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Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis

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Photosynthetica

Abstract

Theoretical modelling is often overlooked in photosynthesis research even if it can significantly help with understanding of explored system. A new model of light-induced photosynthetic reactions occurring in and around thylakoid membrane is introduced here and used for theoretical modelling of not only the light-induced chlorophyll (Chl) a fluorescence rise (FLR; the O-J-I-P transient), reflecting function of photosystem II (PSII), but also of the 820 nmtransmittance signal (I820), reflecting function of photosystem I (PSI) and plastocyanin (PC), paralleling the FLR. Correctness of the model was verified by successful simulations of the FLR and I820 signal as measured with the control (no treatment) sample but also as measured with 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone- (inhibits electron transport in cytochrome b 6/f) and methylviologen- (accepts electrons from iron-sulphur cluster of PSI) treated samples and with the control sample upon different intensities of excitation light. From the simulations performed for the control sample, contribution of the oxidised donor of PSI, P700, and oxidised PC to the I820 signal minimum (reflects maximal accumulations of the two components) was estimated to be 75% and 25%, respectively. Further in silico experiments showed that PC must be reduced in the dark, cyclic electron transport around PSI must be considered in the model and activation of ferredoxin-NADP+-oxidoreductase (FNR) also affects the FLR. Correct simulations of the FLR and I820 signal demonstrate robustness of the model, confirm that the electron transport reactions occurring beyond PSII affect the shape of the FLR, and show usefulness and perspective of theoretical approach in studying of the light-induced photosynthetic reactions.

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Abbreviations

bH or H:

high potential haem b of cyt b 6/f

bL or L:

low potential haem b of cyt b 6/f

c or C:

haem c of cyt b 6/f

CET:

cyclic electron transport

Chl:

chlorophyll

cyt:

cytochrome

DBMIB:

2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone

F:

haem f of cyt b 6/f

F0 :

minimal fluorescence

FB or X:

iron-sulphur cluster of PSI

FM :

maximal fluorescence

Fd:

ferredoxin

FLD:

fluorescence decrease

FLI:

fluorescence induction

FLR:

fluorescence rise

FNR:

ferredoxin-NADP+-oxidoreductase

I820 :

relative transmittance signal measured at 820 nm

MV:

1,1′dimethyl-4,4′-bipyridinium-dichloride (methylviologen)

NADP+ and NADPH:

oxidised and reduced nicotinamide adenine dinucleotide phosphate

O, K, J, I, P, G, H:

particular steps of the FLR

OEC:

oxygen evolving complex

P680 or P:

electron donor of PSII

P700 or R:

electron donor of PSI

PC:

plastocyanin

PQ and PQH2 :

oxidised and reduced plastoquinone

PSI:

photosystem I

PSII:

photosystem II

QA or A:

first quinone electron acceptor of PSII

QB or B:

second quinone electron acceptor of PSII

RCII:

reaction centre of PSII

RT:

room temperature

Si (i = 0, 1, 2, 3):

redox states of OEC

TM:

thylakoid membrane

References

  • Baake, E., Schlöder, J.P.: Modelling the fast fluorescence rise of photosynthesis. — Bull. Math. Biol. 54: 999–1021, 1992.

    CAS  Google Scholar 

  • Bennoun, P.: Evidence for a respiratory chain in the chloroplast. — Proc. Natl. Acad. Sci. USA 79: 4352–4356, 1982.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cramer, W.A., Zhang, H.: Consequences of the structure of the cytochrome b 6 f complex for its charge transfer pathways. — Biochim. Biophys. Acta 1757: 339–345, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Crofts, A.R., Wraight, C.A.: The electrochemical domain of photosynthesis. — Biochim. Biophys. Acta 726: 149–185, 1983.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dau, H., Windecker, R., Hansen, U.-P.: Effect of light-induced changes in thylakoid voltage on chlorophyll fluorescence of Aegopodium podagraria leaves. — Biochim. Biophys. Acta 1057: 337–345, 1991.

    Article  CAS  Google Scholar 

  • Duysens, L.N.M., Sweers, H.E.: Mechanism of the two photochemical reactions in algae as studied by means of fluorescence. — In: Japanese Society of Plant Physiologists (ed.): Studies on Microalgae and Photosynthetic Bacteria. Pp 353–372. Univ.Tokyo Press, Tokyo 1963.

    Google Scholar 

  • Feild, T.S., Nedbal, L., Ort, D.R.: Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. — Plant Physiol. 116: 1209–1218, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Giersch, C.: Mathematical modelling of metabolism. — Curr. Opin. Plant Biol. 3: 249–253, 2000.

    CAS  PubMed  Google Scholar 

  • Govindjee: 63 years since Kautsky — chlorophyll a fluorescence. — Aust. J. Plant Physiol. 22: 131–160, 1995.

    Article  CAS  Google Scholar 

  • Guissé, B., Srivastava, A., Strasser, R.J.: The polyphasic rice of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves. — Arch. Sci. 48: 147–160, 1995.

    Google Scholar 

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

    CAS  Google Scholar 

  • Heredia, P., De Las Rivas, J.: Fluorescence induction of Photosystem II membranes shows the steps till reduction and protonation of the quinone pool. — J. Plant Physiol. 160: 1499–1506, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Holtgrefe, S., Bader, K.P., Horton, P., Scheibe, R., von Schaewen, A., Backhausen, J.E.: Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants. — Plant Physiol. 133: 1768–1778, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Ilík, P., Kouřil, R., Fiala, J., Nauš, J., Vácha, F.: Spectral characterization of chlorophyll fluorescence in barley leaves during linear heating. Analysis of high-temperature fluorescence rise around 60°C. — J. Photochem. Photobiol. 59: 103–114, 2000.

    Article  Google Scholar 

  • Ilík, P., Schansker, G., Kotabová, E., Váczi, P., Strasser, R.J., Barták, M.: A dip in the chlorophyll fluorescence induction at 0.2 — 2 s in Trebouxia-possessing lichens reflects a fast reoxidation of photosystem I. A comparison with higher plants. — Biochim. Biophys. Acta 1757: 12–20, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Jablonsky, J., Lazar, D.: Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation. — Biophys. J. 94: 2725–2736, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Jablonsky, J., Susila, P., Lazar, D.: Impact of dimeric organization of enzyme on its function: the case of photosynthetic water splitting. — Bioinformatics 24: 2755–2759, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, G.N.: Cyclic electron transport in C3 plants: fact or artefact? — J. Exp. Bot. 56: 407–416, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Joliot, A., Joliot, P.: Étude cinétique de la réaction photochimique libérant l’ oxygène au cours de la photosynthèse. — C. R. Acad. Sci. 258: 4622–4625, 1964.

    CAS  Google Scholar 

  • Joliot, P., Joliot, A.: Mechanism of electron transfer in the cytochrome b/f complex of algae: Evidence for a semiquinone cycle. — Proc. Natl. Acad. Sci. USA 91: 1034–1038, 1994.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Joly, D., Bigras, C., Harnois, J., Govindachary, S., Carpentier, R.: Kinetic analyses of the OJIP chlorophyll fluorescence rise in thylakoid membranes. — Photosynth. Res. 84: 107–112, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff, H., Schöttler, M.A., Maurer, J., Weis E.: Plastocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. — Biochim. Biophys. Acta 1659: 63–72, 2004.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kroon, B.M.A., Thoms, S.: From electron to biomass: A mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. — J. Phycol. 42: 593–609, 2006.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lazár, D.: Chlorophyll a fluorescence induction. — Biochim. Biophys. Acta 1412: 1–28, 1999.

    Article  PubMed  Google Scholar 

  • Lazár, D.: 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, 2003.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lazár, D., Ilík, P.: High-temperature induced chlorophyll fluorescence changes in barley leaves — Comparison of the critical temperatures determined from fluorescence induction and from fluorescence temperature curve. — Plant Sci. 124: 159–164, 1997.

    Article  Google Scholar 

  • Lazár, D., Jablonský, J.: On the approaches applied in formulation of a kinetic model of photosystem II: Different approaches lead to different simulations of the chlorophyll a fluorescence transients. — J. Theor. Biol. 257: 260–269, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Lazár, D., Kaňa, R., Klinkovský, T., Nauš, J.: Experimental and theoretical study on high temperature induced changes in chlorophyll a fluorescence oscillations in barley leaves upon 2 % CO2. — Photosynthetica 43: 13–27, 2005.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lazár, D., Pospíšil, P.: Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea-treated barley leaves at room and high temperatures. — Eur. Biophys. J. 28: 468–477, 1999.

    Article  PubMed  Google Scholar 

  • Lazár, D., Schansker, G.: Models of chlorophyll a fluorescence transients. — In: Laisk, A., Nedbal, L., Govindjee (ed.): Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Pp 85–123. Springer, Dordrecht 2009.

    Google Scholar 

  • Lebedeva, G.V., Belyaeva, N.E., Demin, O.V., Riznichenko, G.Y., Rubin, A.B.: A kinetic model of primary photosynthetic processes. Description of the fast phase of chlorophyll fluorescence induction under different light intensities. — Biofizika 47: 1044–1058, 2002.

    CAS  PubMed  Google Scholar 

  • McClendon, J.H., Fukshansky, L.: On the interpretation of absorption-spectra of leaves. 2. The nonabsorbed ray of the sieve effect and the mean optical pathlength in the remainder of the leaf. — Photochem. Photobiol. 51: 211–216, 1990.

    Article  CAS  Google Scholar 

  • Mendes, P.: GEPASI — a software package for modelling the dynamics, steady states and control of biochemical and other systems. — Comput. Appl. Biosci. 9: 563–571, 1993.

    CAS  PubMed  Google Scholar 

  • Oja, V., Bichele, I., Hüve, K., Rasulov, B., Laisk, A.: Reductive titration of photosystem I and differential extinction coefficient of P700+ at 810-950 nm in leaves. — Biochim. Biophys. Acta 1658: 225–234, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Pospíšil, P., Dau, H.: Chlorophyll fluorescence transients of Photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution. — Photosynth. Res. 65: 41–52, 2000.

    Article  PubMed  Google Scholar 

  • Pospíšil, P., Dau, H.: Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients. — Biochim. Biophys. Acta 1554: 94–100, 2002.

    Article  PubMed  Google Scholar 

  • Rios-Estepa, R., Lange, B.M.: Experimental and mathematical approaches to modeling plant metabolic network. — Phytochemistry 68: 2351–2374, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Rubin, A.B., Riznichenko, G.: Modeling of the primary processes in a photosynthetic membrane. — In: Laisk, A., Nedbal, L., Govindjee (ed.): Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Pp 151–176. Springer, Dordrecht 2009.

    Google Scholar 

  • Santabarbara, S., Heathcote, P., Evans, M.C.V.: Modelling of the electron transfer reactions in Photosystem I by electron tunnelling theory: The phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron-sulfur cluster FX. — Biochim. Biophys. Acta 1708: 283–310, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Satoh, K.: Fluorescence induction and activity of ferredoxin-NADP+ reductase in Bryopsis chloroplasts. — Biochim. Biophys. Acta 638: 327–333, 1981.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schansker, G., Tóth, S.Z., Strasser, R.J.: 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, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Schreiber, U., Neubauer, C.: O2-dependent electron flow, membrane energization and the mechanism of nonphotochemical quenching of chlorophyll fluorescence. — Photosynth. Res. 25: 279–293, 1990.

    Article  CAS  Google Scholar 

  • Stirbet, A., Govindjee, Strasser, B.J., Strasser, R.J.: Chlorophyll a fluorescence induction in higher plants: Modelling and numerical simulation. — J. Theor. Biol. 193: 131–151, 1998.

    Article  CAS  Google Scholar 

  • Strasser, B.J.: Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. — Photosynth. Res. 52: 147–155, 1997.

    Article  CAS  Google Scholar 

  • Strasser, R.J., Srivastava, A., Govindjee: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. — Photochem. Photobiol. 61: 32–42, 1995.

    Article  CAS  Google Scholar 

  • Strasser, R.J., Stirbet, A.D.: Estimation of the energetic connectivity of PS II centres in plants using the fluorescence rise O-J-I-P — Fitting of experimental data to three different PS II models. — Math. Comput. Simulat. 56: 451–461, 2001.

    Article  Google Scholar 

  • Sušila, P., Lazár, D., Ilík, P., Tomek, P., Nauš, J.: The gradient of exciting radiation within a sample affects relative heights of steps in the fast chlorophyll a fluorescence rise. — Photosynthetica 42: 161–172, 2004.

    Article  Google Scholar 

  • Tomek, P., Lazár, D., Ilík, P., Nauš, J.: On the intermediate steps between the O and P steps in chlorophyll alpha fluorescence rise measured at different intensities of exciting light. — Aust. J. Plant Physiol. 28: 1151–1160, 2001.

    Google Scholar 

  • Tóth, S.Z., Schansker, G., Strasser, R.J.: In intact leaves, the maximum fluorescence level (F M) is independent of the redox state of the plastoquinone pool: A DCMU-inhibition study. — Biochim. Biophys. Acta 1708: 275–282, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Tsimilli-Michael, M., Pêcheux, M., Strasser, R.J.: Vitality and stress adaptation of the symbionts of coral reef and temperature foraminifers probed in hospite by the fluorescence kinetics OJIP. — Arch. Sci. 51: 205–240, 1998.

    Google Scholar 

  • van Thor, J.J., Geerlings, T.H., Matthijs, H.C.P., Hellingwerf, K.J.: Kinetic evidence for the PsaE-dependent transient ternary complex photosystem I/ferredoxin/ferredoxin:NADP+ reductase in a cyanobacterium. — Biochemistry 38: 12735–12746, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Vernotte, C., Etienne, A.-L., Briantais, J.-M.: Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. — Biochim. Biophys. Acta 545: 519–527, 1979.

    Article  CAS  PubMed  Google Scholar 

  • Vredenberg, W.J.: A three-state model for energy trapping and chlorophyll fluorescence in photosystem II incorporating radical pair recombination. — Biophys. J. 79: 26–38, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Vredenberg, W.J., Bulychev, A.A.: Photo-electrochemical control of photosystem II chlorophyll fluorescence in vivo. — Bioelectrochem. 57: 123–128, 2002.

    Article  CAS  Google Scholar 

  • Vredenberg, W., Prášil, O.: Modeling of chlorophyll a fluorescence kinetics in plant cells: derivation of a descriptive algorithm. — In: Laisk, A., Nedbal, L., Govindjee (ed.): Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Pp 125–149. Springer, Dordrecht 2009.

    Google Scholar 

  • Zhu, X.-G., Govindjee, Baker, N.R., deSturler, E., Ort, D.R., Long, S.P.: 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, 2005.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Ministry of Education of the Czech Republic by a grant number MSM 6198959215 and through the Marie Curie Initial Training Network of the 7th Framework Programme of the European Union, contract number PITN-GA-2009-238017. The experimental data presented in Fig. 1 are courtesy of Gert Schansker and Petr Ilík.

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  1. Laboratory of Biophysics, Faculty of Science, Palacký University, Tř. Svobody 26, 771 46, Olomouc, Czech Republic

    D. Lazár

  2. Photon Systems Instruments, Ltd., Koláčkova 39, 621 00, Brno, Czech Republic

    D. Lazár

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Lazár, D. Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47, 483–498 (2009). https://doi.org/10.1007/s11099-009-0074-8

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