Skip to main content
Log in

Thylakoid membrane model of the Chl a fluorescence transient and P700 induction kinetics in plant leaves

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

A new Thylakoid model is presented, which describes in detail the electron/proton transfer reactions between membrane protein complexes including photosystems II and I (PSII, PSI), cytochrome (Cyt) b 6 f, mobile plastoquinone PQ pool in the thylakoid membrane, plastocyanin in lumen and ferredoxin in stroma, reduction of NADP via FNR and cyclic electron transfer. The Thylakoid model parameters were fitted both to Chl fluorescence induction data (FI) and oxido-reductions of P700 (ΔA 810) measured from 20 μs up to 20 s in pea leaves. The two-wave kinetics of FI and ΔA 810 (O(JI)PSM and OABCDE) were described quantitatively, provided that the values of membrane electrochemical potential components ΔΨ(t), pHL(t)/pHS(t) are in physiologically relevant ranges. The time courses on the time scale from nanoseconds to tens of seconds of oxido-reduction changes of ET components as well as concentrations of proton/ions (K+, Cl) were calculated. We assume a low constant FNR activity over this period. Charge movements across the thylakoid membrane by passive leakage and active ATPase transport and proton buffer reactions are simulated. The dynamics of charge fluxes during photosynthetic induction under low light (PFD 200 μmol photons m−2 s−1) were analyzed. The initial wave of P700 oxidation within 20 ms during independent operation of PSI and PSII was followed after 50 ms by PSI donor-side reduction from reduced PQ pool via Cyt b 6 f site. The Cyt b 6 f reactions contribute to the stabilization of fluxes in the time range 1 s < t < 10 s. The detailed analysis of Chl a fluorescence at the PSM stage (t > 10 s) would need the investigation of FNR activation effect in order to explain the transitions between cyclic and linear electron transport.

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

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

Cyt b 6 f :

Cytochrome b 6 f complex

EET:

Excitation energy transfer

ET:

Electron transfer

ETC:

Electron transport chain

Fd:

Ferredoxin

FL:

Fluorescence

FNR:

Ferredoxin-NADP+-oxidoreductase

F0 :

Minimal chlorophyll fluorescence yield

Fm :

Maximal chlorophyll fluorescence yield induced by multi-turnover light

H +L , H +S :

Protons in lumen, in stroma

NADP+ :

Nicotinamide adenine dinucleotide phosphate, oxidized form

PFD:

Photon flux density

Phe, Ph:

Primary PSII electron acceptor, pheophytin

pHL, pHS :

pH in lumen, in stroma

PQ:

Plastoquinone

PQH2 :

Plastoquinol

PS II, PS I:

Photosystems II, I

PT:

Proton transfer

P680, P680 :

Chlorophyll a acting as electron donor in PSII

P700:

Chlorophyll a acting as electron donor in PSI

QA and QB :

Primary and secondary plastoquinone electron acceptors of PSII

RC:

Reaction center (of PS II)

WOC:

Water-oxidizing complex

YZ :

Tyrosine 161 of the PS II D1 polypeptide

ΔΨ:

Electrical potential across the thylakoid membrane

References

  • Baake E, Schlöder JP (1992) Modelling the fast fluorescence rise of photosynthesis. Bull Math Biol 54:999–1021

    Article  CAS  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  Google Scholar 

  • Belyaeva NE (2004) Generalized model of primary photosynthetic processes in chloroplasts. Ph.D. thesis, Moscow

  • Belyaeva NE, Lebedeva GV, Riznichenko GY (2003) Kinetic model of primary photosynthetic processes in chloroplasts. Modeling of thylakoid membranes electric potential. In: Riznichenko GY (ed) Mathematics computer education, vol 10. Progress-Traditsiya, Moscow, pp 263–276 (Russian)

    Google Scholar 

  • Belyaeva NE, Paschenko VZ, Renger G, Riznichenko GY, Rubin AB (2006) Application of photosystem II model for analysis of fluorescence induction curves in the 100 ns to 10 s time domain after excitation with a saturating light pulse. Biophysics 51(6):860–872

    Article  Google Scholar 

  • Belyaeva NE, Schmitt F-J, Steffen R, Paschenko VZ, Riznichenko GY, Chemeris YuK, Renger G, Rubin AB (2008) PS II model-based simulations of single turnover flash-induced transients of fluorescence yield monitored within the time domain of 100 ns–10 s on dark-adapted Chlorella pyrenoidosa cells. Photosynth Res 98:105–119

    Article  CAS  PubMed  Google Scholar 

  • Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB, Renger G (2011a) PS II model based analysis of transient fluorescence yield measured on whole leaves of Arabidopsis thaliana after excitation with light flashes of different energies. BioSystems 103(2):188–195

    Article  CAS  PubMed  Google Scholar 

  • Belyaeva NE, Bulychev AA, Riznichenko GY, Rubin AB (2011b) A model of photosystem II for the analysis of fast fluorescence rise in plant leaves. Biophysics 56(3):464–477

    Article  Google Scholar 

  • Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB, Renger G (2014) Model based analysis of transient fluorescence yield induced by actinic laser flashes in spinach leaves and cells of green alga Chlorella pyrenoidosa Chick. Plant Physiol Biochem 77:49–59

    Article  CAS  PubMed  Google Scholar 

  • Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB (2015) Modelling of the redox state dynamics in photosystem II of Chlorella pyrenoidosa Chick cells and leaves of spinach and Arabidopsis thaliana from single flash induced fluorescence quantum yield changes on the 100 ns–10 s time scale. Photosynth Res 125:123–140

    Article  CAS  PubMed  Google Scholar 

  • Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell, Oxford

    Book  Google Scholar 

  • Boork J, Wennerstrцm H (1984) The influence of membrane potentials on reaction rates. Control in free-energy transducing systems. Biochim Biophys Acta 767(2):314–320

    Article  CAS  PubMed  Google Scholar 

  • Bowes JM, Crofts AR (1980) Binary oscillations in the rate of reoxidation of the primary acceptor of Photosystem II. Biochim Biophys Acta 590:373–384

    Article  CAS  PubMed  Google Scholar 

  • Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318(3):322–373

    Article  CAS  Google Scholar 

  • Bulychev AA (1984) Different kinetics of membrane potential formation in dark-adapted and preilluminated chloroplasts. Biochim Biophys Acta 766(3):647–652

    Article  CAS  Google Scholar 

  • Bulychev AA (2011) Induction changes in photosystems I and II in plant leaves upon modulation of membrane ion transport. Biochem (Mosc) Suppl Ser A Membr Cell Biol 5:335–342

    Article  Google Scholar 

  • Bulychev AA, Vredenberg WJ (1999) Light-triggered electrical events in the thylakoid membrane of plant chloroplast. Physiol Plant 105:577–584

    Article  CAS  Google Scholar 

  • Bulychev AA, Vredenberg WJ (2001) Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I. Bioelectrochemistry 54:157–168

    Article  CAS  PubMed  Google Scholar 

  • Bulychev AA, Niyazova MM, Turovetsky VB (1986) Electro-induced changes of chlorophyll fluorescence in individual intact chloroplasts. Biochim Biophys Acta 850:218–225

    Article  CAS  Google Scholar 

  • Bulychev AA, Niyazova MM, Rubin AB (1987) Fluorescence changes of chloroplasts caused by the shifts of membrane-potential and their dependence on the redox state of the acceptor of photosystem II. Biol Membr 4:262–269

    CAS  Google Scholar 

  • Bulychev AA, Cherkashin AA, Rubin AB (2010) Dependence of chlorophyll P700 redox transients during the induction period on the transmembrane distribution of protons in chloroplasts of pea leaves. Rus J Plant Physiol 57(1):20–27

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Carrillo N, Ceccarelli EA (2003) Open questions in ferredoxin-NADP+ reductase catalytic mechanism. Eur J Biochem 270:1900–1915

    Article  CAS  PubMed  Google Scholar 

  • Carrillo N, Lucero H, Vallejos RH (1981) Light modulation of chloroplast membrane-bound ferredoxin-NADP+ oxidoreductase. J Biol Chem 256:1058–1059

    CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Cruz JA, Kanazawa A, Treff N, Kramer DM (2005) 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

    Article  CAS  PubMed  Google Scholar 

  • Dau H (1994) Molecular mechanism and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23

    Article  CAS  Google Scholar 

  • Dau H, Sauer K (1991) Electric field effect on chlorophyll fluorescence and its relation to photosystem II charge separation reactions studied by a salt jump technique. Biochim Biophys Acta 1089:49–60

    Article  Google Scholar 

  • Dau H, Sauer K (1992) Electric field effect on the picosecond fluorescence of photosystem II and its relation to the energetics and kinetics of primary charge separation. Biochim Biophys Acta 1102:91–106

    Article  CAS  Google Scholar 

  • de Wijn R, van Gorkom HJ (2001) Kinetics of electron transfer from Q(a) to Q(b) in photosystem II. Biochemistry 40:11912–11922

    Article  PubMed  CAS  Google Scholar 

  • Demin OV, Westerhoff HV, Kholodenko BN (1998) Mathematical modeling of superoxide generation with the bc 1 complex of mitochondria. Biochemistry (Moscow) 6:634–649

    Google Scholar 

  • Ebenhöh O, Houwaart T, Lokstein H, Schlede S, Tirok K (2011) A minimal mathematical model of nonphotochemical quenching of chlorophyll fluorescence. Biosystems 103(2):196–204 http://www.sciencedirect.com/science/article/pii/S0303264710001851-cor0005mailto:ebenhoeh@abdn.ac.uk

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gizzatkulov N, Klimov A, Lebedeva G, Demin O (2004) DBsolve7: New update version to develop and analyze models of complex biological systems. ISMB/ECCB conference, Glasgow, Scotland, UK, 31 July–5 August 2004. http://www.insysbio.ru

  • Govindjee (ed) (1982) Photosynthesis, vol 2. Academic Press, New York

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Govindjee (2004) Chlorophyll a fluorescence: A bit of basics and history. In: Papageorgiou GC, Govindjee G (eds) Chlorophyll fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 1–42

    Chapter  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Haumann M, Mulkidjanian AY, Junge W (1997) The electrogenicities of electron and proton transfer at the oxidizing side of photosystem II. Biochemistry 36:9304–9315

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hope AB (1993) The chloroplast cytochrome bf complex: a critical focus on function. Biochim Biophys Acta 1143:1–22

    Article  CAS  PubMed  Google Scholar 

  • Hope AB, Huilgol RR, Panizza M, Thomson M, Matthews DB (1992) The flash-induced turnover of cytochrome b-563, cytochrome f and plastocyanin in chloroplasts. Models and estimation of kinetic parameters. Biochim Biophys Acta 1100:15–26

    Article  CAS  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. PNAS 99:10209–10214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Junge W, Auslander W, McGeer A, Runge T (1979) The buffering capacity of the internal phase of thylakoids and the magnitude of the pH changes inside under flashing light. Biochim Biophys Acta 546:121–141

    Article  CAS  PubMed  Google Scholar 

  • Kamali MJ, Lebedeva GV, Demin OV, Beljaeva NE, Riznichenko GY, Rubin AB (2004) A kinetic model of the cytochrome bf complex with fitted parameters. Biophysics 49:1061–1068

    CAS  Google Scholar 

  • Kholodenko BN (1988) Stabilizing regulation on multienzyme systems: modeling of bioenergetic processes. Doktoral (Phys-Math) Dissertation, Moscow, Belozersky Institute of Physico-Chemical Biology, MSU

  • Klughammer C, Schreiber U (2016) Deconvolution of ferredoxin, plastocyanin, and P700 transmittance changes in intact leaves with a new type of kinetic LED array spectrophotometer. Photosynth Res. doi:10.1007/s11120-016-0219-0

    PubMed  PubMed Central  Google Scholar 

  • Kodru S, Malavath T, Devadasu E, Nellaepalli S, Stirbet A, Subramanyam R, Govindjee (2015) The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231

    Article  CAS  PubMed  Google Scholar 

  • Krab K, van Walraven HS, Scholts MJS, Kraayenhof R (1985) Measurement of diffusion potential in liposomes. Origin and properties of the threshold level in the oxonol VI response. Biochim Biophys Acta 809:228–235

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Krieger A, Moya I, Weis E (1992) Energy-dependent quenching of chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem preparations. Biochim Biophvs Acta 102:167–176

    Article  Google Scholar 

  • Kroon BMA, Thoms S (2006) From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. J Phycol 42:593–609

    Article  CAS  Google Scholar 

  • Kuvykin IV, Ptushenko VV, Vershubskii AV, Tikhonov AN (2011) Regulation of electron transport in C(3) plant chloroplasts in situ and in silico: short-term effects of atmospheric CO(2) and O(2). Biochim Biophys Acta 1807(3):336–347

    Article  CAS  PubMed  Google Scholar 

  • Laible PD, Zipfel W, Owens TG (1994) Excited state dynamics in chlorophyll-based antennae: the role of transfer equilibrium. Biophys J 66:844–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laisk A, Walker DA (1989) A mathematical model of electron transport. Thermodynamic necessity for photosystem II regulation. Proc R Soc London B 237:417–444

    Article  CAS  Google Scholar 

  • Laisk A, Eichelmann H, Oja V (2006) C3 photosynthesis in silico. Photosynth Res 90:45–66

    Article  CAS  PubMed  Google Scholar 

  • Läuger P (1984) Thermodynamic and kinetic properties of electrogenic ion pumps. Biochim Biophys Acta 779(3):307–341

    Article  PubMed  Google Scholar 

  • Lazár 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

    Article  PubMed  CAS  Google Scholar 

  • Lazár D (2009) Modelling of light-induced chlorophyll a fluorescence rise (O–J–I–P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47(4):483–498

    Article  CAS  Google Scholar 

  • Lazár 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  PubMed  CAS  Google Scholar 

  • Lazár D, Nauš J, Matoušková M, Flašarová M (1997) Mathematical modeling of changes in chlorophyll fluorescence induction caused by herbicides. Pestic Biochem Physiol 57:200–210

    Article  Google Scholar 

  • Lebedeva GV, Beljaeva NE, Riznichenko GY, Demin OV (1998) Modelling of the primary events of photosynthesis and the fast phase of fluorescence induction. In: Larsson C, Pahlman I, Gustafsson L (eds) BioThermoKinetics in the post genomic era. Chalmers Reproservice, Goteborg, pp 196–199

    Google Scholar 

  • Lebedeva GV, Belyaeva NE, Riznichenko GY, Rubin AB, Demin OV (2000) Kinetic model of photosystem II of higher green plants. Russ J Phys Chem 74:1702–1710

    Google Scholar 

  • Lebedeva GV, Belyaeva NE, Demin OV, Riznichenko GY, Rubin AB (2002) Kinetic model of primary photosynthetic processes in chloroplasts. Description of the fast phase of chlorophyll fluorescence induction under different light intensities. Biophysics 47:968–980

    Google Scholar 

  • Leibl W, Breton J, Deprez J, Trissl HW (1989) Photoelectric study on the kinetics of trapping and charge stabilization in oriented PS II membranes. Photosynth Res 22:257–275

    Article  CAS  PubMed  Google Scholar 

  • Mamedov M, Govindjee, Nadtochenko V, Semenov A (2015) Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms. Photosynth Res 125:51–63

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht

    Google Scholar 

  • Papageorgiou GC, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94:275–290

    Article  CAS  PubMed  Google Scholar 

  • Pottossin II, Schönknecht G (1996) Ion channel permeable for divalent and monovalent cations in native spinach thylakoid membranes. J Membr Biol 152:223–233

    Article  Google Scholar 

  • Renger G (2004) Coupling of electron and proton transfer in oxidative water cleavage in photosynthesis. Biochim Biophys Acta 1655:195–204

    Article  CAS  PubMed  Google Scholar 

  • Renger G (2007) Oxidative photosynthetic water splitting: energetics, kinetics and mechanism. Photosynth Res 92:407–425

    Article  CAS  PubMed  Google Scholar 

  • Renger G (2012) Mechanism of light induced water splitting. In Photosystem II of oxygen evolving photosynthetic organisms. Biochim Biophys Acta 1817:1164–1176

    Article  CAS  PubMed  Google Scholar 

  • Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Berlin, pp 139–175

    Google Scholar 

  • Renger T, Schlodder E (2010) Primary photophysical processes in photosystem II: bridging the gap between crystal structure and optical spectra. Chem Phys Chem 11:1141–1153

    CAS  PubMed  Google Scholar 

  • Renger G, Schulze A (1985) Quantitative analysis of fluorescence induction curves in isolated spinach chloroplasts. Photobiochem Photobiophys 9:79–87

    CAS  Google Scholar 

  • Renger G, Eckert HJ, Bergmann A, Bernarding J, Liu B, Napiwotzki A, Reifarth F, Eichler HJ (1995) Fluorescence and spectroscopic studies on exciton trapping and electron transfer in photosystem II of higher plants. Aust J Plant Physiol 22:167–181

    Article  CAS  Google Scholar 

  • Reynolds IA, Johnson EA, Tanford C (1985) Incorporation of membrane potential into theoretical analysis of electrogenic ion pumps. Proc Natl Acad Sci USA 82:6869–6873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rich PR (1988) A critical examination of the supposed variable proton stoichiometry of the chloroplast cytochrome b/f complex. Biochim Biophys Acta 932:33–42

    Article  CAS  Google Scholar 

  • Riznichenko GY, Lebedeva GV, Demin OV, Rubin AB (1999) Kinetic mechanisms of biological regulation in photosynthetic organisms. J Biol Phys 25:177–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roelofs TA, Lee CH, Holzwarth AR (1992) Global target analysis of picosecond chlorophyll fluorescence kinetic from pea chloroplasts. Biophys J 61:1147–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero E, Augulis R, Novoderezjkin VI, Ferretti M, Thieme J, Zigmantas D, van Grondelle R (2014) Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat Phys. doi:10.1038/NPHYS3017

    PubMed  PubMed Central  Google Scholar 

  • Rubin A, Riznichenko GY (2009) Modeling of the primary processes in a photosynthetic membrane. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems, advances in photosynthesis and respiration, vol 29. Springer, Dordrecht, pp 151–176

    Chapter  Google Scholar 

  • Samson G, Bruce D (1996) Origins of the low yield of chlorophyll fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta 1276:147–153

    Article  Google Scholar 

  • Satoh K (1982) Mechanism of photoactivation of electron transport in intact Bryopsis chloroplasts. Plant Physiol 70:1413–1416

    Article  CAS  PubMed  PubMed Central  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 

  • Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromorhymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261

    Article  CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, Strasser RJ (2006) Dark-recovery of the Chl a fluorescence transient (OJIP) after light adaptation: The qTcomponent of non-photochemical quenching is related to an activated photosystem I acceptor side. Biochim Biophys Acta 1757:787–797

    Article  CAS  PubMed  Google Scholar 

  • Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheibe R, Stitt MN (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and 02 evolution in spinach leaves. Plant Physiol Biochem 26:473–481

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Semenov AYu, Cherepanov DA, Mamedov MD (2008) Electrogenic reactions and dielectric properties of photosystem II. Photosynth Res 98:121–130

    Article  CAS  PubMed  Google Scholar 

  • Shevela D, Eaton-Rye JJ, Shen J-R, Govindjee (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta 1817:1134–1151

    Article  CAS  PubMed  Google Scholar 

  • Steffen R, Eckert H-J, Kelly AA, Dörmann PG, Renger G (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana by time-resolved fluorometric analysis. Biochemistry 44:3123–3132

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee, Strasser BJ, Strasser RJ (1998) Chlorophyll a fluorescence induction in higher plants: modeling and numerical simulation. J Theor Biol 193:131–151

    Article  CAS  Google Scholar 

  • Stirbet AD, Rosenau Ph, Ströder AC, Strasser RJ (2001) Parameter optimisation of fast chlorophyll fluorescence induction model. Math Comput Simul 56:443–450

    Article  Google Scholar 

  • Stirbet A, Riznichenko GY, Rubin AB, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow) 79:291–323

    Article  CAS  Google Scholar 

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

    Chapter  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    Article  CAS  PubMed  Google Scholar 

  • Talts E, Oja V, Rämma H, Rasulov B, Anijalg A, Laisk A (2007) Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under far-red light in sunflower leaves. Photosynth Res 94:109–120

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Blatt MR (1989) Direct measurement of K+ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol 91:249–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183

    Article  CAS  PubMed  Google Scholar 

  • Tikhonov AN (2015) Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynth Res 125:65–94

    Article  CAS  PubMed  Google Scholar 

  • van Kooten O, Snel JFH, Vredenberg WJ (1986) Photosynthetic free energy transduction to the electric potential changes across the thylakoid membrane. Photosynth Res 9:211–227

    Article  PubMed  Google Scholar 

  • Vredenberg WJ (2000) A 3-state model for energy trapping and fluorescence in PS II incorporating radical pair recombination. Biophys J 79:26–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vredenberg WJ (2011) Kinetic analysis and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. BioSystems 103:139–151

    Article  CAS  Google Scholar 

  • Walz D, Goldstein L, Avron M (1974) Determination and analysis of the buffer capacity of isolated chloroplasts in the light and in the dark. Eur J Biochem 47:403–407

    Article  CAS  PubMed  Google Scholar 

  • Zhu XG, Govindjee, Baker NR, deSturler E, Ort DR, Long SP (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II. Planta 223:114–133

    Article  CAS  PubMed  Google Scholar 

  • Zhu XG, Wang Y, Ort DR, Long SP (2013) e-photosynthesis: a comprehensive dynamic mechanistic model of C3 photosynthesis: from light capture to sucrose synthesis. Plant, Cell Environ 36:1711–1727

    Article  CAS  Google Scholar 

  • Zwolinski BJ, Eyring H, Reese CE (1949) Diffusion and membrane permeability. J Phys Chem 53:1426–1453

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the RFBR, Projects nos. 14-04-01536, 16-04-00318. The authors thank our reviewers for their very useful comments, which helped us to improve the manuscript. We are especially grateful to Dr. Alexandrina Stirbet for important recommendations concerning the model description in our paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. E. Belyaeva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 222 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Belyaeva, N.E., Bulychev, A.A., Riznichenko, G.Y. et al. Thylakoid membrane model of the Chl a fluorescence transient and P700 induction kinetics in plant leaves. Photosynth Res 130, 491–515 (2016). https://doi.org/10.1007/s11120-016-0289-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0289-z

Keywords

Navigation