Drop B, Yadav SKN, Boekema EJ, Croce R (2014b) Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii. Plant J:181–191

    Google Scholar 

  • Duan Z, Kong F, Zhang L, Li W, Zhang J (2016) A bestrophin-like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis. J Integr Plant Biol:1–32

    Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  CAS  PubMed  Google Scholar 

  • Fan M, Li M, Liu Z, Cao P, Pan X, Zhang H, Zhao X, Zhang J, Chang W (2015) Crystal structures of the PsbS protein essential for photoprotection in plants. Nat Struct Mol Biol 22:729–735

    Article  CAS  PubMed  Google Scholar 

  • Feilke K, Streb P, Gabriel C, Perreau F, Kruk J, Krieger-Liszkay A (2015) Effect of Chamydomonas plastid terminal oxidase 1 expressed in tobacco on photosynthetic electron transfer. Plant J 85:219–228

    Article  CAS  Google Scholar 

  • Finazzi G, Rappaport F (1998) In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on cytochrome b6f turnover. Biochemistry 37:9999–10005

    Article  CAS  PubMed  Google Scholar 

  • Finazzi G, Sommer F, Hippler M (2005) Release of oxidized plastocyanin from photosystem I limits electron transfer between photosystem I and cytochrome b6f complex in vivo. Proc Natl Acad Sci 102(19):7031–7036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fink RC, Scandalios JG (2002) Molecular evolution and structure–function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399:19–36

    Article  CAS  PubMed  Google Scholar 

  • Fischer BB, Eggen RIL, Trebst A, Krieger-Liszkay A (2006) The glutathione peroxidase homologous gene Gpxh in Chlamydomonas reinhardtii is upregulated by singlet oxygen produced in photosystem II. Planta 223:583–590

    Article  CAS  PubMed  Google Scholar 

  • Fischer BB, Eggen RIL, Niyogi KK (2010) Characterization of singlet oxygen-accumulating mutants isolated in a screen for altered oxidative stress response in Chlamydomonas reinhardtii. BMC Plant Biol 10:279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D, Pellegrini M, Merchant SS, Koller A, Eggen RIL, Niyogi KK (2012) SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 109:E1302–E1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Halliwell B (1977) Purification and properties of dehydroascorbate reductase from spinach leaves. Phytochemistry 16:1347–1350

    Article  CAS  Google Scholar 

  • Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152:1219–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghysels B, Godaux D, Matagne RF, Cardol P, Franck F (2013) Function of the chloroplast hydrogenase in the microalga Chlamydomonas: the role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis. PLoS One. doi:10.1371/journal.pone.0064161

  • Godaux D, Bailleul B, Berne N, Cardol P (2015) Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and PGRL1-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol 168:00105.2015

    Article  CAS  Google Scholar 

  • Goldschmidt-Clermont M, Bassi R (2015) Sharing light between two photosystems: mechanism of state transitions. Curr Opin Plant Biol 25:71–78

    Article  CAS  PubMed  Google Scholar 

  • Goss T, Hanke GT (2014) The end of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons? Curr Protein Pept Sci 15:385–393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goyer A, Haslekås C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot JP, Decottignies P (2002) Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269:272–282

    Article  CAS  PubMed  Google Scholar 

  • Groden D, Beck E (1979) H2O2 destruction by ascorbate-dependent systems from chloroplasts. BBA-Bioenergetics 546:426–435

    Article  CAS  PubMed  Google Scholar 

  • Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz MC, Seibert M (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol 190:279–288

    Article  CAS  PubMed  Google Scholar 

  • Haehnel W, Jansen T, Gause K, Klösgen RB, Stahl B, Michl D, Huvermann B, Karas M, Herrmann RG (1994) Electron transfer from plastocyanin to photosystem I. EMBO J 13:1028–1038

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hald S, Nandha B, Gallois P, Johnson GN (2008) Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. Biochim Biophys Acta 1777:433–440

    Article  CAS  PubMed  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  CAS  PubMed  Google Scholar 

  • Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    Article  CAS  PubMed  Google Scholar 

  • Herdean A, Nziengui H, Zsiros O, Solymosi K, Garab G, Lundin B, Spetea C (2016a) The arabidopsis thylakoid chloride channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport. Front Plant Sci 7:1–15

    Article  Google Scholar 

  • Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON, Ünnep R, Nagy G, Zsiros O, Dana S, Solymosi K et al (2016b) A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun 7:11654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49:511–523

    Article  CAS  PubMed  Google Scholar 

  • Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, Krieger-Liszky A (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J Biol Chem 284:31174–31180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hippler M, Reichert J, Sutter M, Zak E, Altschmied L, Schröer U, Herrmann RG, Haehnel W (1996) The plastocyanin binding domain of photosystem I. EMBO J 15:6374–6384

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hippler M, Drepper F, Farah J, Rochaix J (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36:6343–6349

    Article  CAS  PubMed  Google Scholar 

  • Hippler M, Drepper F, Haehnel W, Rochaix J-D (1998) The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 95:7339–7344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochmal AK, Schulze S, Trompelt K, Hippler M (2015) Calcium-dependent regulation of photosynthesis. Biochim Biophys Acta 1847:993–1003

    Article  CAS  PubMed  Google Scholar 

  • Hochmal AK, Zinzius K, Charoenwattanasatien R, Gäbelein P, Mutoh R, Tanaka H, Schulze S, Liu G, Scholz M, Nordhues A et al (2016) Calredoxin represents a novel type of calcium-dependent sensor-responder connected to redox regulation in the chloroplast. Nat Commun. doi:10.1038/ncomms11847

  • Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Natl Acad Sci 108:20820–20825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010a) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Yokono M, Inada N, Minagawa J (2010b) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci U S A 107:2337–2342

    Article  CAS  PubMed  Google Scholar 

  • Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329

    Article  CAS  PubMed  Google Scholar 

  • Janero DR, Barrnett R (1982) Thylakoid membrane biogenesis in Chlamydomonas reinhardtii 137+. II. Cell-cycle variations in the synthesis and assembly of pigment. J Cell Biol 93:411–416

    Article  CAS  PubMed  Google Scholar 

  • Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW et al (2004) Two enzymes in one: two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117:625–635

    Article  CAS  PubMed  Google Scholar 

  • Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A 105:20546–20551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Järvi S, Suorsa M, Aro EM (2015) Photosystem II repair in plant chloroplasts – regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim Biophys Acta Bioenerg 1847:900–909

    Article  CAS  Google Scholar 

  • Johansson L, Gafvelin G, Arnér ESJ (2005) Selenocysteine in proteins – properties and biotechnological use. Biochim Biophys Acta - Gen Subj 1726:1–13

    Article  CAS  Google Scholar 

  • Johnson GN (2003) Thiol regulation of the thylakoid electron transport chain – a missing link in the regulation of photosynthesis? Biochemistry 42:3040–3044

    Article  CAS  PubMed  Google Scholar 

  • Johnson GN (2004) Controversy remains: regulation of pH gradient across the thylakoid membrane. Trends Plant Sci 9:570–571

    Article  CAS  PubMed  Google Scholar 

  • Johnson GN (2011) Reprint of: physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:906–911

    Article  CAS  PubMed  Google Scholar 

  • Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287:26445–26452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P, Ozawa S-I, Houille-Vernes L, Petroutsos D, Rappaport F, Grossman AR et al (2014) Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: a study of ΔATpase pgr5 and ΔrbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol 165:438–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jokel M, Kosourov S, Battchikova N, Tsygankov AA, Aro EM, Allahverdiyeva Y (2015) Chlamydomonas flavodiiron proteins facilitate acclimation to anoxia during sulfur deprivation. Plant Cell Physiol 56:1598–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368

    Article  CAS  PubMed  Google Scholar 

  • Josse EM, Alcaraz JP, Labouré AM, Kuntz M (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270:3787–3794

    Article  CAS  PubMed  Google Scholar 

  • Kaiser W (1976) The effect of hydrogen peroxide on CO2 fixation of isolated intact chloroplasts. BBA-Bioenergetics 440:476–482

    Article  CAS  PubMed  Google Scholar 

  • Kelly GJ, Latzko E (1979) Soluble ascorbate peroxidase: detection in plants and use in vitamim C estimation. Naturwissenschaften 66:617–619

    CAS  PubMed  Google Scholar 

  • Kim SY, Jang HH, Lee JR, Sung NR, Lee HB, Lee DH, Park DJ, Kang CH, Chung WS, Lim CO et al (2009) Oligomerization and chaperone activity of a plant 2-Cys peroxiredoxin in response to oxidative stress. Plant Sci 177:227–232

    Article  CAS  Google Scholar 

  • Kirchhoff H (2014) Diffusion of molecules and macromolecules in thylakoid membranes. Biochim Biophys Acta Bioenerg 1837:495–502

    Article  CAS  Google Scholar 

  • Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB, Ikeuchi M (2004) Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 45:290–299

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Avenson TJ, Edwards GE (2004a) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Avenson TJ, Edwards GE (2004b) Response to Johnson: Controversy remains: regulation of pH gradient across thylakoid membrane. Trends Plant Sci 9:571–572

    Article  CAS  Google Scholar 

  • Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of Photosystem II. Photosynth Res 37:117–130

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A, Feilke K (2016) The dual role of the plastid terminal oxidase PTOX: between a protective and a pro-oxidant function. Front Plant Sci 6:2015–2017

    Article  Google Scholar 

  • Kuhlgert S, Drepper F, Fufezan C, Sommer F, Hippler M (2012) Residues PsaB Asp612 and PsaB Glu613 of photosystem I confer pH-dependent binding of plastocyanin and cytochrome c(6). Biochemistry 51:7297–7303

    Article  CAS  PubMed  Google Scholar 

  • Kukuczka B, Magneschi L, Petroutsos D, Steinbeck J, Bald T, Powikrowska M, Fufezan C, Finazzi G, Hippler M (2014) Proton gradient regulation5-like1-mediated cyclic electron flow is crucial for acclimation to anoxia and complementary to nonphotochemical quenching in stress adaptation. Plant Physiol 165:1604–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunz HH, Gierth M, Herdean A, Satoh-Cruz M, Kramer DM, Spetea C, Schroeder JI (2014) Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc Natl Acad Sci USA 111:7480–7485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurisu G, Kusunoki M, Katoh E, Yamazaki T, Teshima K, Onda Y, Kimata-Ariga Y, Hase T (2001) Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP(+) reductase. Nat Struct Biol 8:117–121

    Article  CAS  PubMed  Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schöttler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A et al (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981

    Article  CAS  PubMed  Google Scholar 

  • Laureau C, De Paepe R, Latouche G, Moreno-Chacón M, Finazzi G, Kuntz M, Cornic G, Streb P (2013) Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant Cell Environ 36:1296–1310

    Article  CAS  PubMed  Google Scholar 

  • Ledford HK, Baroli I, Shin JW, Fischer BB, Eggen RIL, Niyogi KK (2004) Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii. Mol Gen Genomics 272:470–479

    Article  CAS  Google Scholar 

  • Ledford HK, Chin BL, Niyogi KK (2007) Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot Cell 6:919–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leisinger U, Rüfenacht K, Fischer B, Pesaro M, Spengler A, Zehnder AJ, Eggen RI (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol Biol 46:395–408

    Article  CAS  PubMed  Google Scholar 

  • Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, Rochaix J-D (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7:e45

    Article  PubMed  CAS  Google Scholar 

  • Lennon AM, Prommeenate P, Nixon PJ (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218:254–260

    Article  CAS  PubMed  Google Scholar 

  • Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  CAS  PubMed  Google Scholar 

  • Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874

    Article  CAS  PubMed  Google Scholar 

  • Liguori N, Roy LM, Opacic M, Durand G, Croce R, Roy LM (2013) Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: the C-terminus of LHCSR is the knob of a dimmer switch. J Am Chem Soc 135:18339–18342

    Article  CAS  PubMed  Google Scholar 

  • Lobanov AV, Fomenko DE, Zhang Y, Sengupta A, Hatfield DL, Gladyshev VN (2007) Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol 8:R198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lucker B, Kramer DM (2013) Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth Res. doi:10.1007/s11120-013-9932-0

  • Malnoë A, Wang F, Girard-Bascou J, Wollman FA, de Vitry C (2014) Thylakoid FtsH protease contributes to photosystem II and cytochrome b6f remodeling in Chlamydomonas reinhardtii under stress conditions. Plant Cell 26:373–390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maruyama S, Tokutsu R, Minagawa J (2014) Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii. Plant Cell Physiol 55:1304–1310

    Article  CAS  PubMed  Google Scholar 

  • Mehler AH (1951) Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. Arch Biochem Biophys 34:339–351

    Article  CAS  PubMed  Google Scholar 

  • Meyer Zu Tittingdorf JMW, Rexroth S, Schäfer E, Schlichting R, Giersch C, Dencher NA, Seelert H (2004) The stoichiometry of the chloroplast ATP synthase oligomer III in Chlamydomonas reinhardtii is not affected by the metabolic state. Biochim Biophys Acta Bioenerg 1659:92–99

    Article  CAS  Google Scholar 

  • Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191(4784):144–148

    Article  CAS  PubMed  Google Scholar 

  • Moore AL, Shiba T, Young L, Harada S, Kita K, Ito K (2013) Unraveling the heater: new insights into the structure of the alternative oxidase. Annu Rev Plant Biol 64:637–663

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    Article  CAS  PubMed  Google Scholar 

  • Munekage YN, Genty B, Peltier G (2008) Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol 49(11):1688–1698

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  CAS  PubMed  Google Scholar 

  • Muranaka LS, Rütgers M, Bujaldon S, Heublein A, Geimer S, Wollman FA, Schroda M (2016) TEF30 interacts with photosystem II monomers and is involved in the repair of photodamaged photosystem II in Chlamydomonas reinhardtii. Plant Physiol 170:821–840

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y (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 Bioenerg 1817:1127–1133

    Article  CAS  Google Scholar 

  • Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H(2) photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708:322–332

    Article  CAS  PubMed  Google Scholar 

  • Nagy G, Unnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G et al (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proc Natl Acad Sci U S A 111:5042–5047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nandha B, Finazzi G, Joliot P, Hald S, Johnson GN (2007) The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim Biophys Acta Bioenerg 1767:1252–1259

    Article  CAS  Google Scholar 

  • Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman F-A (2014) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu Rev Plant Biol 66:150112150216002

    Google Scholar 

  • Nawrocki WJ, Santabarbara S, Mosebach L, Wollman FA, Rappaport F (2016) State transitions redistribute rather than dissipate energy between the two photosystems in Chlamydomonas. Nat Plants 2:16031

    Article  CAS  PubMed  Google Scholar 

  • Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982

    Article  CAS  PubMed  Google Scholar 

  • Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565

    Article  CAS  PubMed  Google Scholar 

  • Nordling M, Sigfridsson K, Young S, Lundberg LG, Hansson Ö (1991) Flash-photolysis studies of the electron transfer from genetically modified spinach plastocyanin to photosystem I. FEBS Lett 291:327–330

    Article  CAS  PubMed  Google Scholar 

  • Ogawa K, Kanematsu S, Takabe K, Asada K (1995) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immuno-gold labeling after rapid freezing and substitution method. Plant Cell Physiol 36:565–573

    CAS  Google Scholar 

  • Page MD, Allen MD, Kropat J, Urzica EI, Karpowicz SJ, Hsieh SI, Loo JA, Merchant SS (2012) Fe sparing and Fe recycling contribute to increased superoxide dismutase capacity in iron-starved Chlamydomonas reinhardtii. Plant Cell 24:2649–2665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peden EA, Boehm M, Mulder DW, Davis R, Old WM, King PW, Ghirardi ML, Dubini A (2013) Identification of global ferredoxin interaction networks in chlamydomonas reinhardtii. J Biol Chem 288:35192–35209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521

    Article  CAS  PubMed  Google Scholar 

  • Peltier J-B (2005) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133

    Article  PubMed  CAS  Google Scholar 

  • Peltier G, Ravenel J, Verméglio A (1987) Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: evidence for a chlororespiration. BBA-Bioenergetics 893:83–90

    Article  CAS  Google Scholar 

  • Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106:19–31

    Article  CAS  PubMed  Google Scholar 

  • Peltier G, Aro EM, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu Rev Plant Biol 67:6.1–6.26

    Article  CAS  Google Scholar 

  • Peng L, Shimizu H, Shikanai T (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J Biol Chem 283:34873–34879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersson UA, Kieselbach T, García-Cerdán JG, Schröder WP (2006) The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. FEBS Lett 580:6055–6061

    Article  CAS  PubMed  Google Scholar 

  • Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284:32770–32781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petroutsos D, Busch A, Janssen I, Trompelt K, Bergner SV, Weinl S, Holtkamp M, Karst U, Kudla J, Hippler M (2011) The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23:2950–2963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P et al (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537:563–566

    Article  CAS  PubMed  Google Scholar 

  • Pitsch NT, Witsch B, Baier M (2010) Comparison of the chloroplast peroxidase system in the chlorophyte Chlamydomonas reinhardtii, the bryophyte Physcomitrella patens, the lycophyte Selaginella moellendorffii and the seed plant Arabidopsis thaliana. BMC Plant Biol 10:133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Priya B, Premanandh J, Dhanalakshmi RT, Seethalakshmi T, Uma L, Prabaharan D, Subramanian G (2007) Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics 8:435

    Article  PubMed  PubMed Central  Google Scholar 

  • Raven EL, Lad L, Sharp KH, Mewies M, Moody PC (2004) Defining substrate specificity and catalytic mechanism in ascorbate peroxidase. Biochem Soc Symp 38:27–38

    Article  Google Scholar 

  • Rochaix J-D (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309

    Article  CAS  PubMed  Google Scholar 

  • Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR et al (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142:574–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM, Schöttler M a (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23:304–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616

    Article  CAS  PubMed  Google Scholar 

  • Sandmann G (2009) Evolution of carotene desaturation: the complication of a simple pathway. Arch Biochem Biophys 483:169–174

    Article  CAS  PubMed  Google Scholar 

  • Saroussi SI, Wittkopp TM, Grossman AR (2016) The type II NADPH dehydrogenase facilitates cyclic electron flow, energy dependent quenching and chlororespiratory metabolism during acclimation of Chlamydomonas reinhardtii to nitrogen deprivation. Plant Physiol pp 02014(2015)

    Google Scholar 

  • Shikanai T, Yamamoto H (2016) Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. Mol Plant. doi:10.1016/j.molp.2016.08.004

  • Singh SK, Hasan SS, Zakharov SD, Naurin S, Whitelegge JP, Cramer WA, Lafayette W, Pasarow T, Spectrometry M, Angeles L et al (2016) Trans-membrane signaling in photosynthetic state transitions: redox- and structure-dependent interaction in vitro between Stt7 kinase and cytochrome b6f complex. J Biol Chem. doi:10.1074/jbc.M116.732545

  • Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. Philos Trans R Soc Lond Ser B Biol Sci 355:1455–1464

    Article  CAS  Google Scholar 

  • Sommer F, Drepper F, Hippler M (2002) The luminal helix l of PsaB is essential for recognition of plastocyanin or cytochrome c6 and fast electron transfer to photosystem I in Chlamydomonas reinhardtii. J Biol Chem 277:6573–6581

    Article  CAS  PubMed  Google Scholar 

  • Sommer F, Drepper F, Haehnel W, Hippler M (2004) The hydrophobic recognition site formed by residues PsaA-Trp651 and PsaB-Trp627 of photosystem I in Chlamydomonas reinhardtii confers distinct selectivity for binding of plastocyanin and cytochrome c 6. J Biol Chem 279:20009–20017

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  CAS  PubMed  Google Scholar 

  • Steinbeck J, Nikolova D, Weingarten R, Johnson X, Richaud P, Peltier G, Hermann M, Magneschi L, Hippler M (2015) Deletion of Proton Gradient Regulation 5 (PGR5) and PGR5-Like 1 (PGRL1) proteins promote sustainable light-driven hydrogen production in Chlamydomonas reinhardtii due to increased PSII activity under sulfur deprivation. Front Plant Sci 6:1–11

    Article  Google Scholar 

  • Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stiehl HH, Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Zeitschrift fur Naturforsch – Sect B J Chem Sci 24:1588–1598

    CAS  Google Scholar 

  • Stroebel D, Choquet Y, Popot J-L, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S et al (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Clowez S, Wollman F-A, Vallon O, Rappaport F (2013) Cyclic electron flow is redox-controlled but independent of state transition. Nat Commun 4:1954

    PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Okamuro A, Minagawa J, Takahashi Y (2014) Biochemical characterization of photosystem I-associated light-harvesting complexes I and II isolated from state 2 cells of chlamydomonas reinhardtii. Plant Cell Physiol 55:1437–1449

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Schmollinger S, Lee J-H, Schroda M, Rappaport F, Wollman F-A, Vallon O (2016) The PETO protein interacts with other effectors of cyclic electron flow in Chlamydomonas. Mol Plant. doi:10.1016/j.molp.2015.12.017

  • Takeda T, Ishikawa T, Shigeoka S (1997) Metabolism of hydrogen peroxide by the scavenging system in Chlamydomonas reinhardtii. Physiol Plant 99:49–55

    Article  CAS  Google Scholar 

  • Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9:1514–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57:151–168

    Article  CAS  PubMed  Google Scholar 

  • Terashima M, Petroutsos D, Hüdig M, Tolstygina I, Trompelt K, Gäbelein P, Fufezan C, Kudla J, Weinl S, Finazzi G et al (2012) Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc Natl Acad Sci U S A 109:17717–17722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terauchi AM, Lu S-F, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T et al (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284:25867–25878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tibiletti T, Auroy P, Peltier G, Caffarri S (2016) Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol pp. 00572(2016)

    Google Scholar 

  • Tikkanen M, Rantala S, Aro E-M (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6

    Google Scholar 

  • Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 110:10016–10021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, Krawietz D, Happe T, Auroy P, Adriano J-M, Beyly A et al (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–2630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trouillard M, Shahbazi M, Moyet L, Rappaport F, Joliot P, Kuntz M, Finazzi G (2012) Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim Biophys Acta Bioenerg 1817:2140–2148

    Article  CAS  Google Scholar 

  • Ünlü C, Drop B, Croce R, van Amerongen H (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc Natl Acad Sci U S A 111:3460–3465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ünlü C, Polukhina I, Van Amerongen H (2015) Origin of pronounced differences in 77 K fluorescence of the green alga Chlamydomonas reinhardtii in state 1 and 2. Eur Biophys J. doi:10.1007/s00249-015-1087-9

  • Urzica EI, Adler LN, Page MD, Linster CL, Arbing MA, Casero D, Pellegrini M, Merchant SS, Clarke SG (2012) Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDP-L-galactose phosphorylase. J Biol Chem 287:14234–14245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol 112:1703–1714

    Article  PubMed  PubMed Central  Google Scholar 

  • Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87

    Article  CAS  PubMed  Google Scholar 

  • Vinyard DJ, Ananyev GM, Dismukes CG (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606

    Article  CAS  PubMed  Google Scholar 

  • Wagner V, Ullmann K, Mollwo A, Kaminski M, Mittag M, Kreimer G (2007) The phosphoproteome of a Chlamydomonas reinhardtii eyespot fraction includes key proteins of the light signaling pathway. Plant Physiol 146:772–788

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Yamamoto H, Shikanai T (2015) Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim Biophys Acta Bioenerg 1847(9):931–938

    Article  CAS  Google Scholar 

  • Wang L, Yamano T, Takane S, Niikawa Y, Toyokawa C, Ozawa S, Tokutsu R, Takahashi Y, Minagawa J, Kanesaki Y et al (2016) Chloroplast-mediated regulation of CO2-concentrating mechanism by Ca2+-binding protein CAS in the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci 113:201606519

    Google Scholar 

  • Wei L, Derrien B, Gautier A, Houille-Vernes L, Boulouis A, Saint-Marcoux D, Malnoë A, Rappaport F, de Vitry C, Vallon O et al (2014) Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26:353–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whatley FR, Tagawa K, Arnon DI (1962) Separation of the light and dark reactions in electron transfer during photosynthesis. Biochemistry 49:266–270

    Google Scholar 

  • Wobbe L, Bassi R, Kruse O (2015) Multi-level light capture control in plants and green algae. Trends Plant Sci xx:1–14

    Google Scholar 

  • Wu D, Wright DA, Wetzel C, Voytas DF, Rodermel S (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11:43–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue H, Tokutsu R, Bergner SV, Scholz M, Minagawa J, Hippler M (2014) PSBR is required for efficient binding of LHCSR3 to photosystem II – light-harvesting supercomplexes in Chlamydomonas reinhardtii. Plant Physiol 167:1566–1578

    Article  CAS  Google Scholar 

  • Yadav KNS, Semchonok DA, Nosek L, Kouřil R, Fucile G, Boekema EJ, Eichacker LA (2017) Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH. Biochim Biophys Acta Bioenerg 1858:12–20

    Article  CAS  Google Scholar 

  • Yamamoto H, Peng L, Fukao Y, Shikanai T (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 23:1480–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Catalanotti C, Wittkopp TM, Posewitz MC, Grossman AR (2015a) Algae after dark: mechanisms to cope with anoxic/hypoxic conditions. Plant J 82:481–503

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Wittkopp TM, Li X, Warakanont J, Dubini A, Catalanotti C, Kim RG, Nowack ECM, Mackinder LCM, Aksoy M et al (2015b) Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. Proc Natl Acad Sci U S A 112:14978–14983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Feilke K, Krieger-Liszkay A, Beyer P (2014) Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim Biophys Acta Bioenerg 1837:1284–1292

    Article  CAS  Google Scholar 

  • Zhang H, Whitelegge JP, Cramer WA (2001) Ferredoxin:NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J Biol Chem 276:38159–38165

    CAS  PubMed  Google Scholar 

  • Zhang Z, Shrager J, Jain M, Vallon O, Grossman AR, Chang C (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman F a (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The research of MH is funded by the Deutsche Forschungsgemeinschaft (Grant no. HI 739/13-1).

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Correspondence to Michael Hippler .

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Gäbelein, P., Mosebach, L., Hippler, M. (2017). Bioenergetic Pathways in the Chloroplast: Photosynthetic Electron Transfer. In: Hippler, M. (eds) Chlamydomonas: Molecular Genetics and Physiology. Microbiology Monographs, vol 30. Springer, Cham. https://doi.org/10.1007/978-3-319-66365-4_4

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