SpringerLink
Log in

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

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The set up described in Steffen et al. (Biochemistry 40:173–180, 2001) was used to monitor in the time domain from 100 ns to 10 s single turnover flash-induced transients of the normalized fluorescence yield (SFITFY) on dark-adapted cells of the thermophilic algae Chlorella pyrenoidosa Chick. Perfect data fit was achieved within the framework of a previously proposed model for the PS II reaction pattern (Lebedeva et al., Biophysics 47:968–980, 2002; Belyaeva et al., Biophysics 51:860–872, 2006) after its modification by taking into account nonradiative decay processes including nonphotochemical quenching due to time-dependent populations of P680+• and 3Car. On the basis of data reported in the literature, a consistent set of rate constants was obtained for electron transfer at the donor and acceptor sides of PS II, pH in lumen and stroma, the initial redox state of plastoquinone pool and the rate of plastoquinone oxidation. The evaluation of the rate constant values of dissipative processes due to quenching by carotenoid triplets in antennae and P680+•QA −• recombination as well as the initial state populations after excitation with a single laser flash are close to that outlined in (Steffen et al., Biochemistry 44:3123–3133, 2005a). The simulations based on the model of the PS II reaction pattern provide information on the time courses of population probabilities of different PS II states. We analyzed the maximum (\( F_{\text{m}}^{\text{STF}} \)) and minimum (F 0) of the normalized FL yield dependence on the rate of the recombination processes (radiative and dissipative nonradiative) and of P680+• reduction. The developed PS II model provides a basis for theoretical comparative analyses of time-dependent fluorescence signals, observed at different photosynthetic samples under various conditions (e.g. presence of herbicides, other stress conditions, excitation with actinic pulses of different intensity, and duration).

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Chl:

Chlorophyll

PS II:

Photosystem II

RC:

Reaction center of PS II

P680:

Photoactive pigment of the RC of PS II

Phe:

Primary electron acceptor pheophytin

QA and QB :

Primary and secondary quinone electron acceptors of PS II

3Car:

Triplet carotenoid states

WOC:

Water-oxidizing complex

PQ:

Plastoquinone

PQH2 :

Plastoquinol

HL + :

Protons in lumen

HS + :

Protons in stroma

YZ :

Tyrosine 161 of the PS II D1 polypeptide

S i :

Redox states of the WOC

ΔΨ:

Electric potential across the thylakoid membrane

ET:

Electron transfer

FL, FL(t):

Fluorescence

k L :

Rate constant of light excitation

\( k_{{{\text{P}}680^{ + } }} ,\;k_{{3_{\text{Car}} }} \) :

Rate constants of quenching: by cation radical P680+• by triplet carotenoids

k F :

Rate constant of fluorescence emission

k HD :

Rate constant of heat dissipation of Chl excitation

k Z :

Rate constant of the electron donation to the oxidized P680+•

k CL :

Rate constant of the charge separation for closed RCs

LED:

Light-emitting diode

SFITFY:

Single flash-induced transient of fluorescence yield

PPFD:

Photosynthetic photon flux density

\( F_{0} ,F_{\text{m}}^{\text{STF}} \) :

Minimal maximal FL yield

References

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

    CAS  Google Scholar 

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

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

    Google Scholar 

  • Belyaeva NE, Pashchenko VZ, Renger G, Riznichenko GY, Rubin AB (2006) Application of a 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 51:860–872

    Article  Google Scholar 

  • Bernarding J, Eckert HJ, Eichler HJ, Napiwotzki A, Renger G (1994) Kinetic studies on the stabilization of the primary radical pair P680+ Pheo− in different photosystem II preparations from higher plants. Photochem Photobiol 59:566–573

    Article  CAS  Google Scholar 

  • Bergmann A, Eichler HJ, Eckert HJ, Renger G (1998) Picosecond laser-fluorometer with simultaneous time- and wavelength resolution for monitoring decay spectra of photoinhibited photosystem II particles at 277 K and 10 K. Photosynth Res 58:305–312

    Article  Google Scholar 

  • Brettel K, Schlodder E, Witt HT (1984) Nanosecond reduction kinetics of photooxidized chlorophyll-a II (P–680) in single flashes as a probe for the electron pathway, H+-release and charge accumulation in the O2-evolving complex. Biochim Biophys Acta 766:403–415

    Article  CAS  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  PubMed  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. Biolog Membr 4:262–269

    CAS  Google Scholar 

  • Chemeris YuK, Korol’kov NS, Seifullina NKh, Rubin AB (2004) PSII complexes with destabilized primary quinone acceptor of electrons in dark-adapted chlorella. Russ J Plant Physiol 51:9–14

    Article  CAS  Google Scholar 

  • Christen G, Seeliger A, Renger G (1999) P680•+ reduction kinetics and redox transition probability of the water oxidizing complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry 38:6082–6092

    Article  PubMed  CAS  Google Scholar 

  • Christen G, Steffen R, Renger G (2000) Delayed fluorescence emitted from light harvesting complex II and photosystem II of higher plants in the 100 ns–5μs time domain. FEBS Lett 475:103–106

    Article  PubMed  CAS  Google Scholar 

  • Crofts AR, Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185

    CAS  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  PubMed  CAS  Google Scholar 

  • Dau H (1994) Short-term adaptation of plants to changing light intensities and its relation to photosystem II photochemistry and fluorescence emission. J Photochem Photobiol B Biol 26:3–27

    Article  CAS  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 

  • Eckert H-J, Renger G (1988) Temperature-dependence of P680+ reduction in O2-evolving PS-II membrane-fragments at different redox states Si of the water oxidizing system. FEBS Lett 236:425–431

    Article  CAS  Google Scholar 

  • Gibasiewicz K, Dobek A, Breton J, Leibl W (2001) Modulation of primary radical pair kinetics and energetics in photosystem II by the redox state of the quinone electron acceptor QA. Biophys J 80:1617–1630

    PubMed  CAS  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 Aug 2004. http://www.insysbio.ru

  • Goh C-H, Schreiber U, Hedrich R (1999) New approach of monitoring changes in chlorophyll a fluorescence of single guard cells and protoplasts in response to physiological stimuli. Plant Cell Environ 22:1057–1070

    Article  CAS  Google Scholar 

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

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

    Article  CAS  Google Scholar 

  • Ireland CR, Long SP, Baker NR (1984) The relationship between carbon dioxide fixation and chlorophyll a fluorescence during induction of photosynthesis in maize leaves at different temperatures and carbon dioxide concentration. Planta 160:550–558

    Article  CAS  Google Scholar 

  • Kamali J, Lebedeva GV, Demin OV, Belyaeva NE, Riznichenko GYu, Rubin AB (2004) Kinetic model of cytochrome bf complex. Fitting of model parameters to experimental data. Biofizika (Russ) 49:1061–1068

    CAS  Google Scholar 

  • Karavaev VA, Kukushkin AK (1993) Theoretical model of light and dark processes of photosynthesis: the problem of regulation. Biophysics 38:987–1003

    Google Scholar 

  • Kern J, Renger G (2007) Photosystem II: structure and mechanism of the water:plastoquinone oxidoreductase. Photosynth Res 94:183–202

    Article  PubMed  CAS  Google Scholar 

  • Kühn P, Eckert HJ, Eichler HJ, Renger G (2004) Analysis of the P680+· reduction pattern and its temperature dependence in oxygen evolving PS II core complexes from thermophilic cyanobacteria and higher plants. Phys Chem Chem Phys 6:4838–4843

    Article  CAS  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

    PubMed  CAS  Google Scholar 

  • Laisk A, Walker DA (1989) A mathematical model of electron transport. Thermodynamic necessity for photosystem II regulation. Proc R Soc Lond B237:417–444

    Google Scholar 

  • Lavergne J, Trissl HW (1995) Theory of fluorescence induction in photosystem II. Biophys J 68:2474–2492

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Lazar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30

    Article  CAS  Google Scholar 

  • Lebedeva GV, Belyaeva NE, Riznichenko GYu, 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 GYu, 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 trap** and charge stabilization in oriented PS II membranes. Photosynth Res 22:257–275

    Article  CAS  Google Scholar 

  • Messinger J, Renger G (1993) Generation, oxidation by YD ox and possible electronic configuration of the redox states S0, S−1 and S−2 of the water oxidase in isolated spinach thylakoids. Biochemistry 32:9379–9386

    Article  PubMed  CAS  Google Scholar 

  • Messinger J, Renger G (2008) Photosynthetic water splitting. In: Renger G (ed) Primary processes of photosynthesis: basic principles and apparatus, vol II: reaction centers/photosystems. Electron transport chains, photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 295–352

    Google Scholar 

  • Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: I. Saturation characteristics and partial control by the photosystem II acceptor side. Z Naturforsch C 42:1246–1254

    CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Berlin

    Google Scholar 

  • Rappaport F, Cuni A, **ong L, Sayre R, Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88:1948–1958

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2001) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503:210–228

    Article  PubMed  CAS  Google Scholar 

  • Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 139–175

    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 trap** 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  PubMed  CAS  Google Scholar 

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

    Article  CAS  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

    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

    CAS  PubMed  Google Scholar 

  • Schödel R, Irrgang KD, Voigt J, Renger G (1998) Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys J 75:3143–3153

    PubMed  Google Scholar 

  • Schödel R, Irrgang KD, Voigt J, Renger G (1999) Quenching of chlorophyll fluorescence by triplets in solubilized light-harvesting complex II (LHCII). Biophys J 76:2238–2248

    PubMed  Google Scholar 

  • Schreiber U, Krieger A (1996) Two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett 397:131–135

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shuvalov VA, Klimov VV, Dolan E, Parson WW, Ke B (1980) Nanosecond fluorescence and absorbance changes in photosystem II at low redox potential. FEBS Lett 118:279–282

    Article  CAS  Google Scholar 

  • Steffen R (2003) Time-resolved spectroscopic investigations of photosystem II. PhD thesis, Berlin

  • Steffen R, Christen G, Renger G (2001) Time-resolved monitoring of flash-induced changes of fluorescence quantum yield and decay of delayed light emission in oxygen-evolving photosynthetic organisms. Biochemistry 40:173–180

    Article  PubMed  CAS  Google Scholar 

  • Steffen R, Eckert HJ, Kelly AA, Dormann P, Renger G (2005a) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana by time-resolved fluorometric analysis. Biochemistry 44:3123–3133

    Article  PubMed  CAS  Google Scholar 

  • Steffen R, Kelly AA, Huyer J, Doermann P, Renger G (2005b) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44:3134–3142

    Article  PubMed  CAS  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 

  • Strasser RJ, Srivastava A, Govindgee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

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

  • Toth SZ, Schansker G, Strasser RJ (2005) In intact leaves, the maximum fluorescence level (FM) is independent of the redox state of the plastoquinone pool: a DCMU inhibition study. Biochim Biophys Acta 1708:275–282

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Vasil’ev S, Bergmann A, Redlin H, Eichler HJ, Renger G (1996) On the role of exchangeable hydrogen bonds for the kinetics of P680+QA − formation and P680+Pheo− recombination in photosystem II. Biochim Biophys Acta 1276:35–44

    Article  Google Scholar 

  • Vermaas WCJ, Renger G, Dohnt G (1984) The reduction of the oxygen-evolving system in chloroplasts by thylakoid components. Biochim Biophys Acta 764:194–202

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vredenberg WJ, Bulychev AA (2003) Photoelectric effects on chlorophyll fluorescence of photosystem II in vivo. Kinetic in the absence and presence of valinomycin. Bioelectrochemistry 60:87–95

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. A. A. Bulychev for the fruitful discussions, Dr. O. V. Demin for DBsolve software: version 7.01 (demin@genebee.msu.su). This work was supported by the Russian Foundation for Basic Research, project nos. 07-04-00375, 05-04-48912, 08-04-01112, by the International Bureau of BMBF, Germany, project RUS 06/003, and by Deutsche Forschungsgemeinschaft (SfB 429).

Author information

Authors and Affiliations

  1. Department of Biophysics, Biology Faculty of the M.V. Lomonosov Moscow State University, 119992, Moscow, Russia

    N. E. Belyaeva, V. Z. Paschenko, G. Yu. Riznichenko, Yu. K. Chemeris & A. B. Rubin

  2. Max-Volmer Laboratory, Institute of Optics and Atomic Physics, Berlin Institute of Technology, 10623, Berlin, Germany

    F.-J. Schmitt, R. Steffen & G. Renger

Authors
  1. N. E. Belyaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F.-J. Schmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Steffen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Z. Paschenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Yu. Riznichenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu. K. Chemeris
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Renger
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. B. Rubin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. E. Belyaeva.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belyaeva, N.E., Schmitt, FJ., Steffen, R. et al. 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 (2008). https://doi.org/10.1007/s11120-008-9374-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-008-9374-2

Keywords

Search

Navigation