Biophysics; Cyclic electron flow; Cytochrome b(6)f; Photosynthesis; Photosystem I; Plastoquinone
Abstract :
[en] Apart from the canonical light-driven linear electron flow (LEF) from water to CO2, numerous regulatory and alternative electron transfer pathways exist in chloroplasts. One of them is the cyclic electron flow around Photosystem I (CEF), contributing to photoprotection of both Photosystem I and II (PSI, PSII) and supplying extra ATP to fix atmospheric carbon. Nonetheless, CEF remains an enigma in the field of functional photosynthesis as we lack understanding of its pathway. Here, we address the discrepancies between functional and genetic/biochemical data in the literature and formulate novel hypotheses about the pathway and regulation of CEF based on recent structural and kinetic information.
Nawrocki, Wojciech J.; Institut de Biologie Physico-Chimique (Paris)
Bailleul, Benjamin; Institut de Biologie Physico-Chimique (Paris)
Picot, Daniel; Institut de Biologie Physico-Chimique (Paris)
Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Rappaport, Fabrice; Institut de Biologie Physico-Chimique (Paris)
Wollman, Françis Andrè; Institut de Biologie Physico-Chimique (Paris)
Joliot, Pierre A.; Institut de Biologie Physico-Chimique (Paris)
Language :
English
Title :
The mechanism of cyclic electron flow.
Publication date :
2019
Journal title :
Biochimica et Biophysica Acta. Bioenergetics
ISSN :
0005-2728
eISSN :
1879-2650
Publisher :
Elsevier, Netherlands
Volume :
1860
Issue :
5
Pages :
433-438
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
H2020 - 682580 - BEAL - Bioenergetics in microalgae : regulation modes of mitochondrial respiration, photosynthesis, and fermentative pathways, and their interactions in secondary algae
Funders :
CE - Commission Européenne
Commentary :
Copyright (c) 2018 Elsevier B.V. All rights reserved.
Nawrocki, W., Bailleul, B., Cardol, P., Rappaport, F., Wollman, F.-A., Joliot, P., Cyclic Electron Flow in Chlamydomonas reinhardtii. 2017, bioRxiv.
Tagawa, K., Tsujimoto, H.Y., Arnon, D.I., Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 49 (1963), 567–572.
Cleland, R.E., Bendall, D.S., Photosystem I cyclic electron transport: measurement of ferredoxin-plastoquinone reductase activity. Photosynth. Res. 34 (1992), 409–418.
Yamori, W., Shikanai, T., Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu. Rev. Plant Biol. 67 (2016), 81–106.
Yamamoto, H., Peng, L., Fukao, Y., Shikanai, T., 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 (2011), 1480–1493.
Nawrocki, W.J., Tourasse, N.J., Taly, A., Rappaport, F., Wollman, F.A., The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu. Rev. Plant Biol. 66 (2015), 49–74.
Iwata, M., Lee, Y., Yamashita, T., Yagi, T., Iwata, S., Cameron, A.D., Maher, M.J., The structure of the yeast NADH dehydrogenase (Ndi1) reveals overlapping binding sites for water- and lipid-soluble substrates. Proc. Natl. Acad. Sci. 109 (2012), 15247–15252.
Blobel, G., Intracellular protein topogenesis. Proc. Natl. Acad. Sci. 77 (1980), 1496–1500.
Jans, F., Mignolet, E., Houyoux, P.A., Cardol, P., Ghysels, B., Cuine, S., Cournac, L., Peltier, G., Remacle, C., Franck, F., 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 (2008), 20546–20551.
Joliot, P., Beal, D., Joliot, A., Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim. Biophys. Acta 1656 (2004), 166–176.
Joliot, P., Johnson, G.N., Regulation of cyclic and linear electron flow in higher plants. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 13317–13322.
Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P., Nixon, P.J., Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J., 17, 1998, 868.
Trouillard, M., Shahbazi, M., Moyet, L., Rappaport, F., Joliot, P., Kuntz, M., Finazzi, G., Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim. Biophys. Acta 1817 (2012), 2140–2148.
Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K., Yokota, A., Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 9705–9709.
Mignolet, E., Lecler, R., Ghysels, B., Remacle, C., Franck, F., Function of the chloroplastic NAD(P)H dehydrogenase Nda2 for H(2) photoproduction in sulphur-deprived Chlamydomonas reinhardtii. J. Biotechnol. 162 (2012), 81–88.
Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.-I., Endo, T., Tasaka, M., Shikanai, T., Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 2004, 579.
Dalcorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schünemann, D., Finazzi, G., Joliot, P., Barbato, R., Leister, D., A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132 (2008), 273–285.
Nandha, B., Finazzi, G., Joliot, P., Hald, S., Johnson, G.N., The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim. Biophys. Acta 1767 (2007), 1252–1259.
Godaux, D., Bailleul, B., Berne, N., Cardol, P., Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-like1-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol. 168 (2015), 648–658.
Alric, J., 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 (2014), 825–834.
Johnson, X., Steinbeck, J., Dent, R.M., Takahashi, H., Richaud, P., Ozawa, S.I., Houille-Vernes, L., Petroutsos, D., Rappaport, F., Grossman, A.R., Niyogi, K.K., Hippler, M., Alric, J., Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: a study of delta ATPase pgr5 and delta rbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol. 165 (2014), 438–452.
Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., Shikanai, T., PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110 (2002), 361–371.
Toshiharu, S., Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58 (2007), 199–217.
Hertle, A.P., Blunder, T., Wunder, T., Pesaresi, P., Pribil, M., Armbruster, U., Leister, D., PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell 49 (2013), 511–523.
Albertsson, P.-Å., A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6 (2001), 349–354.
Dalcorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schunemann, D., Finazzi, G., Joliot, P., Barbato, R., Leister, D., A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132 (2008), 273–285.
Mitchell, P., The protonmotive Q cycle: a general formulation. FEBS Lett. 59 (1975), 137–139.
Lavergne, J., Membrane potential-dependent reduction of cytochrome b-6 in an algal mutant lacking Photosystem I centers. Biochim. Biophys. Acta Bioenerg. 725 (1983), 25–33.
Stroebel, D., Choquet, Y., Popot, J.L., Picot, D., An atypical haem in the cytochrome b(6)f complex. Nature 426 (2003), 413–418.
Kurisu, G., Zhang, H., Smith, J.L., Cramer, W.A., Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science, 302, 2003, 1009.
Cramer, W.A., Hasan, S.S., Yamashita, E., The Q cycle of cytochrome bc complexes: a structure perspective. Biochim. Biophys. Acta Bioenerg. 1807 (2011), 788–802.
Crofts, A.R., The Q-cycle – a personal perspective. Photosynth. Res. 80 (2004), 223–243.
Baniulis, D., Yamashita, E., Zhang, H., Hasan, S.S., Cramer, W.A., Structure–function of the cytochrome b 6 f complex. Photochem. Photobiol. 84 (2008), 1349–1358.
Page, C.C., Moser, C.C., Chen, X., Dutton, P.L., Natural engineering principles of electron tunnelling in biological oxidation–reduction. Nature, 402, 1999, 47.
Zhang, H.M., Whitelegge, J.P., Cramer, W.A., Ferredoxin: NADP(+) oxidoreductase is a subunit of the chloroplast cytochrome b(6)f complex. J. Biol. Chem. 276 (2001), 38159–38165.
Mosebach, L., Heilmann, C., Mutoh, R., Gäbelein, P., Steinbeck, J., Happe, T., Ikegami, T., Hanke, G., Kurisu, G., Hippler, M., Association of Ferredoxin:NADP+ oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii. Photosynth. Res. 134 (2017), 291–306.
Correll, C.C., Ludwig, M.L., Bruns, C.M., Karplus, P.A., Structural prototypes for an extended family of flavoprotein reductases: comparison of phthalate dioxygenase reductase with ferredoxin reductase and ferredoxin. Protein Sci. 2 (1993), 2112–2133.
Alric, J., Pierre, Y., Picot, D., Lavergne, J., Rappaport, F., Spectral and redox characterization of the heme ci of the cytochrome b 6 f complex. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 15860–15865.
Hald, S., Nandha, B., Gallois, P., Johnson, G.N., Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. Biochim. Biophys. Acta 1777 (2008), 433–440.
Joliot, P., Joliot, A., The low-potential electron-transfer chain in the cytochrome bf complex. Biochim. Biophys. Acta Bioenerg. 933 (1988), 319–333.
Takahashi, H., Schmollinger, S., Lee, J.-H., Schroda, M., Rappaport, F., Wollman, F.-A., Vallon, O., PETO interacts with other effectors of cyclic electron flow in Chlamydomonas. Mol. Plant 9 (2016), 558–568.
Buchert, F., Hamon, M., Gäbelein, P., Scholz, M., Hippler, M., Wollman, F.-A., The labile interactions of cyclic electron flow effector proteins. J. Biol. Chem. 293 (2018), 17559–17573.
Terashima, M., Petroutsos, D., Hudig, M., Tolstygina, I., Trompelt, K., Gabelein, P., Fufezan, C., Kudla, J., Weinl, S., Finazzi, G., Hippler, M., Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 17717–17722.
Cramer, W.A., Zhang, H., Yan, J., Kurisu, G., Smith, J.L., Transmembrane traffic in the cytochrome b 6 f complex. Annu. Rev. Biochem. 75 (2006), 769–790.
Swierczek, M., Cieluch, E., Sarewicz, M., Borek, A., Moser, C.C., Dutton, P.L., Osyczka, A., An electronic bus bar lies in the core of cytochrome bc1. Science 329 (2010), 451–454.
Lanciano, P., Lee, D.W., Yang, H., Darrouzet, E., Daldal, F., Intermonomer electron transfer between the low-potential b hemes of cytochrome bc(1). Biochemistry 50 (2011), 1651–1663.
Hasan, S.S., Proctor, Elizabeth A., Yamashita, E., Dokholyan, Nikolay V., Cramer, William A., Traffic within the cytochrome b 6 f lipoprotein complex: gating of the quinone portal. Biophys. J. 107 (2014), 1620–1628.
Joliot, P., Joliot, A., Mechanism of proton-pumping in the cytochrome b/f complex. Photosynth. Res. 9 (1986), 113–124.
Moser, C.C., Keske, J.M., Warncke, K., Farid, R.S., Dutton, P.L., Nature of biological electron transfer. Nature, 355, 1992, 796.
Hong, S., Victoria, D., Crofts, A.R., Inter-monomer electron transfer is too slow to compete with monomeric turnover in bc1 complex. Biochim. Biophys. Acta Bioenerg. 1817 (2012), 1053–1062.
Van Eerden, F.J., Melo, M.N., Frederix, P.W.J.M., Periole, X., Marrink, S.J., Exchange pathways of plastoquinone and plastoquinol in the photosystem II complex. Nat. Commun., 8, 2017, 15214.
Allen, J.F., Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8 (2003), 15–19.
Alric, J., The plastoquinone pool, poised for cyclic electron flow?. Front. Plant Sci., 6, 2015, 540.
Joliot, P., Joliot, A., Cyclic electron transfer in plant leaf. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 10209–10214.
Ilik, P., Pavlovic, A., Kouril, R., Alboresi, A., Morosinotto, T., Allahverdiyeva, Y., Aro, E.M., Yamamoto, H., Shikanai, T., Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol. 214 (2017), 967–972.
Gerotto, C., Alboresi, A., Meneghesso, A., Jokel, M., Suorsa, M., Aro, E.M., Morosinotto, T., Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 12322–12327.
Dumas, L., Zito, F., Blangy, S., Auroy, P., Johnson, X., Peltier, G., Alric, J., A stromal region of cytochrome b 6 f subunit IV is involved in the activation of the Stt7 kinase in Chlamydomonas. Proc. Natl. Acad. Sci. 114 (2017), 12063–12068.
Schonberg, A., Rodiger, A., Mehwald, W., Galonska, J., Christ, G., Helm, S., Thieme, D., Majovsky, P., Hoehenwarter, W., Baginsky, S., Identification of STN7/STN8 kinase targets reveals connections between electron transport, metabolism and gene expression. Plant J. 90 (2017), 1176–1186, 10.1111/tpj.13536.
Hanke, G.U.Y., Mulo, P., Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ. 36 (2013), 1071–1084.
Mulo, P., Chloroplast-targeted ferredoxin-NADP+ oxidoreductase (FNR): structure, function and location. Biochim. Biophys. Acta Bioenerg. 1807 (2011), 927–934.
Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., Minagawa, J., Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464 (2010), 1210–U1134.
Yadav, K.N.S., Semchonok, D.A., Nosek, L., Kouril, R., Fucile, G., Boekema, E.J., Eichacker, L.A., Supercomplexes of plant photosystem I with cytochrome b 6 f, light-harvesting complex II and NDH. BBA-Bioenergetics 1858 (2017), 12–20.
Takahashi, H., Clowez, S., Wollman, F.A., Vallon, O., Rappaport, F., Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun., 4, 2013, 1954.
Johnson, X., Steinbeck, J., Dent, R.M., Takahashi, H., Richaud, P., Ozawa, S., Houille-Vernes, L., Petroutsos, D., Rappaport, F., Grossman, A.R., Niyogi, K.K., Hippler, M., Alric, J., Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: a study of DeltaATpase pgr5 and DeltarbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol. 165 (2014), 438–452.
Anderson, J.M., Cytochrome b 6 f complex: dynamic molecular organization, function and acclimation. Photosynth. Res. 34 (1992), 341–357.
Vallon, O., Bulte, L., Dainese, P., Olive, J., Bassi, R., Wollman, F.A., Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc. Natl. Acad. Sci. 88 (1991), 8262–8266.
Drop, B., Yadav, K.N.S., Boekema, E.J., Croce, R., Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii. Plant J. 78 (2014), 181–191.
Steinbeck, J., Ross, I.L., Rothnagel, R., Gäbelein, P., Schulze, S., Giles, N., Ali, R., Drysdale, R., Sierecki, E., Gambin, Y., Stahlberg, H., Takahashi, Y., Hippler, M., Hankamer, B., Structure of a PSI–LHCI–cyt b 6 f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proc. Natl. Acad. Sci. 115 (2018), 10517–10522.
Genova, M.L., Lenaz, G., Functional role of mitochondrial respiratory supercomplexes. BBA-Bioenergetics 1837 (2014), 427–443.
Letts, J.A., Fiedorczuk, K., Sazanov, L.A., The architecture of respiratory supercomplexes. Nature, 537, 2016, 644.
Trouillard, M., Meunier, B., Rappaport, F., Questioning the functional relevance of mitochondrial supercomplexes by time-resolved analysis of the respiratory chain. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), E1027–E1034.
Drop, B., Yadav, K.N.S., Boekema, E.J., Croce, R., Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J. 78 (2014), 181–191.
Kouril, R., Strouhal, O., Nosek, L., Lenobel, R., Chamrad, I., Boekema, E.J., Sebela, M., Ilik, P., Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J. 77 (2014), 568–576.
Peng, L., Fukao, Y., Fujiwara, M., Takami, T., Shikanai, T., Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21 (2009), 3623–3640.
