Skip to main content
SpringerLink
Log in

Chlorophyll a fluorescence: beyond the limits of the QA model

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

Abstract

Chlorophyll a fluorescence is a non-invasive tool widely used in photosynthesis research. According to the dominant interpretation, based on the model proposed by Duysens and Sweers (1963, Special Issue of Plant and Cell Physiology, pp 353–372), the fluorescence changes reflect primarily changes in the redox state of QA, the primary quinone electron acceptor of photosystem II (PSII). While it is clearly successful in monitoring the photochemical activity of PSII, a number of important observations cannot be explained within the framework of this simple model. Alternative interpretations have been proposed but were not supported satisfactorily by experimental data. In this review we concentrate on the processes determining the fluorescence rise on a dark-to-light transition and critically analyze the experimental data and the existing models. Recent experiments have provided additional evidence for the involvement of a second process influencing the fluorescence rise once QA is reduced. These observations are best explained by a light-induced conformational change, the focal point of our review. We also want to emphasize that—based on the presently available experimental findings—conclusions on α/ß-centers, PSII connectivity, and the assignment of FV/FM to the maximum PSII quantum yield may require critical re-evaluations. At the same time, it has to be emphasized that for a deeper understanding of the underlying physical mechanism(s) systematic studies on light-induced changes in the structure and reaction kinetics of the PSII reaction center are required.

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

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

CP43, CP47:

Core antenna proteins of photosystem II of 43 and 47 kDa, respectively

DCMU:

3-(3′,4′-Dichlorophenyl)-1,1-dimethylurea

ETC:

Electron transport chain

FCCP:

Carbonylcyanide-p-trifluoromethoxyphenylhydrazone

F0 :

Minimum chl a fluorescence yield in the dark-adapted state

FM :

Maximum chl a fluorescence yield in the dark-adapted state

FV :

Variable fluorescence defined as FM−F0

LED:

Light emitting diode

P680:

Reaction center pigments of photosystem II

PFD:

Photon flux density

Pheo:

Pheophytin

PMS:

Phenazine methosulfate

PQ:

Plastoquinone

PSII and PSI:

Photosystem II and I, respectively

QA and QB :

Primary and secondary quinone electron acceptors of photosystem II, respectively

RC:

Reaction center

S-states S0, S1, S2, S3, and S4 :

Different redox states of the oxygen-evolving complex

SSTF:

Saturating single turnover flash

TMPD:

N,N,N’,N’-tetramethyl-p-phenylenediamine dihydrochloride

TRIS:

Tris(hydroxymethyl)aminomethane

TyrZ, TyrD:

Tyrosine donors to P680 localized on the PSII reaction center D1 and D2 proteins, respectively

References

  • Abgaryan GA, Christophorov LN, Goushcha AO, Holzwarth AR, Kharkyanen VN, Knox PP, Lukashev EA (1998) Effects of mutual influence of photoinduced electron transitions and slow structural rearrangements in bacterial photosynthetic reaction centers. J Biol Phys 24:1–17

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amesz J, Fork DC (1967) Quenching of chlorophyll fluorescence by quinones in algae and chloroplasts. Biochim Biophys Acta 143:97–107

    CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    CAS  PubMed  Google Scholar 

  • Barabás K, Kravcova T, Garab G (1993) Flash-induced reduction of cytochrome b-559 by Q −B in chloroplasts in the presence of protonophores. Photosynth Res 36:59–64

    PubMed  Google Scholar 

  • Barabash YM, Berezetskaya NM, Christophorov LN, Goushcha AO, Kharkyanen VN (2002) Effects of structural memory in protein reactions. J Chem Phys 116:4339–4352

    CAS  Google Scholar 

  • Boussac A, Sugiura M, Rappaport F (2011) Probing the quinone binding site of photostem II from Thermosynechococcus elongatus containing PsbA1 or PabA3 as the D1 protein through the binding characteristics of herbicides. Biochim Biophys Acta 1807:119–129

    CAS  PubMed  Google Scholar 

  • Braslavsky SE, Holzwarth AR (2012) Role of carotenoids in photosystem II (PS II) reaction centres. Int J Thermophys 33:2021–2025

    CAS  Google Scholar 

  • Brudvig GW, Casey JL, Sauer K (1983) The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution. Biochim Biophys Acta 723:366–371

    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

    CAS  PubMed  Google Scholar 

  • Butler WL, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376:116–125

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Christophorov LN, Holzwarth AR, Kharkyanen VN, van Mourik F (2000) Structure-function self-organization in nonequilibrium macromolecular systems. Chem Phys 256:45–60

    CAS  Google Scholar 

  • Christophorov LN, Holzwarth AR, Kharkyanen VN (2003) Conformational regulation in single molecule reactions. Ukrainian J Phys 48:672–680

    CAS  Google Scholar 

  • Cseh Z, Rajagopal S, Tsonev T, Busheva M, Papp E, Garab G (2000) Thermooptic effect in chloroplast thylakoid membranes; Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry 39:15250–15257

    CAS  PubMed  Google Scholar 

  • Danielsson R, Suorsa M, Paakkarinen V, Albertsson P-Å, Styring S, Aro E-M, Mamedov F (2006) Dimeric and monomeric organization of photosystem II; Distribution of five distinct complexes in the different domains of the thylakoid membrane. J Biol Chem 281:14241–14249

    CAS  PubMed  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 1098:49–60

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Dekker JP, van Grondelle R (2000) Primary charge separation in photosystem II. Photosynth Res 63:195–208

    CAS  PubMed  Google Scholar 

  • Delosme R (1967) Étude de l’induction de fluorescence des algues vertes et des chloroplastes au début d’une illumination intense. Biochim Biophys Acta 143:108–128

    CAS  PubMed  Google Scholar 

  • Delosme R (1971) Photosynthèse—variations du rendement de fluorescence de la chlorophylle in vivo sous l’action d’éclairs de forte intensité. C R Acad Sci Paris 272D:2828–2831

    Google Scholar 

  • Delosme R, Béal D, Joliot P (1994) Photoacoustic detection of flash-induced charge separation in photosynthetic systems. Spectral dependence of the quantum yield. Biochim Biophys Acta 1185:56–64

    CAS  Google Scholar 

  • Deshmukh SS, Williams JC, Allen JP, Kálmán L (2011a) Light-induced conformational changes in photosynthetic reaction centers: dielectric relaxation in the vicinity of the dimer. Biochemistry 50:340–348

    CAS  PubMed  Google Scholar 

  • Deshmukh SS, Williams JC, Allen JP, Kálmán L (2011b) Light-induced conformational changes in photosynthetic reaction centers: redox regulated proton pathway near the dimer. Biochemistry 50:3321–3331

    CAS  PubMed  Google Scholar 

  • Diner BA (1977) Dependence of the deactivation reactions of photosystem II on the redox state of plastoquinone pool A varied under anaerobic conditions; Equilibria on the acceptor side of photosystem II. Biochim Biophys Acta 460:247–258

    CAS  PubMed  Google Scholar 

  • Duysens LNM, Sweers HE (1963) Mechanisms of two photochemical reactions in algae as studied by means of fluorescence, In: Japanese Society of Plant Physiologists (ed) Studies on microalgae and photosynthetic bacteria, Special Issue of Plant and Cell Physiology. University of Tokyo Press, Tokyo, pp 353–372

  • Forbush B, Kok B, McGloin MP (1971) Cooperation of charges in photosynthetic oxygen evolution. II. Damping of flash yield oscillation, deactivation. Photochem Photobiol 14:307–321

    CAS  Google Scholar 

  • Fowler CF, Kok B (1974) Direct observation of a light-induced electric field in chloroplasts. Biochim Biophys Acta 357:308–318

    CAS  PubMed  Google Scholar 

  • France LL, Geacintov NE, Breton J, Valkunas L (1992) The dependence of the dregrees of sigmoidicities of fluorescence induction curves in spinach chloroplasts on the duration of actinic pulses in pump-probe experiments. Biochim Biophys Acta 1101:105–119

    CAS  Google Scholar 

  • Goushcha AO, Kapoustina MT, Kharkyanen VN, Holzwarth AR (1997a) Nonlinear dynamic processes in an ensemble of photosynthetic reaction centers; Theory and experiment. J Phys Chem B 101:7612–7619

    CAS  Google Scholar 

  • Goushcha AO, Kharkyanen VN, Holzwarth AR (1997b) Nonlinear light-induced properties of photosynthetic reaction centers under low intensity irradition. J Phys Chem B 101:259–265

    CAS  Google Scholar 

  • Goushcha AO, Holzwarth AR, Kharkyanen VN (1999) Self-regulation phenomenon of electron-conformational transitions in biological electron transfer under nonequilibrium conditions. Phys Rev E 59:3444–3452

    CAS  Google Scholar 

  • Goushcha AO, Kharkyanen VN, Scott GW, Holzwarth AR (2000) Self-regulation phenomena in bacterial reaction centers. I. General theory. Biophys J 79:1237–1252

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gulbinas V, Karpicz R, Garab G, Valkunas L (2006) Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochemistry 45:9559–9565

    CAS  PubMed  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 Central  PubMed  Google Scholar 

  • Harbinson J, Genty B, Baker NR (1990) The relationship between CO2 assimilation and electron transport in leaves. Photosynth Res 25:213–224

    CAS  PubMed  Google Scholar 

  • Heber U (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231

    CAS  PubMed  Google Scholar 

  • Hemelrijk PW, van Gorkom HJ (1992) No double hit involved in fluorescence induction of photosystem II of spinach chloroplasts. In: Murata N (ed) Research in photosynthesis. Kluwer Academic, Dordrecht, pp 33–36

    Google Scholar 

  • Holzwarth AR (2008a) Ultrafast primary reactions in the photosystems of oxygen evolving organisms. In: Braun M, Gilch P, Zinth W (eds) Ultrashort laser pulses in biology and medicine. Springer, Dordrecht, pp 141–164

    Google Scholar 

  • Holzwarth AR (2008b) Primary reactions—from isolated complexes to intact plants. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 77–83

    Google Scholar 

  • Holzwarth AR, Müller MG (1996) Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides; A femtosecond transient absorption study. Biochemistry 35:11820–11831

    CAS  PubMed  Google Scholar 

  • Hou J-M, Boichenko VA, Diner BA, Mauzerall D (2001) Thermodynamics of electron transfer in oxygenix photosynthetic reaction centers: volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes. Biochemistry 40:7117–7125

    CAS  PubMed  Google Scholar 

  • Joliot A (1974) Effect of low temperature (-30 to -60°C) on the reoxidation of the photosystem II primary electron acceptor in the presence and absence of 3(3,4-dichlorophenyl)-1,1-dimethyl-urea. Biochim Biophys Acta 357:439–448

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Joliot P, Joliot A (1979) Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. Biochim Biophys Acta 546:93–105

    CAS  PubMed  Google Scholar 

  • Joliot P, Joliot A (1981) A photosystem II electron acceptor which is not a plastoquinone. FEBS Lett 134:155–158

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Junge W (1977) Membrane potentials in photosynthesis. Annu Rev Plant Physiol 28:503–536

    CAS  Google Scholar 

  • Kautsky H, Appel W, Amann H (1960) Chlorophyllfluorescenz und Kohlensäure-assimilation: XIII. Die Fluorescencekurve und die Photochemie der Pflanze. Biochem Z 332:277–292

    CAS  PubMed  Google Scholar 

  • Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115

    CAS  PubMed  Google Scholar 

  • Knox PP, Venediktov PS, Kononenko AA, Garab GI, Faludi-Daniel Á (1984) Role of electric polarization in the thermoluminescence of chloroplasts. Photochem Photobiol 40:119–125

    CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    CAS  PubMed  Google Scholar 

  • Krieger A, Rutherford AW (1997) Comparison of chloride-depleted and calcium-depleted PSII: the midpoint potential of QA and susceptibility to photodamage. Biochim Biophys Acta 1319:91–98

    CAS  Google Scholar 

  • Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37:17339–17344

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lambrev PH, Schmitt F-J, Kussin S, Schoengen M, Várkonyi Z, Eichler HJ, Garab G, Renger G (2011) Functional domain size in aggregates of light-harvesting complex II and thylakoid membranes. Biochim Biophys Acta 1807:1022–1031

    CAS  PubMed  Google Scholar 

  • Lavergne J (1982) Two types of primary acceptors in chloroplasts photosystem II. I. Different recombination properties. Photobiochem Photobiophys 3:257–271

    CAS  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

    PubMed  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 47:483–498

    Google Scholar 

  • Lazár D, Pospíšil P (1999) 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

    PubMed  Google Scholar 

  • Lazár D, Schansker G (2009) Models of Chlorophyll a fluorescence transients. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems, vol 29., Advances in photosynthesis and respiration. Springer, Dordrecht, pp 85–123

    Google Scholar 

  • Loach PA (1976) Oxidation-reduction potentials, absorbance bands and molar absorbance of compounds used in biochemical studies. In: Fasman GD (ed) Handbook of biochemistry and molecular biology, 3rd edn, vol I., Physical Chemical Data. CRC Press, Cleveland, pp 122–130

    Google Scholar 

  • Mano J, Hideg E, Asada K (2004) Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys 429:71–80

    CAS  PubMed  Google Scholar 

  • Martinez-Junza V, Szczepaniak M, Braslavsky SE, Sander J, Nowaczyk M, Rögner M, Holzwarth AR (2008) A photoprotection mechanism involving the D2 branch in photosystem II cores with closed reaction centers. Photochem Photobiol Sci 7:1337–1343

    CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence— a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Google Scholar 

  • McCauley SW, Melis A, Tang GM-S, Arnon DI (1987) Protonophores induce plastoquinol oxidation and quench chloroplast fluorescence: evidence for a cyclic, proton-conducting pathway in oxygenic photosynthesis. Proc Natl Acad Sci USA 84:8424–8428

    CAS  PubMed Central  PubMed  Google Scholar 

  • McMahon BH, Müller JD, Wraight CA, Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74:2567–2587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Melis A (1985) Functional properties of photosystem IIß in spinach chloroplasts. Biochim Biophys Acta 808:334–342

    CAS  Google Scholar 

  • Melis A, Homann PH (1975) Kinetic analysis of the fluorescence induction in 3-(3,4- dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts. Photochem Photobiol 21:431–437

    CAS  Google Scholar 

  • Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350

    CAS  PubMed  Google Scholar 

  • Moise N, Moya I (2004a) Correlation between lifetime heterogeneity and kinetics heterogeneity during chlorophyll fluorescence induction in leaves: 1. Mono-frequency phase and modulation analysis reveals a conformational change of a PSII pigment complex during the IP thermal phase. Biochim Biophys Acta 1657:33–46

    CAS  PubMed  Google Scholar 

  • Moise N, Moya I (2004b) Correlation between lifetime heterogeneity and kinetics heterogeneity during chlorophyll fluorescence induction in leaves: 2. Multi-frequency phase and modulation analysis evidences a loosely connected PSII pigment-protein complex. Biochim Biophys Acta 1657:47–60

    CAS  PubMed  Google Scholar 

  • Morin P (1964) Études des cinétiques de fluorescence de la chlorophylle in vivo, dans les premiers instants qui suivent le début de l’illumination. J Chim Phys 61:674–680

    CAS  Google Scholar 

  • Müller MG, Dorra D, Holzwarth AR, Gad’on N, Drews G (1995) Time-dependent radical pair relaxation in chromatophores of an antenna-free mutant from Rhodobacter capsulatus. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 1. Kluwer Academic, Dordrecht, pp 595–598

    Google Scholar 

  • Munday JCM, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagy L, Maroti P, Terazima M (2008) Spectrally silent light induced conformation change in photosynthetic reaction centers. FEBS Lett 582:3657–3662

    CAS  PubMed  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 42c:1246–1254

    Google Scholar 

  • Oberhuber W, Dai Z-Y, Edwards GE (1993) Light dependence of quantum yields of photosystem II and CO2 fixation in C3 and C4 plants. Photosynth Res 35:265–274

    CAS  PubMed  Google Scholar 

  • Osváth S, Meszéna G, Barzda V, Garab G (1994) Trapping magnetically oriented chloroplast thylakoid membranes in gels for electric measurements. J Photochem Photobiol, B 26:287–292

    Google Scholar 

  • Paillotin G (1976) Movement of excitations in photosynthetic domains of photosystem II. J Theor Biol 58:237–252

    CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19., Advances in photosynthesis and respiration. Springer, Dordrecht 818 pp

    Google Scholar 

  • Petrouleas V, Crofts AR (2005) The iron-quinone acceptor complex. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase, vol 22., Advances in photosynthesis and respiration. Springer, Dordrecht, pp 177–206

    Google Scholar 

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

    PubMed  Google Scholar 

  • Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around Photosystem II in vivo. Photosynth Res 48:395–410

    CAS  PubMed  Google Scholar 

  • Prince RC, Linkletter SJG, Dutton PL (1981) The thermodynamic properties of some commonly used oxidation-reduction mediators, inhibitors and dyes, as determined by polarography. Biochim Biophys Acta 635:132–148

    CAS  PubMed  Google Scholar 

  • Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130:4431–4446

    CAS  PubMed  Google Scholar 

  • Robinson HH, Crofts AR (1984) Kinetics of proton uptake and the oxidation-reduction reactions of the quinone acceptor complex of PS II from pea chloroplasts. In: Sybesma C (ed) Advances in photosynthesis research, vol I. Martinus Nijhoff/Dr W Junk, Den Haag, pp 477–480

  • Rubin A, Riznichenko G (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, vol 29., Advances in photosynthesis and respiration. Springer, Dordrecht, pp 151–176

    Google Scholar 

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

    Google Scholar 

  • Samson G, Prášil O, Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 37:163–182

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151

    CAS  PubMed  Google Scholar 

  • Schansker G, van Rensen JJS (1999) Performance of active photosystem II centers in photoinhibited pea leaves. Photosynth Res 62:175–184

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schansker G, Tóth SZ, 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 1757:787–797

    CAS  PubMed  Google Scholar 

  • Schansker G, Yuan Y, Strasser RJ (2008) Chl a fluorescence and 820 nm transmission changes occurring during a dark-to-light transition in pine needles and pea leaves: a comparison. In: Allen JF, Osmond B, Golbeck JH, Gantt E (eds) Energy from the sun. Springer, Dordrecht, pp 951–955

    Google Scholar 

  • Schansker G, Tóth SZ, Kovács L, Holzwarth AR, Garab G (2011) Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise. Biochim Biophys Acta 1807:1032–1043

    CAS  PubMed  Google Scholar 

  • Schlodder E (2008) Temperature dependence of the reduction kinetics of P680+ in oxygen-evolving PSII complexes throughout the range from 320 to 80 K. In: Allen JF, Osmond B, Golbeck JH, Gantt E (eds) Energy from the sun. Springer, Dordrecht, pp 187–190

    Google Scholar 

  • Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272

    CAS  PubMed  Google Scholar 

  • Schreiber U (2002) Assessment of maximal fluorescence yield: donor-side dependent quenching and QB-quenching. In: Van Kooten O, Snel JFH (eds) Plant spectrofluorometry: applications and basic research. Rozenberg, Amsterdam, pp 23–47

    Google Scholar 

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 279–319

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schreiber U, Neubauer C, Klughammer C (1989) Devices and methods for room-temperature fluorescence analysis. Philos Trans R Soc Lond B 323:241–251

    CAS  Google Scholar 

  • Schreiber U, Hormann H, Neubauer C, Klughammer C (1995) Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust J Plant Physiol 22:209–220

    CAS  Google Scholar 

  • Shinkarev V (2005) Flash-Induced oxygen evolution in photosynthesis: simple solution for the extended S-state model that includes misses, double-hits, inactivation, and backward-transitions. Biophys J 88:412–421

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sokolove PM, Marsho TV (1979) The effect of valinomycin on electron transport in intact spinach chloroplasts. FEBS Lett 100:179–184

    CAS  PubMed  Google Scholar 

  • 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

    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

    CAS  PubMed  Google Scholar 

  • Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 513–524

    Google Scholar 

  • Strasser RJ, Govindjee (1991) The F0 and the O-J-I-P fluorescence rise in higher plants and algae. In: Argyroudi-Akoyunoglou JH (ed) Regulation of chloroplast biogenesis. Plenum Press, New York, pp 423–426

    Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: The JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol V. Kluwer Academic, Dordrecht, pp 977–980

    Google Scholar 

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

    Google Scholar 

  • Szczepaniak M, Sugiura M, Holzwarth AR (2008) The role of TyrD in the electron transfer kinetics in photosystem II. Biochim Biophys Acta 1777:1510–1517

    CAS  PubMed  Google Scholar 

  • Szczepaniak M, Sander J, Nowaczyk M, Müller MG, Rögner M, Holzwarth AR (2009) Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction center. Biophys J 96:621–631

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura N, Inoue H, Inoue Y (1990) Inactivation of the water-oxidizing complex by exogenous reductants in PSII membranes depleted of extrinsic proteins. Plant Cell Physiol 31:469–477

    CAS  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2005a) 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

    PubMed  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2005b) Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedling (Hordeum vulgare L.). J Plant Physiol 162:181–194

    PubMed  Google Scholar 

  • Tóth SZ, Schansker G, Garab G, Strasser RJ (2007a) Photosynthetic electron transport activity in heat-treated barley leaves: the role of internal alternative electron donors to photosystem II. Biochim Biophys Acta 1767:295–305

    PubMed  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2007b) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203

    PubMed  Google Scholar 

  • Tóth SZ, Puthur JT, Nagy V, Garab G (2009) Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygen-evolving complexes. Plant Physiol 149:1568–1578

    PubMed Central  PubMed  Google Scholar 

  • Trissl H-W, Lavergne J (1994) 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 22:183–193

    Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    PubMed  Google Scholar 

  • van Wijk KJ, Krause GH (1991) O2-dependence of photoinhibition at low temperature in intact protoplasts of Locusta valerianella L. Planta 186:135–142

    PubMed  Google Scholar 

  • Vasil’ev S, Bruce D (1998) Nonphotochemical quenching of excitation energy in photosystem II. A picoseconds time-resolved study of the low yield of chlorophyll a fluorescence induced by single-turnover flash in isolated spinach thylakoids. Biochemistry 37:11046–11054

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vredenberg WJ (2004) System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: A challenging view. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19., Advances in photosynthesis and respiration. Springer, Dordrecht, pp 133–172

    Google Scholar 

  • Vredenberg WJ (2008) Analysis of initial chlorophyll fluorescence induction kinetics in chloroplasts in terms of rate constants of donor side quenching release and electron trapping in photosystem II. Photosynth Res 96:83–97

    CAS  PubMed  Google Scholar 

  • Vredenberg WJ (2011) Kinetic analysis and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. Biosystems 103:138–151

    CAS  PubMed  Google Scholar 

  • Vredenberg WJ, Bulychev AA (2002) Photo-electrochemical control of photosystem II chlorophyll fluorescence in vivo. Bioelectrochemistry 57:123–128

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vredenberg W, Kasalicky V, Durchan M, Prasil 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 1757:173–181

    CAS  PubMed  Google Scholar 

  • Vredenberg W, Durchan M, Prasil O (2007) On the chlorophyll a fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains. Photosynth Res 93:183–192

    CAS  PubMed  Google Scholar 

  • Vredenberg W, Durchan M, Prášil O (2012) The analysis of PS II photochemical activity using single and multi-turnover excitations. J Photochem Photobiol, B 107:45–54

    CAS  Google Scholar 

  • Wientjes E, Croce R (2012) PMS: photosystem I electron donor or fluorescence quencher. Photosynth Res 111:185–191

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yaakoubd B, Andersen R, Desjardins Y, Samson G (2002) Contributions of the free oxidized and QB-bound plastoquinone molecules to the thermal phase of chlorophyll-a fluorescence. Photosynth Res 74:251–257

    CAS  PubMed  Google Scholar 

  • Zhu X-G, 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

    CAS  PubMed  Google Scholar 

  • Zimányi L, Garab G (1989) Configuration of the electric field and distribution of ions in energy transducing biological membranes: model calculations in a vesicle containing discrete charges. J Theor Biol 138:59–76

    Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Petar Lambrev, László Kovács, and Fabrice Rappaport for useful discussions. This work was supported by the Hungarian Research Foundation (OTKA, grant no. MB08B82403, PD72718 and CNK80345 to G.S., S.Z.T. and G.G., respectively), and by NIH-A*STAR grant (TÉT-10-1-2011-0279) to GG. S.Z.T. acknowledges financial support by the Bolyai János Research Foundation of the Hungarian Academy of Sciences. This work was also supported by the Marie Curie Initial Training Network “HARVEST” sponsored by the 7th Framework Program of the European Union (grant number 238017 to G.G. and A.R.H.).

Author information

Authors and Affiliations

  1. Institute of Plant Biology, Biological Research Center Szeged, Hungarian Academy of Sciences, Szeged, 6701, Hungary

    Gert Schansker, Szilvia Z. Tóth & Győző Garab

  2. Max-Planck-Institute for Chemical Energy Conversion, 45470, Mülheim an der Ruhr, Germany

    Alfred R. Holzwarth

Authors
  1. Gert Schansker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Szilvia Z. Tóth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alfred R. Holzwarth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Győző Garab
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Gert Schansker or Győző Garab.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schansker, G., Tóth, S.Z., Holzwarth, A.R. et al. Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynth Res 120, 43–58 (2014). https://doi.org/10.1007/s11120-013-9806-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9806-5

Keywords

Search

Navigation