Skip to main content
Log in

Induction events and short-term regulation of electron transport in chloroplasts: an overview

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Regulation of photosynthetic electron transport at different levels of structural and functional organization of photosynthetic apparatus provides efficient performance of oxygenic photosynthesis in plants. This review begins with a brief overview of the chloroplast electron transport chain. Then two noninvasive biophysical methods (measurements of slow induction of chlorophyll a fluorescence and EPR signals of oxidized P700 centers) are exemplified to illustrate the possibility of monitoring induction events in chloroplasts in vivo and in situ. Induction events in chloroplasts are considered and briefly discussed in the context of short-term mechanisms of the following regulatory processes: (i) pH-dependent control of the intersystem electron transport; (ii) the light-induced activation of the Calvin–Benson cycle; (iii) optimization of electron transport due to fitting alternative pathways of electron flow and partitioning light energy between photosystems I and II; and (iv) the light-induced remodeling of photosynthetic apparatus and thylakoid membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19
Fig. 20

Similar content being viewed by others

Notes

  1. Here and below, the term “memory” is used colloquially to characterize the rate of post-illumination relaxation of NPQ: a slow decay of NPQ corresponds to long “memory” of photosynthetic apparatus about plant illumination.

Abbreviations

b 6 f :

Cytochrome b 6 f complex

CBC:

Calvin–Benson cycle

Chl:

Chlorophyll

CEF1:

Cyclic electron flow around photosystem I

EPR:

Electron paramagnetic resonance

ETC:

Electron transport chain

ISP:

Iron-sulfur protein

Fd:

Ferredoxin

FNR:

Ferredoxin-NADP-oxidoreductase

FQR:

Ferredoxin-quinone-reductase

FRL:

Far-red light

HL:

High light

LEF:

Linear electron flow

LHCI:

Light-harvesting complex I

LHCII:

Light-harvesting complex II

LL:

Low light

MV:

Methylviologen

NDH:

NAD(P)H dehydrogenase complex

NPQ:

Non-photochemical quenching

PAM:

Pulse-amplitude modulation

pmf :

Proton motive force

PSI:

Photosystem I

PSII:

Photosystem II

PTOX:

Plastoquinol terminal oxidase

P700 :

Reduced form of electron donor of PSI

\( {\text{P}}_{700}^{ + } \) :

Oxidized form of electron donor of PSI

Pc:

Plastocyanin

PQ:

Plastoquinone

PQH2 :

Plastoquinol

ROS:

Reactive oxygen species

SIF:

Slow induction of fluorescence

Tr:

Thioredoxin

TrR:

Thioredoxin reductase

VDE:

Violaxanthin de-epoxidase

Vx:

Violaxanthin

WL:

White light

WOC:

Water-oxidizing complex

WWC:

Water–water cycle

Zx:

Zeaxanthin

ΔpH:

Transthylakoid pH difference

References

  • Adams WW III, Barker DH (1998) Seasonal changes in xanthophylls cycle-dependent energy dissipation in Yucca glauca Nuttall. Plant, Cell Environ 21:501–512

    CAS  Google Scholar 

  • Adams III WW, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC, Govindjee (eds), Chlorophyll a fluorescence. A signature of photosynthesis, vol 19. Springer, Dordrecht, pp 583–604

  • Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276

    CAS  Google Scholar 

  • Albertsson P-A (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6:349–354

    CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Murata N (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 1657:23–32

    CAS  PubMed  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    CAS  PubMed  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Alric J, Pierre Y, Picot D, Lavergne J, Rappaport F (2005) Spectral and redox characterization of the heme c i of the cytochrome b 6 f complex. Proc Natl Acad Sci USA 102:15860–15865

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63

    CAS  PubMed  Google Scholar 

  • Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568

    CAS  PubMed  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (eds), Chlorophyll a fluorescence. A signature of photosynthesis, vol 19. Springer, Dordrecht, pp 65–82

  • Bakker-Grunwald T, van Dam K (1974) On the mechanism of activation of the ATPase in chloroplasts. Biochim Biophys Acta 347:290–298

    CAS  PubMed  Google Scholar 

  • Bald D, Noji H, Yoshida M, Hirono-Hara Y, Hisabori T (2001) Redox regulation of the rotation of F1-ATP synthase. J Biol Chem 276:39505–39507

    CAS  PubMed  Google Scholar 

  • Barber J (1976) Ionic regulation in intact chloroplasts and its effects on primary photosynthetic processes. In: Barber J (ed) The intact chloroplasts, vol 1. Topics in photosynthesis. Elsevier, Amsterdam, pp 88–134

  • Barber J (1979) A mechanism of controlling the stacking and unstacking of chloroplast thylakoid membranes. FEBS Lett 105:5–10

    CAS  Google Scholar 

  • Barber J (2008) Crystal structure of the oxygen-evolving complex of photosystem II. Inorg Chem 47:1700–1710

    CAS  PubMed  Google Scholar 

  • Battchikova N, Eisenhut M, Aro E-M (2011) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944

    CAS  PubMed  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    CAS  PubMed  Google Scholar 

  • Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229:23–38

    Google Scholar 

  • Benz JP, Lintala M, Soll J, Mulo P, Bölter B (2010) A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids. Trends Plant Sci 15:608–613

    CAS  PubMed  Google Scholar 

  • Berry EA, Guergova-Kuras M, Huang LS, Crofts AR (2000) Structure and function of cytochrome bc complexes. Annu Rev Biochem 69:1005–1075

    CAS  PubMed  Google Scholar 

  • Bjorkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    CAS  PubMed  Google Scholar 

  • Blanco NE, Ceccoli RD, Dalla Vía MV, Voss I, Segretin ME, Bravo-Almonacid FF, Melzer M, Hajirezaei M-R, Scheibe R, Hanke GT (2013) Expression of the minor isoform pea ferredoxin in tobacco alters photosynthetic electron partitioning and enhances cyclic electron flow. Plant Physiol 161:866–879

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boyer PD (1993) The binding change mechanism for ATP synthase—some probabilities and possibilities. Biochim Biophys Acta 1140:215–250

    CAS  PubMed  Google Scholar 

  • Boyer PD (1997) The ATP synthase—a splendid molecular machine. Annu Rev Biochem 66:717–749

    CAS  PubMed  Google Scholar 

  • Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318:322–373

    CAS  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

    CAS  PubMed  Google Scholar 

  • Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341–374

    CAS  Google Scholar 

  • Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288:1–9

    CAS  PubMed  Google Scholar 

  • Bulychev AA (2011) Induction changes in Photosystems I and II in plant leaves upon modulation of membrane ion transport. Biochemistry (Moscow) 5:335–342

    Google Scholar 

  • Bulychev AA, Vredenberg WJ (2010) Induction kinetics of photosystem I-activated P700 oxidation in plant leaves and their dependence on pre-energization. Russ J Plant Physiol 57:599–608

    CAS  Google Scholar 

  • Bulychev AA, Cherkashin AA, Rubin AB (2010) Dependence of chlorophyll P700 redox transients during induction period on the transmembrane distribution of protons in chloroplasts of pea leaves. Russ J Plant Physiol 57:23–31

    Google Scholar 

  • Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cardon ZG, Berry J (1992) Effects of O2 and CO2 concentration on the steady-state fluorescence yield of single guard cell pairs in intact leaf discs of Tradescantia albiflora. Plant Physiol 99:1238–1244

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in Photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817:26–43

    CAS  PubMed  Google Scholar 

  • Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134

    CAS  Google Scholar 

  • Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V, Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20:1029–1039

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen RO, Shen G, Golbeck JH, Xu W, Chitnis PR, Valieva A, van der Est A, Pushkar Y, Stehlik D (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 43:4741–4754

    CAS  PubMed  Google Scholar 

  • Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b 6 f complex. Annu Rev Biochem 75:769–790

    CAS  PubMed  Google Scholar 

  • Cramer WA, Hasan SS, Yamashita E (2011) The Q cycle of cytochrome bc complexes: a structure perspectives. Biochim Biophys Acta 1807:788–802

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crofts AR (2004) The cytochrome bc 1 complex: function in the context of structure. Annu Rev Physiol 66:689–733

    CAS  PubMed  Google Scholar 

  • Crofts AR, Guergova-Kuras M, Kuras R, Ugulava N, Li J, Hong S (2000) Proton-coupled electron transfer at the Qo-site: what type of mechanism can account for the high activation barrier? Biochim Biophys Acta 1459:456–466

  • Crofts AR, Hong S, Wilson C, Burton R, Victoria D, Harrison C, Schulten K (2013) The mechanism of ubihydroquinone oxidation at the Qo-site of the cytochrome bc 1 complex. Biochim Biophys Acta 1827:1362–1377

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vivo and in vitro. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry 40:1226–1237

    CAS  PubMed  Google Scholar 

  • Cruz JA, Kanazawa A, Treff N, Kramer DM (2005a) Storage of light-driven transthylakoid proton motive force as an electric field (Δψ) under steady-state conditions in intact cells of Chlamydomonas reinhardtii. Photosynth Res 85:221–233

    CAS  PubMed  Google Scholar 

  • Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005b) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406

    CAS  PubMed  Google Scholar 

  • DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann 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

    CAS  PubMed  Google Scholar 

  • Dashdorj N, Xu W, Cohen RO, Golbeck JH, Savikhin S (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 88:1238–1249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    CAS  PubMed  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 1273:150–158

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    CAS  Google Scholar 

  • Demmig-Adams B, Cohu CM, Muller O, Adams WW (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75–88

    CAS  PubMed  Google Scholar 

  • Dietz K-J, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Edwards GE, Walker DA (1983) C3, C4: mechanisms, and cellular and environmental regulation of photosynthesis. Blackwell, Oxford

    Google Scholar 

  • Endo T, Shikanai T, Sato F, Asada K (1998) NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron donation to plastoquinone in tobacco chloroplasts. Plant Cell Physiol 39:1226–1231

    CAS  Google Scholar 

  • Feniouk BA, Yoshida M (2008) Regulatory mechanisms of proton translocating F0F1-ATP synthase. In: Schaefer G, Penefsky HS (eds) Bioenergetics. Springer, Berlin, pp 279–308

    Google Scholar 

  • Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129

    CAS  PubMed  Google Scholar 

  • Finazzi G, Zito F, Barbagallo RP, Wollman F-A (2001) Contrasted effects of inhibitors of cytochrome b 6 f complex on state transitions in Chlamydomonas reinhardtii: the role of Qo site occupancy in LHCII kinase activation. J Biol Chem 276:9770–9774

    CAS  PubMed  Google Scholar 

  • Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix J-D, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flügge UI, Friesl M, Heldt HW (1980) The mechanism of the control of carbon fixation by the pH in the chloroplast stroma. Studies with acid mediated proton transfer across the envelope. Planta 149:48–51

    PubMed  Google Scholar 

  • Forti G, Furia A, Bombelli P, Finazzi G (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 132:1464–1474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foyer CH, Furbank RT, Harbinson J, Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25:83–100

    CAS  PubMed  Google Scholar 

  • Foyer CH, Lelandais M, Harbinson J (1992) Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves. Plant Physiol 99:979–986

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661

    CAS  PubMed  Google Scholar 

  • Fromme P, Jordan P, Krauss N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31

    CAS  PubMed  Google Scholar 

  • Galka P, Santabarbara S, Khuong TTH, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (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 24:2963–2978

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta 1837:481–494

    CAS  PubMed  Google Scholar 

  • Gardemann A, Schimkat D, Heldt HW (1986) Control of CO2 fixation regulation of stromal fructose-1,6-bisphosphatase in spinach by pH and Mg2+ concentration. Planta 168:536–545

    CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Google Scholar 

  • Gins VK, Tikhonov AN, Mukhin EN, Ruuge EK (1982) Peculiarities of the functioning of two molecular forms of pea ferredoxin in chloroplast electron transport chain. Biochemistry (Moscow) 47:1581–1587

    Google Scholar 

  • Goltsev VN, Kalaji MN, Kouzmanova MA, Allakhverdiev SI (2014) Variable and delayed chlorophyll a fluorescence—basics and applications in plant sciences. Institute of Computer Sciences, Moscow-Izchevsk, p 220

    Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    CAS  PubMed  Google Scholar 

  • Guss JM, Harrowell PR, Murata M, Norris VA, Freeman HC (1986) Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values. J Mol Biol 192:361–387

    CAS  PubMed  Google Scholar 

  • Haehnel W (1976) The reduction kinetics of chlorophyll a 1 as an indicator for proton uptake between the light reactions in chloroplasts. Biochim Biophys Acta 440:506–521

  • Haehnel W (1984) Photosynthetic electron transport in higher plants. Annu Rev Plant Physiol 35:659–693

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hald S, Pribil M, Leister D, Gallois P, Johnson GN (2008b) Competition between linear and cyclic electron flow in plants deficient in Photosystem I. Biochim Biophys Acta 1777:1173–1183

    CAS  PubMed  Google Scholar 

  • Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305

    CAS  PubMed  Google Scholar 

  • Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant, Cell Environ 36:1071–1084

    CAS  Google Scholar 

  • Harbinson J, Hedley CL (1989) The kinetics of P-700+ reduction in leaves—a novel in situ probe of thylakoid functioning. Plant Cell Environment 12:357–369

  • Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:649–660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harbinson J, Genty B, Foyer C (1990) Relationship between photosynthetic electron transport and stromal enzyme activity in pea leaves: toward an understanding of the nature of photosynthetic control. Plant Physiol 94:545–553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hasan SS, Yamashita E, Cramer WA (2013) Transmembrane signaling and assembly of the cytochrome b 6 f-lipidic charge transfer complex. Biochim Biophys Acta 1827:1295–1308

    CAS  PubMed Central  Google Scholar 

  • He X, Miginiac-Maslow M, Sigalat C, Keryer E, Haraux F (2000) Mechanism of activation of the chloroplasts ATP synthase. J Biol Chem 275:13250–13258

    CAS  PubMed  Google Scholar 

  • Heber U (2002) Irrungen, wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231

    CAS  PubMed  Google Scholar 

  • Heldt HW, Werdan K, Milivancev M, Geller G (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta 314:224–241

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Hodges M, Cornic G, Briantais J-M (1989) Chlorophyll fluorescence from spinach leaves: resolution of non-photochemical quenching. Biochim Biophys Acta 974:289–293

    CAS  Google Scholar 

  • Hofmann NR (2012) A refined model of state transitions in plant thylakoid membranes. Plant Cell 24:2708

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holmgren A (1985) Thioredoxin. Annu Rev Biochem 54:237–271

    CAS  PubMed  Google Scholar 

  • Hope AB, Valente P, Matthews DB (1994) Effects of pH on the kinetics of redox reactions in and around the cytochrome bf complex in an isolated system. Photosynth Res 42:111–120

    CAS  PubMed  Google Scholar 

  • Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Phil Trans R Soc B 367:3455–3465

    CAS  PubMed Central  PubMed  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    CAS  PubMed  Google Scholar 

  • Ikeuchi M, Uebayashi N, Sato F, Endo T (2014) Physiological functions of PsbS-dependent and PsbS-independent NPQ under naturally fluctuating light conditions. Plant Cell Physiol 55:1286–1295

    CAS  PubMed  Google Scholar 

  • Ivanov B, Kobayashi Y, Bukhov NG, Heber U (1998) Photosystem I-dependent cyclic electron flow in intact spinach chloroplasts: occurrence dependence on redox conditions and electron acceptors and inhibition by antimycin A. Photosynth Res 57:61–70

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010b) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1214

    CAS  PubMed  Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    CAS  PubMed  Google Scholar 

  • Järvi S, Gollan PJ, Aro E-M (2013) Understanding the roles of the thylakoid lumen in photosynthetic regulation. Front Plant Sci. doi:10.3389/fpls.2013.00434

    PubMed Central  PubMed  Google Scholar 

  • Joet T, Cournac L, Horvath EM, Medgyesy P, Peltier G (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 125:1919–1929

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artefact? J Exp Bot 56:407–416

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Johnson MP, Ruban AV (2014) Rethinking the existence of a steady-state Δψ component of the proton motive force across plant thylakoid membranes. Photosynth Res 119:233–242

    CAS  PubMed  Google Scholar 

  • Johnson GN, Young AJ, Scholes JD, Horton P (1993) The dissipation of excess excitation energy in British plant species. Plant, Cell Environ 16:673–679

    CAS  Google Scholar 

  • Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582:259–263

    Google Scholar 

  • Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kangasjärvi S, Tikkanen M, Durian G, Aro E-M (2014) Photosynthetic light reactions—an adjustable hub in basic production and plant immunity signaling. Plant Physiol Biochem 81:128–134

    PubMed  Google Scholar 

  • Karavaev VA, Kukushkin AK (1975) Adaptation to darkness and far red light of leaves of higher plants in conditions of oxygen deficiency. Biophysics 20:86–91

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

  • Kautski H, Hirsch A (1931) Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 19:964

    Google Scholar 

  • Kereïche S, Kiss AZ, Kouril R, Boekema EJ, Horton P (2010) The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:759–764

    PubMed  Google Scholar 

  • Khatoon M, Inagawa K, Pospíšil P, Yamashita A, Yoshioka M, Lundin B, Horie J, Morita N, Jajoo A, Yamamoto Y, Yamamoto Y (2009) Quality control in Photosystem II. Thylakoid unstacking is necessary to avoid further damage to the D1 protein and to facilitate D1 degradation under light stress in spinach thylakoids. J Biol Chem 284:25343–25352

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirchhoff H (2008) Significance of protein crowding, order and mobility for photosynthetic membrane functions. Biochem Soc Trans 36:967–970

    CAS  PubMed  Google Scholar 

  • Kirchhoff H (2013) Architectural switches in plant thylakoid membranes. Photosynth Res 116:481–487

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kirchhoff H, Horstmann S, Weis E (2000) Control of the photosynthetic electron transport by PQ diffusion in microdomains in thylakoids of higher plants. Biochim Biophys Acta 1459:148–168

    CAS  PubMed  Google Scholar 

  • Kirchhoff H, Tremmel I, Haase W, Kubitscheck U (2004) Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry 43:9204–9213

    CAS  PubMed  Google Scholar 

  • Kirchhoff H, Haferkamp S, Allen JF, Epstein DBA, Mulineaux CW (2008) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol 146:1571–1578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirchhoff H, Hall C, Wood M, Herbstová M, Tsabari O, Nevo R, Charuvi D, Shimoni E, Reich Z (2011) Dynamic control of protein diffusion within the granal thylakoid lumen. Proc Natl Acad Sci USA 108:20248–20253

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978

    CAS  PubMed  Google Scholar 

  • Kobayasi Y, Inoue Y, Furuya F, Shibata K, Heber U (1979a) Regulation of adenylate level in intact spinach chloroplasts. Planta 147:69–75

  • Kobayasi Y, Inoue Y, Shibata K, Heber U (1979b) Control of electron flow in intact chloroplasts by the intrathylakoid pH, not by phosphorylation potential. Planta 146:481–486

    Google Scholar 

  • Kong S-G, Wada M (2011) New insights into dynamic actin-based chloroplast photorelocation movement. Mol Plant 4:771–781

    CAS  PubMed  Google Scholar 

  • Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B 137:89–99

    CAS  PubMed  Google Scholar 

  • Kono M, Noguchi K, Terashima I (2014) Roles of cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004

    CAS  PubMed  Google Scholar 

  • Kouril R, Zygadlo A, Arteni AA, DeWit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940

    CAS  PubMed  Google Scholar 

  • Kouril R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Asta 1817:2–12

    CAS  Google Scholar 

  • Kraayenhof R (1969) ‘State 3–State 4 transition’ and phosphate potential in ‘Class I’ spinach chloroplasts. Biochim Biophys Acta 180:213–215

    CAS  PubMed  Google Scholar 

  • Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163

    CAS  Google Scholar 

  • Kramer DM, Sacksteder CA, Cruz JA (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kubicki A, Funk E, Westhoff P, Steinmuller K (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 199:276–281

  • Kubota K, Sakurai I, Katayama K, Mizusawa N, Ohashi S, Kobayashi M, Zhang P, Aro E-M, Wada H (2010) Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits. Biochim Biophys Acta 1797:98–105

    CAS  PubMed  Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    CAS  PubMed  Google Scholar 

  • Kurisu G, Nishiyama D, Kusunoki M, Fujikawa S, Katoh M, Hanke GT, Hase T, Teshima K (2005) A structural basis of Equisetum arvense ferredoxin isoform II producing an alternative electron transfer with ferredoxin-NADP-Reductase. J Biol Chem 280:2275–2281

    CAS  PubMed  Google Scholar 

  • Kurreck J, Schödel R, Renger G (2000) Investigation of the plastoquinone pool size and fluorescence quenching in thylakoid membranes and photosystem II (PS II) membrane fragments. Photosynth Res 63:171–182

    CAS  PubMed  Google Scholar 

  • Kuvykin IV, Vershubskii AV, Ptushenko VV, Tikhonov AN (2008) Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants. Biochemistry (Moscow) 73:1063–1075

  • Kuvykin IV, Ptushenko VV, Vershubskii AV, Tikhonov AN (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 1807:336–347

  • Laisk A (1977) Kinetics of photosynthesis and photorespiration in C3 plants. Nauka, Moscow 198 pp

  • Laisk A, Oja V, Kiirats O, Raschke K, Heber U (1989) The state of photosynthetic apparatus in leaves as analyzed by rapid gas exchange and optical methods: the pH of the chloroplast stroma and activation of enzymes in vivo. Planta 177:350–358

    CAS  PubMed  Google Scholar 

  • Laisk A, Eichelmann H, Oja V, Peterson RB (2005) Control of cytochrome b 6 f at low and high light intensity and cyclic electron transport in leaves. Biochim Biophys Acta 1708:79–90

    CAS  PubMed  Google Scholar 

  • Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48:1575–1588

    CAS  PubMed  Google Scholar 

  • Laisk A, Talts E, Oja V, Eichelmann H, Peterson R (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95

    CAS  PubMed  Google Scholar 

  • Lavergne J, Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16:129–134

    CAS  PubMed  Google Scholar 

  • Lavergne J, Bouchaud J-P, Joliot P (1992) Plastoquinone compartimentation in chloroplasts. II. Theoretical aspects. Biochim Biophys Acta 1101:13–22

    CAS  Google Scholar 

  • Lawson T, Oxborough K, Morison JIL, Baker NR (2002) Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. Plant Physiol 128:52–62

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lazar D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28

    CAS  PubMed  Google Scholar 

  • Lazar D (2003) Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J Theor Biol 220:469–503

  • Leister D, Shikanai T (2013) Complexities and protein complexes in the antimycin A—sensitive pathway of cyclic electron flow in plants. Front Plant Sci. doi:10.3389/fpls.2013.00161

    Google Scholar 

  • Lemeille S, Rochaix J-D (2010) State transitions at the crossroad of thylakoid signaling pathways. Photosynth Res 106:33–46

    CAS  PubMed  Google Scholar 

  • Lemeille S, Willig A, Depege-Fargeix N, Delessert C, Bassi R, Rochaix J-D (2009) Analysis of the chloroplasts protein kinase Stt7 during state transition. PLoS Biol 7(e1000045):664–673

    Google Scholar 

  • Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b 6 f complex in Arabidopsis. Plant Cell 13:2539–2551

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Li X-P, Muller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li X-P, 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

    CAS  PubMed  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    CAS  PubMed  Google Scholar 

  • Ligeza A, Tikhonov AN, Subszynski WK (1997) In situ measurements of oxygen production using paramagnetic fusinite particles injected into a bean leaf. Biochim Biophys Acta 1319:133–137

  • Ligeza A, Tikhonov AN, Hyde JS, Subczynski WK (1998) Oxygen permeability of thylakoid membranes: EPR spin labeling study. Biochim Biophys Acta 1365:453–463

    CAS  PubMed  Google Scholar 

  • Los DA, Mironov KS, Allakhverdiev SI (2013) Regulatory role of membrane fluidity in gene expression and physiological functions. Photosynth Res 116:489–509

    CAS  PubMed  Google Scholar 

  • Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981

    CAS  PubMed  Google Scholar 

  • Maxwell PC, Biggins J (1977) The kinetic behavior of P-700 during the induction of photosynthesis in algae. Biochim Piophys Acta 459:442–450

    CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Botany 51:659–668

    CAS  Google Scholar 

  • McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Huner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967

    CAS  PubMed  Google Scholar 

  • Mehler AH (1951) Studies on reactions of illuminated chloroplasts. I. Mechanisms of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77

    CAS  PubMed  Google Scholar 

  • Michelet L, Zaffagnini M, Morisse S, Sparla F, Perez-Perez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin–Benson cycle: something old, something new. Front Plant Sci. doi:10.3389/fpls.2013.00470

    PubMed Central  PubMed  Google Scholar 

  • Mills JD (2004) The regulation of chloroplast ATP synthase, CF0–CF1. Oxygenic photosynthesis: the light reactions. Adv Photosynth Respir 4:469–485

    Google Scholar 

  • Minagawa J (2011) State transitions-The molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807:897–905

    CAS  PubMed  Google Scholar 

  • Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:445–502

    CAS  PubMed  Google Scholar 

  • Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62:327–367

    CAS  PubMed  Google Scholar 

  • Miyake C (2010) Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963

    CAS  PubMed  Google Scholar 

  • Miyake C, Yokota A (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 41:335–343

    CAS  PubMed  Google Scholar 

  • Morison JIL (1998) Stomatal response to increased CO2 concentration. J Exp Bot 49:443–453

    Google Scholar 

  • Motohashi K, Hisabori T (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 281:35039–35047

    CAS  PubMed  Google Scholar 

  • Mott KA, Berry JA (1986) Effect of pH on activity and activation of ribulose 1,5-biphosphate carboxylase at air level of CO2. Plant Physiol 82:77–82

  • Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65

  • Mula S, Savitsky A, Moebius K, Lubitz W, Golbeck JH, Mamedov MD, Semenov AYu, van der Est A (2012) Incorporation of a high potential quinone reveals that electron transfer in photosystem I becomes highly asymmetric at low temperature. Photochem Photobiol Sci 11:946–956

  • Mulkidjanian AY (2005) Ubiquinol oxidation in the cytochrome bc 1 complex: reaction mechanism and prevention of short-circuiting. Biochim Biophys Acta 1709:5–34

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mullineaux CW (2014) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    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 49:1688–1698

    CAS  PubMed  Google Scholar 

  • Murata N (2009) The discovery of state transitions in photosynthesis 40 years ago. Photosynth Res 99:155–160

    CAS  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    CAS  PubMed  Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, a-tocopherol, nonphotochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133

    CAS  PubMed  Google Scholar 

  • Nagy G, Posselt D, Kovács L, Holm JK, Szabó M, Ughy B, Rosta L, Peters J, Timmins P, Garab G (2011) Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering. Biochem J 436:225–230

  • Nagy G, Kovács L, Unnep R, Zsiros O, Almásy L, Rosta L, Timmins P, Peters J, Posselt D, Garab G (2013) Kinetics of structural reorganizations in multilamellar photosynthetic membranes monitored by small-angle neutron scattering. Eur Phys J E 36:69. doi:10.1140/epje/i2013-13069-0

    PubMed  Google Scholar 

  • Nakanishi-Matsui M, Sekiya M, Nakamoto RK, Futai M (2010) The mechanism of rotating proton pumping ATPases. Biochim Biophys Acta 1797:1343–1352

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nilkens M, Kress E, Lambrev PH, Miloslavina Y, Muller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady state conditions in Arabidopsis. Biochim Biophys Acta 1797:466–475

    CAS  PubMed  Google Scholar 

  • Nishio JN, Whitmarsh J (1993) Dissipation of the proton electrochemical potential in intact chloroplasts. II. The pH gradient monitored by cytochrome f reduction kinetics. Plant Physiol 101:89–96

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noctor G, Rees D, Young A, Horton P (1991) The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence and the transthylakoid pH-gradient in isolated chloroplasts. Biochim Biophys Acta 1057:320–330

    CAS  Google Scholar 

  • Ogawa T, Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93:69–77

    CAS  PubMed  Google Scholar 

  • Ohyama K, Fukazawa H, Kohchi T, Shirai H, Tohru S, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota SI, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574

    CAS  Google Scholar 

  • Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol 49:825–834

    CAS  PubMed  Google Scholar 

  • Őquist G, Chow WS, Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186:450–460

    PubMed  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opp Plant Biol 5:193–197

    CAS  Google Scholar 

  • Osyczka A, Moser CC, Dutton PL (2005) Fixing the Q cycle. Trends Biochem Sci 30:176–182

    CAS  PubMed  Google Scholar 

  • Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components: calculation of qP and F v /F m without measuring F o. Photosynth Res 54:135–142

    CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence. A signature of photosynthesis, vol 19. Springer, Dordrecht

  • Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Botany 52:1383–1400

    CAS  Google Scholar 

  • Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:412–453

    Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T (2009) Efficient operation of NAD(P)H dehydrogenase requires the supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21:3623–3640

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pfündel EE, Dilley RA (1993) The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts. Plant Physiol 101:65–71

    PubMed Central  PubMed  Google Scholar 

  • Pfündel EE, Renganathan M, Gilmore AM, Yamamoto HY, Dilley RA (1994) Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin deepoxidation. Plant Physiol 106:1647–1658

    PubMed Central  PubMed  Google Scholar 

  • Ptushenko VV, Ptushenko EA, Samoilova OP, Tikhonov AN (2013) Chlorophyll fluorescence in the leaves of Tradescantia species of different ecological groups: induction events at different intensities of actinic light. BioSystems 112:85–97

  • Quick WP, Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim Biophys Acta 977:287–296

    CAS  Google Scholar 

  • Rees D, Young A, Noctor G, Britton G, Horton P (1989) Enhancement of the pH-dependent dissipation of excitation energy in spinach chloroplasts by light activation: correlation with the synthesis of zeaxanthin. FEBS Lett 256:85–90

  • Rees D, Noctor G, Ruban AV, Crofts J, Young A, Horton P (1992) pH dependent chlorophyll fluorescence quenching in spinach thylakoids from light-treated or dark-adapted leaves. Photosynth Res 31:11–19

    CAS  PubMed  Google Scholar 

  • Robinson SP (1985) The involvement of stromal ATP in maintaining the pH gradient across the chloroplast envelope in the light. Biochim Biophys Acta 806:187–194

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Romanovsky YuM, Tikhonov AN (2010) Molecular energy transducers of the living cell. Proton ATP synthase: a rotating molecular motor. Phys Usp 53:893–914

    CAS  Google Scholar 

  • Ruban AV, Horton P (1995) An investigation of the sustained component of non-photochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiol 108:721–726

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Dufy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    CAS  PubMed  Google Scholar 

  • Rumberg B, Siggel U (1969) pH changes in the inner phase of the thylakoids during photosynthesis. Naturwissenschaften 56:130–132

    CAS  PubMed  Google Scholar 

  • Ryzhikov SB, Tikhonov AN (1988) Regulation of electron transfer in photosynthetic membranes of higher plants. Biophysics 33:642–646

  • Sage RF, Cen Y-P, Li M (2002) The activation state of Rubisco directly limits photosynthesis at low CO2 and low O2 partial pressures. Photosynth Res 71:241–250

    CAS  PubMed  Google Scholar 

  • Samoilova OP, Ptushenko VV, Kuvykin IV, Kiselev SA, Ptushenko OS, Tikhonov AN (2011) Effects of light environment on the induction of chlorophyll fluorescence in leaves: a comparative study of Tradescantia species of different ecotypes. BioSystems 105:41–48

    CAS  PubMed  Google Scholar 

  • Sato R, Ohta H, Masuda S (2014) Prediction of respective contributions of linear electron flow and PGR5-dependent cyclic electron flow to non-photochemical quenching induction. Plant Physiol Biochem 81:190–196

    CAS  PubMed  Google Scholar 

  • Savitsky A, Gopta O, Mamedov M, Golbeck JH, Tikhonov A, Möbius K, Semenov A (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 37:85–102

    Google Scholar 

  • Sazanov LA, Burrows P, Nixon PJ (1996) Detection and characterization of a complex I-like NADH-specific dehydrogenase from pea thylakoids. Biochem Soc Trans 24:739–743

    CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynth Res 120:43–58

    CAS  PubMed  Google Scholar 

  • Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plantarum 120:21–26

    CAS  Google Scholar 

  • Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, Dordrecht, pp 409–435

    Google Scholar 

  • Schönknecht G, Neimanis S, Katona E, Gerst U, Heber U (1995) Relationship between photosynthetic electron transport and pH gradient across the thylakoid membrane in intact leaves. Proc Natl Acad Sci USA 92:12185–12189

    PubMed Central  PubMed  Google Scholar 

  • Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272

    CAS  PubMed  Google Scholar 

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. A signature of Photosynthesis, vol 19. Springer, Dordrecht, pp 279–319

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    CAS  PubMed  Google Scholar 

  • Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth Res 113:127–144

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 56:1184–1193

    Google Scholar 

  • Serrato AJ, Fernandez-Trijueque J, Barajas-Lopez J-D, Chueca A, Sahrawy M (2013) Plastid thioredoxins: a “one-for-all”redox-signaling system in plants. Front Plant Sci. doi:10.3389/fpls.2013.00463

    PubMed Central  PubMed  Google Scholar 

  • Shelaev IV, Gostev FE, Mamedov MD, Sarkisov OM, Nadtochenko VA, Shuvalov VA, Semenov AY (2010) Femtosecond primary charge separation in photosystem I. Biochim Biophys Acta 1797:1410–1420

    CAS  PubMed  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    CAS  PubMed  Google Scholar 

  • Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95:9705–9709

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    CAS  PubMed Central  PubMed  Google Scholar 

  • Solovchenko A (2010) Photoprotection in Plants. Springer series in biophysics, vol 14. Springer, Berlin

  • Stiehl HH, Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch Teil B 24:1588–1598

    CAS  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol, B 104:236–257

    CAS  Google Scholar 

  • Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise. Photosynth Res 113:15–61

  • Stock D, Gibbons C, Arechaga I, Leslie AG, Walker JE (2000) The rotary mechanism of ATP synthase. Curr Opin Struct Biol 10:672–679

    CAS  PubMed  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transients. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 321–362

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

    CAS  PubMed  Google Scholar 

  • Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro E-M (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

  • Tagawa K, Tsujimoto HY, Arnon DI (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc Natl Acad Sci USA 49:567–572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969

    CAS  PubMed  Google Scholar 

  • Takahashi S, Badger M (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    CAS  PubMed  Google Scholar 

  • Tikhonov AN (2012) Energetic and regulatory role of proton potential in chloroplasts. Biochemistry (Moscow) 77:956–974

    CAS  Google Scholar 

  • Tikhonov AN (2013) pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynth Res 116:511–534

    CAS  PubMed  Google Scholar 

  • Tikhonov AN (2014) The cytochrome b 6 f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183

    CAS  PubMed  Google Scholar 

  • Tikhonov AN, Timoshin AA (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 (Mosc) 2:608–622

    CAS  Google Scholar 

  • Tikhonov AN, Vershubskii AV (2014) Computer modeling of electron and proton transport in chloroplasts. BioSystems 121:1–21

    CAS  PubMed  Google Scholar 

  • Tikhonov AN, Khomutov GB, Ruuge EK, Blumenfeld LA (1981) Electron transport control in chloroplasts. Effects of photosynthetic control monitored by the intrathylakoid pH. Biochim Biophys Acta 637:321–333

    CAS  Google Scholar 

  • Tikhonov AN, Khomutov GB, Ruuge EK (1984) Electron transport control in chloroplasts. Effects of magnesium ions on the electron flow between two photosystems. Photobiochem Photobiophys 8:261–269

    CAS  Google Scholar 

  • Tikhonov AN, Agafonov RV, Grigor’ev IA, Kirilyuk IA, Ptushenko VV, Trubitsin BV (2008) Spin-probes designed for measuring the intrathylakoid pH in chloroplasts. Biochim Biophys Acta 1777:285–294

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Aro E-M (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817:232–238

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Aro E-M (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’. Trends Plant Sci 16:126–131

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Grieco M, Nurmi M, Rantala M, Suorsa M, Aro E-M (2012) Regulation of the photosynthetic apparatus under fluctuating growth light. Philos Trans R Soc Lond B 367:3486–3493

    CAS  Google Scholar 

  • Tikkanen M, Mekala NR, Aro E-M (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215

    CAS  PubMed  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203

    PubMed  Google Scholar 

  • Tremmel IG, Kirchhoff H, Weis E, Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Biophys Acta 1603:97–109

    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 1817:2140–2148

    CAS  PubMed  Google Scholar 

  • Trubitsin BV, Tikhonov AN (2003) Determination of a transmembrane pH difference in chloroplasts with a spin label Tempamine. J Magn Reson 163:257–269

    CAS  PubMed  Google Scholar 

  • Trubitsin BV, Mamedov MD, Vitukhnovskaya LA, Semenov AYu, Tikhonov AN (2003) EPR study of photosynthetic electron transport control in cells of Synechocystis sp. strain PCC 6803. FEBS Lett 544:15–20

    CAS  PubMed  Google Scholar 

  • Trubitsin BV, Ptushenko VV, Koksharova OA, Mamedov MD, Vitukhnovskaya LA, Grigor’ev IA, Semenov AYu, Tikhonov AN (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 1708:238–249

    CAS  PubMed  Google Scholar 

  • Tychinsky VP, Tikhonov AN (2010) Interference microscopy in cell biophysics. 2. Visualization of individual cells and energy-transducing organelles. Cell Biochem Biophys 58:117–128

    CAS  PubMed  Google Scholar 

  • Tychinsky VP, Kretushev AV, Vyshenskaya TV, Tikhonov AN (2004) A dynamic phase microscopic study of optical characteristics of individual chloroplasts. Biochim Biophys Acta 1665:57–64

    CAS  PubMed  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 A. Nature 473:55–60

    CAS  PubMed  Google Scholar 

  • Vallon O, Bulte L, Dainese P, Olive J, Bassi R, Wollman F-A (1991) Lateral redistribution of cytochrome b 6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci USA 88:8262–8266

    CAS  PubMed Central  PubMed  Google Scholar 

  • van Gorkom HJ, Tamminga JJ, Haveman J (1974) Primary reactions, plastoquinone and fluorescence yield in subchloroplast fragments prepared with deoxycholate. Biochim Biophys Acta 347:417–438

    PubMed  Google Scholar 

  • Vener AV, van Kan PJ, Rich PR, Ohad I, Andersson B (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 USA 94:1585–1590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vershubskii AV, Kuvykin IV, Priklonskii VI, Tikhonov AN (2011) Functional and topological aspects of pH-dependent regulation of electron and proton transport in chloroplasts in silico. BioSystems 103:164–179

  • Vishnyakova EA, Trubitsin BV, Tikhonov AN (2000) Kinetics of photoinduced redox conversions in the reaction center P700 in leaves of C3 and C4 plants. Biophysics 45:873–877

    Google Scholar 

  • von Ballmoos C, Wiedenmann A, Dimroth P (2009) Essentials forATPsynthesis by F1F0 ATP synthases. Annu Rev Biochem 78:649–672

    Google Scholar 

  • Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468

    CAS  PubMed  Google Scholar 

  • Webber AN, Lubitz W (2001) P700: the primary electron donor of photosystem I. Biochim Biophys Acta 1507:61–79

    CAS  PubMed  Google Scholar 

  • Werdan K, Heldt HW, Milovancev M (1975) The role of the pH in the regulation of carbon fixation in the chloroplast stroma. Biochim Biophys Acta 396:276–292

  • Willmer C, Fricker M (1996) Stomata, 2nd edn. Chapman & Hall, London

    Google Scholar 

  • Witt HT (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. Biochim Biophys Acta 505:355–427

    CAS  PubMed  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Woodrow IE, Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol 39:533–594

  • Yamamoto H, Kato H, Shinzaki Y, Horiguchi S, Shikanai T, Hase T, Endo T, Nishioka M, Makino A, Tomizawa K, Miyake C (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 47:1355–1371

    CAS  PubMed  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

  • Yamamoto Y, Kai S, Ohnishi A, Tsumura N, Ishikawa T, Hori H, Morita N, Ishikawa Y (2014) Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol 55:1206–1215

    CAS  PubMed Central  PubMed  Google Scholar 

  • YamamotoY Hori H, Kai S, Ishikawa T, Ohnishi A, Tsumura N, Morita N (2013) Quality control of photosystem II: reversible and irreversible protein aggregation decides the fate of Photosystem II under excessive illumination. Front Plant Sci. doi:10.3389/fpls.2013.00433

    Google Scholar 

  • Zaks J, Amarnath K, Sylak-Glassman EJ, Fleming GR (2013) Models and measurements of energy-dependent quenching. Photosynth Res 116:389–409

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Scheller HV (2004) Light-harvesting complex II binds to several small subunits of photosystem I. J Biol Chem 279:3180–3187

    CAS  PubMed  Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman F-A (1999) The Qo site of cytochrome b 6 f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2969

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Russian Foundation for Basic Researches (project 12-04-01267a). The author is deeply grateful to E.K. Ruuge, G.B. Khomutov, A.A. Timoshin, S.B. Ryzhikov, B.V. Trubitsin, and V.V. Ptushenko who have been involved in our common works on regulation of electron transport in chloroplasts.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander N. Tikhonov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tikhonov, A.N. Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynth Res 125, 65–94 (2015). https://doi.org/10.1007/s11120-015-0094-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0094-0

Keywords

Navigation