Skip to main content
SpringerLink
Log in

Obstacles in the quantification of the cyclic electron flux around Photosystem I in leaves of C3 plants

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

Abstract

Sixty years ago Arnon and co-workers discovered photophosphorylation driven by a cyclic electron flux (CEF) around Photosystem I. Since then understanding the physiological roles and the regulation of CEF has progressed, mainly via genetic approaches. One basic problem remains, however: quantifying CEF in the absence of a net product. Quantification of CEF under physiological conditions is a crucial prerequisite for investigating the physiological roles of CEF. Here we summarize current progress in methods of CEF quantification in leaves and, in some cases, in isolated thylakoids, of C3 plants. Evidently, all present methods have their own shortcomings. We conclude that to quantify CEF in vivo, the best way currently is to measure the electron flux through PS I (ETR1) and that through PS II and PS I in series (ETR2) for the whole leaf tissue under identical conditions. The difference between ETR1 and ETR2 is an upper estimate of CEF, mainly consisting, in C3 plants, of a major PGR5–PGRL1-dependent CEF component and a minor chloroplast NDH-dependent component, where PGR5 stands for Proton Gradient Regulation 5 protein, PGRL1 for PGR5-like photosynthesis phenotype 1, and NDH for Chloroplast NADH dehydrogenase-like complex. These two CEF components can be separated by the use of antimycin A to inhibit the former (major) component. Membrane inlet mass spectrometry utilizing stable oxygen isotopes provides a reliable estimation of ETR2, whilst ETR1 can be estimated from a method based on the photochemical yield of PS I, Y(I). However, some issues for the recommended method remain unresolved.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ATP:

Adenosine triphosphate

CEF:

Cyclic electron flux around PS I

Chl:

Chlorophyll

Cyt:

Cytochrome

ΔFlux:

Difference between ETR1 and ETR2

ΔpH:

Trans-thylakoid membrane pH difference

Δψ :

Trans-thylakoid membrane electric potential difference

DCMU:

3-(3:4-dichlorophenyl)-1:1-dimethylurea

ECS:

Electrochromic shift

ES:

Energy storage

ETR1, ETR2:

The electron flux through PS I, PS II, respectively

ETR2(O2) :

The electron flux through PS II, measured by gross O2 evolution

f I and f II :

The fraction of absorbed light partitioned to PS I and PS II, respectively

F s and F m :

Steady-state and maximum Chl fluorescence yield during illumination, respectively

FNR:

Ferredoxin/NADP reductase

I :

Irradiance

LHCII:

Light-harvesting chlorophyll-protein complex II

MIMS:

Membrane inlet mass spectrometry

MV:

Methyl viologen

NADPH:

Reduced nicotinamide adenine dinucleotide phosphate

NDH:

Chloroplast NADH dehydrogenase-like complex

P700:

Special chlorophyll pair in PS I

Pc:

Plastocyanin

PGR5:

Proton gradient regulation 5 protein

PGRL1:

PGR5-like photosynthesis phenotype 1

Pmf:

Protonmotive force

PQ:

Plastoquinone

PS II, PS I:

Photosystem II, Photosystem I, respectively

PsaF:

Plastocyanin-binding subunit in PS I

PTOX:

Plastid terminal oxidase

Q A, Q B :

Primary and secondary quinine electron acceptor in PS II, respectively

qE:

Energy-dependent quenching

R ph :

The sum of the photochemical rates

Y(I) and Y(II):

The photochemical yield of PS I and PSII, respectively, during illumination

References

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

    Article  CAS  PubMed  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 (2015) The plastoquinone pool, poised for cyclic electron flow? Front Plant Sci 6:540

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnon DI, Whatley FR, Allen MB (1955) Vitamin K as a cofactor of photosynthetic phosphorylation. Biochim Biophys Acta 16:607–608

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Badger MR (1985) Photosynthetic oxygen-exchange. Annu Rev Plant Physiol Plant Mol Biol 36:27–53

    Article  CAS  Google Scholar 

  • Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Phil Trans R Soc B Biol Sci 355:1433–1446

    Article  CAS  Google Scholar 

  • Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman A (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276

    Article  CAS  PubMed  Google Scholar 

  • Bailleul B, Cardol P, Breyton C, Finazzi G (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth Res 106:179–189

    Article  CAS  PubMed  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    Article  CAS  PubMed  Google Scholar 

  • Beckmann K, Messinger J, Badger MR, Wydrzynski T, Hillier W (2009) On-line mass spectrometry: membrane inlet sampling. Photosynth Res 102:511–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Bukhov N, Carpentier R (2004) Alternative Photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33

    Article  CAS  PubMed  Google Scholar 

  • Canaani O, Schuster G, Ohad I (1989) Photoinhibition in Chlamydomonas reinhardtii—effect on state transition, intersystem energy distribution and Photosystem-I cyclic electron flow. Photosynth Res 20:129–146

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918

    Article  CAS  PubMed  Google Scholar 

  • Chow WS, Hope AB (1987) The stoichiometries of supramolecular complexes in thylakoid membranes from spinach chloroplasts. Aust J Plant Physiol 14:21–28

    Article  CAS  Google Scholar 

  • Chow WS, Hope AB (1998) The electrochromic signal, redox reactions in the cytochrome bf complex and photosystem functioanlity in photoinhibited tobacco leaf segments. Aust J Plant Physiol 25:775–784

    Article  CAS  Google Scholar 

  • Cleland RE, Bendall DS (1992) Photosystem-I cyclic electron transport - Measurement of ferredoxin-plastoquinone reductase activity. Photosynth Res 34:409–418

    Article  CAS  PubMed  Google Scholar 

  • Dang KV, Plet J, Tolleter D, Jokel M, Cuine S, Carrier P, Auroy P, Richaud P, Johnson X, Alric J, Allahverdiyeva Y, Peltier G (2014) Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclci electron flow in Chlamydomonas reinhardtii. Plant Cell 26:3036–3050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Driever SM, Baker NR (2011) The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant Cell Environ 34:837–846

    Article  CAS  PubMed  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

    Article  CAS  Google Scholar 

  • Evans JR, Poorter H (2001) Photosynthetic aclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767

    Article  CAS  Google Scholar 

  • Fan D-Y, Nie Q, Hope AB, Hillier W, Pogson BJ, Chow WS (2007) Quantification of cyclic electron flow around Photosystem I in spinach leaves during photosynthetic induction. Photosynth Res 94:347–357

    Article  CAS  PubMed  Google Scholar 

  • Fan D-Y, Jia H, Barber J, Chow WS (2009) Novel effects of methyl viologen on photosystem II function in spinach leaves. Eur Biophys J 39:191–199

    Article  CAS  PubMed  Google Scholar 

  • Fisher N, Kramer DM (2014) Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: relevance to cyclic electron flow around photosystem I? Biochim Biophys Acta 1837:1944–1954

    Article  CAS  PubMed  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The Relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Golding AJ, Joliot P, Johnson GN (2005) Equilibration between cytochrome f and P700 in intact leaves. Biochim Biophys Acta 1706:105–109

    Article  CAS  PubMed  Google Scholar 

  • Gotoh E, Matsumoto M, Ogawa K, Kobayashi Y, Tsuyama M (2010) A qualitative analysis of the regulation of cyclic electron flow around photosystem I from the post-illumination chlorophyll fluorescence transient in Arabidopsis: a new platform for the in vivo investigation of the chloroplast redox state. Photosynth Res 103:111–123

    Article  CAS  PubMed  Google Scholar 

  • Harbinson J, Woodward FI (1987) The use of light-induced absorbancy changes at 820 nm to monitor the oxidation state of P-700 in leaves. Plant Cell Environ 10:131–140

    CAS  Google Scholar 

  • Harbinson J, Genty B, Baker NR (1989) Relationship between the quantum efficiencies of Photosystem-I and Photosystem-II in pea leaves. Plant Physiol 90:1029–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauska G, Schütz M, Büttner M (1996) The cytochrome b6f complex—composition, structure and function. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Advances in photosynthesis and respiration, vol 4. Kluwer, Dordrecht, pp 377–398

    Chapter  Google Scholar 

  • Heber U, Egneus H, Hanck U, Jensen M, Koster S (1978) Regulation of photosynthetic electron transport and photophosphorylation in intact chloroplasts and leaves of spinacia oleracea L. Planta 143:41–49

    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 

  • Hippler M, Reichert J, Sutter M, Zak E, Altschmied L, Schroer 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 JD (1997) Fast electron transfer from cytochrome c(6) and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36:6343–6349

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll protein complex. FEBS Lett 292:1–4

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jia H, Oguchi R, Hope AB, Barber J, Chow WS (2008) Differential effects of severe water stress on linear and cyclic electron fluxes through Photosystem I in spinach leaf discs in CO2-enriched air. Planta 228:803–812

    Article  CAS  PubMed  Google Scholar 

  • Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128:760–769

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Johnson GN (2011) Physiology of PS I cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P, Ozawa SI, Houille-Vernes L, Petroutsos D, Rappaport F, Grossman AR, Niyogi KK, Hippler M, Alric J (2014) Proton gradient regulation-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 165:438–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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 

  • Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99:12789–12794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirchhoff H, Sharpe RM, Herbstova M, Yarbrough R, Edwards GE (2013) Differential mobility of pigment-protein complexes in granal and agranal thylakoid membranes of C3 and C4 plants. Plant Physiol 161:497–507

    Article  CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1991) Analysis of light-induced absorbancy changes in the near-infrared spectral region.1. Characterization of various components in isolated chloroplasts. Z Naturforsch C 46:233–244

    CAS  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of Photosystem-I quantum yield via P700+ absorbancy changes at 830 nm. Planta 192:261–268

    Article  CAS  Google Scholar 

  • Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14. http://www.walz.com/products/chl_p700/pan/overview.html

  • Kobayashi Y, Heber U (1994) Rates of vectorial proton transport supported by cyclic electron flow during oxygen reduction by illuminated intact chloroplasts. Photosynth Res 41:419–428

    Article  CAS  PubMed  Google Scholar 

  • Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PS I (CEF-PS I) 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

    Article  CAS  PubMed  Google Scholar 

  • Kou J, Takahashi S, Oguchi R, Fan D-Y, Badger MR, Chow WS (2013) Estimation of the steady-state cyclic electron flux around PS I in spinach leaf discs in white light, CO2-enriched air and other varied conditions. Funct Plant Biol 40:1018–1028

    Article  CAS  Google Scholar 

  • Kou J, Takahashi S, Fan D-Y, Badger MR, Chow WS (2015) Partially dissecting the steady-state electron fluxes in Photosystem I in wild-type and pgr5 and ndh mutants of Arabidopsis. Frontiers Plant Sci 6:758

    Article  Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    Article  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 reactions. Trends Plant Sci 9:349–357

    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 Regulation 5-Like 1-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 

  • Lam E, Malkin R (1982) Ferredoxin-mediated reduction of Cytochrome-b-563 in a chloroplast cytochrome b-563/f complex. FEBS Lett 141:98–101

    Article  CAS  Google Scholar 

  • Laureau C, De Paepe R, Latouche G, Moreno-Chacon 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 

  • Lavergne J, Trissl H-W (1995) Theory of fluorescence induction in Photosystem II—derivation of analytical expressions in a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68:2474–2492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazar D (2013) Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise. J Theor Biol 335:249–264

    Article  CAS  PubMed  Google Scholar 

  • Malkin S, Canaani O (1994) The use and characteristics of the photoacoustic method in the study of photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45:493–526

    Article  CAS  Google Scholar 

  • Malkin S, Charland M, Leblanc RM (1992) A photoacoustic study of water infiltrated leaves. Photosynth Res 33:37–50

    Article  CAS  PubMed  Google Scholar 

  • Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by photoinduced turnover of P-700 in vivo. Biochem 15:3975–3981

    Article  CAS  Google Scholar 

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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, 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 

  • Nakamura N, Iwano M, Havaux M, Yokota A, Munekage YN (2013) Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C4 photosynthesis in the genus Flavaria. New Phytol 199:832–842

    Article  CAS  PubMed  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 1767:1252–1259

    Article  CAS  PubMed  Google Scholar 

  • Oguchi R, Douwstra P, Fujita T, Chow WS, Terashima I (2011) Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159

    Article  PubMed  Google Scholar 

  • Oja V, Eichelmann H, Peterson RB, Rasulov B, Laisk A (2003) Deciphering the 820 nm signal: redox state of donor side and quantum yield of Photosystem I in leaves. Photosynth Res 78:1–15

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pfundel E (1998) Estimating the contribution of Photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195

    Article  CAS  Google Scholar 

  • Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PS I Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204:81–91

    Article  CAS  PubMed  Google Scholar 

  • Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368

    Article  CAS  PubMed  Google Scholar 

  • Sacksteder CA, Kramer DM (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth Res 66:145–158

    Article  CAS  PubMed  Google Scholar 

  • Schansker G, Srivastava A, Govindjee Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785–796

    Article  CAS  Google Scholar 

  • Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse-modulation ystem. Z Naturforsch C 43:686–698

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotech 26:25–30

    Article  CAS  PubMed  Google Scholar 

  • Shirao M, Kuroki S, Kaneko K, Kinjo Y, Tsuyama M, Forster B, Takahashi S, Badger MR (2013) Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol 54:1152–1163

    Article  CAS  PubMed  Google Scholar 

  • Siebke K, von Caemmerer S, Badger M, Furbank RT (1997) Expressing an RbcS antisense gene in transgenic Flaveria bidentis leads to an increased quantum requirement for CO2 fixed in photosystems I and II. Plant Physiol 115:1163–1174

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sigfridsson K, Young S, Hansson O (1997) Electron transfer between spinach plastocyanin mutants and photosystem 1. Eur J Biochem 245:805–812

    Article  CAS  PubMed  Google Scholar 

  • Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM (2015a) Activation of cyclic electron flow by hydrogen peroxide in vivo. Proc Natl Acad Sci USA 112:5539–5544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strand DD, Fisher N, Davis GA, Kramer DM (2015b) Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystm I in higher plant thylakoids. Biochim Biophys Acta. doi:10.1016/j.bbabio.2015.07.012

    PubMed  Google Scholar 

  • Suorsa M (2015) Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages. Frontiers Plant Sci 6:800

    Article  Google Scholar 

  • Takahashi S, Milward SE, Fan D-Y, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567

    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. Nature Commun 4:1954

    Google Scholar 

  • Vassiliev IR, Jung YS, Mamedov MD, Semenov AY, Golbeck JH (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72:301–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veeranjaneyulu K, Charland M, Leblanc RM (1998) High-irradiance stress and photochemical activities of photosystems 1 and 2 in vivo. Photosynthetica 35:177–190

    Article  CAS  Google Scholar 

  • Vredenberg WJ, Bulychev AA (2010) Photoelectrochemical control of the balance between cyclic and linear electron transport in photosystem I. Algorithm for P700(+) induction kinetics. Biochim Biophys Acta 1797:1521–1532

    Article  CAS  PubMed  Google Scholar 

  • Vredenberg WJ, Tonk WJM (1975) Steady-state electrical potential difference across thylakoid membranes of chloroplasts in illuminated plant cells. Biochim Biophys Acta 387:580–587

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The support of this work by an Australian Research Council Grant (DP1093827) awarded to W.S.C. and a Knowledge Innovation Program of the Chinese Academy of Sciences grant (KZCX2-XB3-09-02) and a grant of NNSF of China (No. 31370424) to D.Y. F. is gratefully acknowledged.

Author information

Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China

    Da-Yong Fan

  2. Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, 980-8578, Japan

    Riichi Oguchi

  3. College of Life & Environment Sciences, Shanghai Normal University, Guilin Road 100, Shanghai, 200234, China

    Weimin Ma

  4. College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China

    Jiancun Kou

  5. Division of Plant Sciences, Research School of Biology, The Australian National University, 46 Sullivans Creek Road, Acton, ACT, 2601, Australia

    Da-Yong Fan, Duncan Fitzpatrick, Riichi Oguchi, Weimin Ma, Jiancun Kou & Wah Soon Chow

Authors
  1. Da-Yong Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duncan Fitzpatrick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Riichi Oguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weimin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiancun Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wah Soon Chow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wah Soon Chow.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, DY., Fitzpatrick, D., Oguchi, R. et al. Obstacles in the quantification of the cyclic electron flux around Photosystem I in leaves of C3 plants. Photosynth Res 129, 239–251 (2016). https://doi.org/10.1007/s11120-016-0223-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0223-4

Keywords

Search

Navigation