Modeling of Chlorophyll a Fluorescence Kinetics in Plant Cells: Derivation of a Descriptive Algorithm

  • Wim Vredenberg
  • Ondřej Prášil
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 29)

In this chapter, we present the model and simulation of light-driven chlorophyll fluorescence induction in 10–20 min dark-adapted intact leaves and thylakoids. The algorithm for it has been derived from analyses of fluorescence kinetics upon excitation with single- (STF), twin- (TTF) and repetitive STF excitations. These analyses have led to definition and formulation of rate equations that describe the sequence of electron transfer steps associated with the oxidation of the oxygen evolving complex (OEC) and the reduction of the primary plastoquinone acceptor QA of photosystem II (PS II) in multi turnover excitation (MTF). The model considers heterogeneity in reaction centers (RCs) associated with the S-states of the OEC and incorporates the presence of a 20–35% fraction of QB nonreducing RCs that probably is identical with the S0 fraction. The fluorescence induction algorithm (FIA) considers a photochemical O—J—D, a photo-electrochemical J—I and an I—P component (phase), which probably is associated with a photoelectric interaction between PS I and PS II. The photochemical phase incorporates the kinetics associated with the double reduction of the acceptor pair of pheophytin (Phe) and plastoquinone QA[PheQA] in QBnonreducing RCs and the associated doubling of the variable fluorescence, in agreement with the three-state trapping model (TSTM) of PS II. Application of and results with the algorithm are illustrated for a variety of MTF-induced OJDIP curves, measured in dark-adapted leaves and thylakoids under various light and dark conditions.


Donor Side Induction Curve Excitation Rate Acceptor Pair Fluorescence Kinetic 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Antal T and Rubin A (2008) In vivo analysis of chlorophyll a fluorescence induction. Photosynth Res 96: 217–226PubMedCrossRefGoogle Scholar
  2. Belyaeva NT, Paschenko VZ, Renger G, Riznichenko G Yu and 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 (translated from Biofizika) 51 (6): 976–990Google Scholar
  3. Belyaeva NE, Schmitt F-J, Steffen, R, Paschenko VZ, Riznichenko G Yu, Chemeris YuK, Renger G, and 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: 105–119CrossRefGoogle Scholar
  4. Bernhardt K and Trissl H-W (1999) Theories for kinetics and yields of fluorescence and photochemistry: how, if at all, can different models of antenna organization be distinguished experimentally? Biochim Biophys Acta 1409: 125–142PubMedCrossRefGoogle Scholar
  5. Boisvert S, Joly D and Carpentier R (2006) Quantitative analysis of the experimental O-J-I-P chlorophyll induction kinetics. Apparent activation energy and origin of each kinetic step. FEBS Lett 273: 4770–4777Google Scholar
  6. Bowes JM and Crofts AR (1980) Binary oscillations in the rate of reoxidation of the primary acceptor of photosystem II. Biochim Biophys Acta 590: 373–384PubMedCrossRefGoogle Scholar
  7. Bukhov NG, Govindachary S, Egorova EA, Joly D and Carpentier R (2003) N, N, N′, N′-tetramethyl-p-phenylenediamine initiates the appearance of a well resolved I-peak in the kinetics of chlorophyll fluorescence rise in isolated thylakoids. Biochim Biophys Acta 1607: 91–96PubMedCrossRefGoogle Scholar
  8. Bulychev AA and Vredenberg WJ (2001) Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I. Bioelectrochem 54: 157–168CrossRefGoogle Scholar
  9. Butler WL (1972) On the primary nature of fluorescence yield changes associated with photosynthesis. Proc Natl Acad Sci USA 69: 3420–3422PubMedCrossRefGoogle Scholar
  10. Christen G, Reifarth F and Renger G (1998) On the origin of the‘35-μs kinetics’ of P+680 reduction in photosystem II with an intact water oxidizing complex. FEBS Lett 419: 49–52CrossRefGoogle Scholar
  11. Chylla RA, Garab G and Whitmarsh J (1987) Evidence for slow turnover in a fraction of photosystem II complexes in thylakoid membranes. Biochim Biophys Acta 894: 562–571CrossRefGoogle Scholar
  12. Crofts AR (2005) The Q-cycle—a personal perspective. In: Govindjee, J.T Beatty, H. Gest and J.F. Allen (eds), Discoveries in Photosynthesis. Advances in Photosynthesis and Respiration, pp 47–499, Vol. 20, Springer, DordrechtCrossRefGoogle Scholar
  13. Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60: 1–23CrossRefGoogle Scholar
  14. Duysens LNM and Sweers HE (1963) Mechanisms of the two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists. Studies on Microalgae and Photosynthetic Bacteria, pp 353–372. University of Tokyo Press, TokyoGoogle Scholar
  15. Forbush B and Kok B (1968) Reaction between primary and secondary electron acceptors of photosystem II of photosynthesis. Biochim Biophys Acta, 162: 243–253CrossRefGoogle Scholar
  16. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22: 131–160Google Scholar
  17. Govindjee (2004) Chlorophyll a fluorescence: a bit of basics and history. In: Papageorgiou, GC, Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Advances in Photosynthesis and Respiration, Vol 19, pp 1–42, Springer, DordrechtGoogle Scholar
  18. Hiraki M, Van Rensen JJS, Vredenberg WJ and Wakabayashi K (2003) Characterization of the alterations of the chlorophyll a fluorescence induction curve after addition of pho-tosystem II inhibiting herbicides. Photosynth Res 78: 35– 46PubMedCrossRefGoogle Scholar
  19. Hiraki M, Vredenberg WJ, Van Rensen JJS and Wakabayashi K (2004) A modified fluorometric method to quantify the concentration effect (pI50) of photosystem II-inhibiting herbicides. Pesticide Biochem Physiol 80: 183–191CrossRefGoogle Scholar
  20. Jablonsky J and Lazar D (2008) Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation. Biophys J 94: 2725–2736PubMedCrossRefGoogle Scholar
  21. Joliot P and Joliot A (1964) Etude cinetique de la reaction photochimique liberant l'oxygene au cours de la photo-synthèse CR Acad Sci Paris 258: 4622–4625Google Scholar
  22. Joliot P and Joliot A (1977) Evidence for a double hit process in photosystem II based on fluorescence studies. Biochim Biophys Acta 462: 559–574PubMedCrossRefGoogle Scholar
  23. Joly D and Carpentier R (2007) The oxidation/reduction kinetics in the plastoquinone pool controls the appearance of the I-peak in the O-J-I-P chlorophyll fluorescence rise: Effects of various electron acceptors. J Photochem Photo-biol B 88: 43–50CrossRefGoogle Scholar
  24. Ke B (2001) Photosynthesis photobiochemistry and photo-biophysics. In: Govindjee (ed), Advances in Photosynthesis (and Respiration), Vol. 10, Kluwer (now Springer), DordrechtGoogle Scholar
  25. Klimov VV and Krasnovskii AA (1981) Participation of pheophytin in the primary processes of electron transfer at the reaction centers of photosystem II. Biophysics 27: 186–198Google Scholar
  26. Koblizek M, Kaftan D and Nedbal L (2001) On the relationship between the non-photochemical quenching of the chlorophyll fluorescence and the photosystem II light harvesting efficiency. A repetitive flash fluorescence study. Photosynth Res 68: 141–152PubMedCrossRefGoogle Scholar
  27. Kolber Z, Prášil O and Falkowski P (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate technique. I. Defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88–106PubMedCrossRefGoogle Scholar
  28. Kramer DM, DiMarco G and Loreto F (1995) Contribution of plastoquinone quenching to saturation pulse-induced rise of chlorophyll fluorescence in leaves. In: Mathis P (ed), Photosynthesis: From Light to Biosphere, Vol. I, pp 147–150, Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  29. Kurreck J, Schödel R and Renger G (2000) Investigation of the plastoquinone pool size and fluorescence quenching in thylakoid membranes and Photosystem II (PSII) membrane fragments. Photosynth Res 63: 171–182PubMedCrossRefGoogle Scholar
  30. Lavergne J and Leci E (1993) Properties of inactive photo-system II centers. Photosynth Res 35: 323–343CrossRefGoogle Scholar
  31. 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 photo-synthetic units. Biophys J 68: 2474–2492PubMedCrossRefGoogle Scholar
  32. Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412: 1–28PubMedCrossRefGoogle Scholar
  33. Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33: 9–30CrossRefGoogle Scholar
  34. Mauzerall D (1972) Light induced fluorescence changes in Chlorella, and the primary photoreactions for the production of oxygen. Proc Natl Acad Sci USA 69: 1358– 1362PubMedCrossRefGoogle Scholar
  35. Melis A (1985) Functional properties of Photosystem IIβ in spinach chloroplasts. Biochim Biophys Acta 808: 334–342CrossRefGoogle Scholar
  36. Papageorgiou GC and Govindjee (eds) (2004) Chlorophyll a fluorescence: A signature of photosynthesis. Advances in Photosynthesis and Respiration, Vol. 19, Springer, DordrechtGoogle Scholar
  37. Papageorgiou GC, Tsimilli-Michael M and Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94: 275–290PubMedCrossRefGoogle Scholar
  38. Pospìšil P and Dau H (2002) Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients. Biochim Biophys Acta 1554: 94–100PubMedCrossRefGoogle Scholar
  39. Reifarth F, Christen G and Renger G (1997) Fluorimetric equipment for monitoring P+680 reduction in PSII preparations and green plants. Photosynth Res 51: 231–242CrossRefGoogle Scholar
  40. Roberts AG, Gregor W, Britt RD and Kramer DM (2003) Acceptor and donor-side interactions of phenolic inhibitors of Photosystem II. Biochim Biophys Acta 1604: 23–32PubMedCrossRefGoogle Scholar
  41. Samson G and Bruce D (1996) Origin of the low yield of chlorophyll fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta 1276: 147–153CrossRefGoogle Scholar
  42. Samson G, Prášil O and Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photo-synthetica 37: 163–182Google Scholar
  43. Schansker G, Toth SZ and Strasser RJ (2006) Dark recovery of the Chl a fluorescence transient (OJIP) after light adaptation: The qT-component of non-photochemical quenching is related to an activated photosystem I acceptor side. Biochim Biophys Acta 1757: 787–797PubMedCrossRefGoogle Scholar
  44. Schreiber U (2002) Assesment of maximal fluorescence yield: Donor-side dependent quenching and QB-quenching. In: Van Kooten O and J Snel (eds) Plant Spectrofluotometry: Applications and Basic Research, pp 23–47. Rozenberg, AmsterdamGoogle Scholar
  45. Schreiber U and Krieger A (1996) Hypothesis: Two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett 397: 131–135PubMedCrossRefGoogle Scholar
  46. Shinkarev VP (2004) Photosystem II: Oxygen evolution and chlorophyll a fluorescence induced by multiple flashes In: Papageorgiou GC and Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Advances in Photosynthesis and Respiration, Vol. 19, pp 197–229. Springer, DordrechtGoogle Scholar
  47. Shinkarev VP and Govindjee (1993) Insight into the relationship of chlorophyll fluorescence yield to the concentration of its natural quenchers in oxygenic photosynthesis. Proc Natl Acad Sci USA 90: 7466–7469PubMedCrossRefGoogle Scholar
  48. Steffen R (2003) Time-resolved spectroscopic investigation pf photosystem II. Ph.D. thesis. Technical University, BerlinGoogle Scholar
  49. Steffen R, Christen G and 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: 173–180PubMedCrossRefGoogle Scholar
  50. Steffen R, Eckert H-J, Kelly AA, Dörmann PG and Renger G (2005) Investigations on the reaction pattern of pho-tosystem II in leaves from Arabidopsis thaliana by time-resolved fluorometric analysis. Biochemistry 44: 3123–3132PubMedCrossRefGoogle Scholar
  51. Stirbet AD, Govindjee, Strasser BJ and Strasser, RJ (1998) Chlorophyll a fluorescence induction in higher plants: Modeling and numerical simulation. J Theor Biol 193: 131–151CrossRefGoogle Scholar
  52. Strasser BJ and Strasser RJ. (1995) Measurement of fast fluorescence transients to address environmental questions; the JIP test. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, pp 977–980, Kluwer, DordrechtGoogle Scholar
  53. Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G (ed) Chloroplast Development, pp 513–524. Elsevier/North Holland, AmsterdamGoogle Scholar
  54. Strasser RJ, Srivastava A and Govindjee (1995) Polypha-sic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61: 32–42CrossRefGoogle Scholar
  55. Strasser RJ, Tsimilli-Michael M and Srivastava, A (2004) Analysis of the fluorescence transient. In: Papageorgiou, G.C., Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in Photosynthesis and Respiration, Vol. 19, pp 321–362. Springer, DordrechtGoogle Scholar
  56. Trissl H-W (2002) Theory of fluorescence induction: an introduction. biophysik/ Trissl/teaching/teaching.html
  57. Trissl H-W and Lavergne J (1995) Fluorescence induction from photosystem II: analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units. Aust J Plant Physiol 22: 183–193CrossRefGoogle Scholar
  58. Urban O, Trtílek M, Feild T and Nedbal L (1999) Single-turnover flashes to saturate the QA reduction in a leaf were generated by the light-emitting diodes of a double modulation kinetic fluorometer. Photosynthetica 37: 201–207CrossRefGoogle Scholar
  59. Vasilév S and Bruce D (1998) Nonphotochemical quenching of excitation energy in photosystem II. A picosecond time-resolved study of the low yield of chlorophyll a fluorescence induced by single-turnover flash in isolated spinach thylakoids. Biochemistry 37: 11046–11054CrossRefGoogle Scholar
  60. Vermaas WFJ, Renger G and Dohnt G (1984) The reduction of the oxygen-evolving system in chloroplasts by thylakoid components. Biochim Biophys Acta 764: 194–202CrossRefGoogle Scholar
  61. Vredenberg WJ (2000) A three-state model for energy trapping and chlorophyll fluorescence in photosystem II incorporating radical pair recombination. Biophys J 79: 25–38CrossRefGoogle Scholar
  62. Vredenberg WJ (2004) System analysis of photoelectro-chemical control of chlorophyll fluorescence in terms of trapping models of Photosystem II: a challenging view. In: Papageorgiou GC and Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, Advances in Photosynthesis and Respiration, Vol. 19, pp 133–172. Springer, DordrechtGoogle Scholar
  63. Vredenberg WJ (2008a) Analysis of initial chlorophyll fuorescence induction kinetics in chloroplasts in terms of rate constants of donor side quenching release and electron trapping in photosystem II. Photosynth Res 96: 83–97CrossRefGoogle Scholar
  64. Vredenberg WJ (2008b) Algorithm for analysis of OJDIP fluoresecnce induction curves in terms of photo- and electrochemical events in photosystems of plant cells. Derivation and application. J Photochem Photobiol B 91: 58–65CrossRefGoogle Scholar
  65. Vredenberg WJ (2008c) Kinetic Models of Photosystem II should incorporate a Role for QB-nonreducing Reaction Centers. Biophys J 95: 3113–3114CrossRefGoogle Scholar
  66. Vredenberg WJ and Duysens LNM (1963) Transfer and trapping of excitation energy from bacteriochlorophyll to a reaction center during bacterial photosynthesis. Nature 197: 355–357PubMedCrossRefGoogle Scholar
  67. Vredenberg WJ, Snel JFH and Dassen JHA (1998) A sizeable increase in the electric conductance of the thylakoid lumen as an early event during reaction center and Q cycle turnover Photosynth Res 58: 111–121Google Scholar
  68. Vredenberg WJ, Rodrigues GC and Van Rensen JJS (2002) A quantitative analysis of the chlorophyll fluorescence induction in terms of electron transfer rates at donor and acceptor sides of photosystem II. In: Proceedings of the 12th International Congress Photosynthesis, Brisbane, 18–23 August, 2001 S14–10 (on CD)Google Scholar
  69. Vredenberg WJ, Van Rensen JJS and Rodrigues GC (2005) On the sub-maximal yield and photo-electric stimulation of chlorophyll a fluorescence in single turnover excitations in plant cells. Bioelectrochemistry 68: 83–90Google Scholar
  70. Vredenberg WJ, Kasalicky V, Durchan M and Prášil O (2006) The chlorophyll a fluorescence induction pattern in chloroplasts upon repetitive single turnover excitations: Accumulation and function of QB-nonreducing centers. Biochim Biophys Acta 1757: 173–181PubMedCrossRefGoogle Scholar
  71. Vredenberg WJ, Durchan M and Prášil O (2007) On the chlorophyll fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains. Photosynth Res 93: 183–192PubMedCrossRefGoogle Scholar
  72. Walas SM (1991) Modeling with differential equations in chemical engineering, Butterworth-Heinemann, Boston, MAGoogle Scholar
  73. Zhu X-G, Govindjee, Baker NR, deSturler E, Ort D and 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 23: 114–133CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Wim Vredenberg
    • 1
  • Ondřej Prášil
    • 2
  1. 1.Department of Plant PhysiologyWageningen University and Research CentreWageningenThe Netherlands
  2. 2.Laboratory of Photosynthesis, Institute of MicrobiologyAcademy of Sciences Czech RepublicTřeboňCzech Republic

Personalised recommendations