Advertisement

Photosynthesis Research

, Volume 120, Issue 1–2, pp 43–58 | Cite as

Chlorophyll a fluorescence: beyond the limits of the QA model

  • Gert SchanskerEmail author
  • Szilvia Z. Tóth
  • Alfred R. Holzwarth
  • Győző GarabEmail author
Review

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.

Keywords

Chl a fluorescence Fluorescence yield changes Light-induced conformational changes OJIP transient Thermal phase 

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

Notes

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.).

References

  1. 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 24:1–17PubMedCentralPubMedGoogle Scholar
  2. Amesz J, Fork DC (1967) Quenching of chlorophyll fluorescence by quinones in algae and chloroplasts. Biochim Biophys Acta 143:97–107PubMedGoogle Scholar
  3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedGoogle Scholar
  4. Barabás K, Kravcova T, Garab G (1993) Flash-induced reduction of cytochrome b-559 by QB in chloroplasts in the presence of protonophores. Photosynth Res 36:59–64PubMedGoogle Scholar
  5. Barabash YM, Berezetskaya NM, Christophorov LN, Goushcha AO, Kharkyanen VN (2002) Effects of structural memory in protein reactions. J Chem Phys 116:4339–4352Google Scholar
  6. 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 1807:119–129PubMedGoogle Scholar
  7. Braslavsky SE, Holzwarth AR (2012) Role of carotenoids in photosystem II (PS II) reaction centres. Int J Thermophys 33:2021–2025Google Scholar
  8. 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 723:366–371Google Scholar
  9. Bulychev AA, Vredenberg WJ (2001) Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I. Bioelectrochemistry 54:157–168PubMedGoogle Scholar
  10. Butler WL, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376:116–125PubMedGoogle Scholar
  11. Carillo N, Arana JL, Vallejos RH (1981) Light modulation of chloroplast membrane-bound ferredoxin-NADP+ oxidoreductase. J Biol Chem 256:1058–1059Google Scholar
  12. Christophorov LN, Holzwarth AR, Kharkyanen VN, van Mourik F (2000) Structure-function self-organization in nonequilibrium macromolecular systems. Chem Phys 256:45–60Google Scholar
  13. Christophorov LN, Holzwarth AR, Kharkyanen VN (2003) Conformational regulation in single molecule reactions. Ukrainian J Phys 48:672–680Google Scholar
  14. 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 39:15250–15257PubMedGoogle Scholar
  15. 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 281:14241–14249PubMedGoogle Scholar
  16. 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 1098:49–60Google Scholar
  17. de Wijn R, van Gorkom HJ (2001) Kinetics of electron transfer from QA to QB in photosystem II. Biochemistry 40:11912–11922PubMedGoogle Scholar
  18. Dekker JP, van Grondelle R (2000) Primary charge separation in photosystem II. Photosynth Res 63:195–208PubMedGoogle Scholar
  19. Delosme R (1967) Étude de l’induction de fluorescence des algues vertes et des chloroplastes au début d’une illumination intense. Biochim Biophys Acta 143:108–128PubMedGoogle Scholar
  20. 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:2828–2831Google Scholar
  21. 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 1185:56–64Google Scholar
  22. 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 50:340–348PubMedGoogle Scholar
  23. 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 50:3321–3331PubMedGoogle Scholar
  24. 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 460:247–258PubMedGoogle Scholar
  25. 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 353–372Google Scholar
  26. Forbush B, Kok B, McGloin MP (1971) Cooperation of charges in photosynthetic oxygen evolution. II. Damping of flash yield oscillation, deactivation. Photochem Photobiol 14:307–321Google Scholar
  27. Fowler CF, Kok B (1974) Direct observation of a light-induced electric field in chloroplasts. Biochim Biophys Acta 357:308–318PubMedGoogle Scholar
  28. 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 1101:105–119Google Scholar
  29. 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 101:7612–7619Google Scholar
  30. Goushcha AO, Kharkyanen VN, Holzwarth AR (1997b) Nonlinear light-induced properties of photosynthetic reaction centers under low intensity irradition. J Phys Chem B 101:259–265Google Scholar
  31. Goushcha AO, Holzwarth AR, Kharkyanen VN (1999) Self-regulation phenomenon of electron-conformational transitions in biological electron transfer under nonequilibrium conditions. Phys Rev E 59:3444–3452Google Scholar
  32. Goushcha AO, Kharkyanen VN, Scott GW, Holzwarth AR (2000) Self-regulation phenomena in bacterial reaction centers. I. General theory. Biophys J 79:1237–1252PubMedCentralPubMedGoogle Scholar
  33. Gulbinas V, Karpicz R, Garab G, Valkunas L (2006) Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochemistry 45:9559–9565PubMedGoogle Scholar
  34. Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:649–660PubMedCentralPubMedGoogle Scholar
  35. Harbinson J, Genty B, Baker NR (1990) The relationship between CO2 assimilation and electron transport in leaves. Photosynth Res 25:213–224PubMedGoogle Scholar
  36. Heber U (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231PubMedGoogle Scholar
  37. 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 33–36Google Scholar
  38. 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 141–164Google Scholar
  39. 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 77–83Google Scholar
  40. Holzwarth AR, Müller MG (1996) Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides; A femtosecond transient absorption study. Biochemistry 35:11820–11831PubMedGoogle Scholar
  41. 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 40:7117–7125PubMedGoogle Scholar
  42. 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 357:439–448PubMedGoogle Scholar
  43. Joliot A, Joliot P (1964) Étude cinétique de la reaction photochimique libérant l’oxygène au cours de la photosynthèse. C R Acad Sci Paris 258:4622–4625PubMedGoogle Scholar
  44. Joliot P, Joliot A (1979) Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. Biochim Biophys Acta 546:93–105PubMedGoogle Scholar
  45. Joliot P, Joliot A (1981) A photosystem II electron acceptor which is not a plastoquinone. FEBS Lett 134:155–158Google Scholar
  46. Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214PubMedCentralPubMedGoogle Scholar
  47. Junge W (1977) Membrane potentials in photosynthesis. Annu Rev Plant Physiol 28:503–536Google Scholar
  48. Kautsky H, Appel W, Amann H (1960) Chlorophyllfluorescenz und Kohlensäure-assimilation: XIII. Die Fluorescencekurve und die Photochemie der Pflanze. Biochem Z 332:277–292PubMedGoogle Scholar
  49. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115PubMedGoogle Scholar
  50. Knox PP, Venediktov PS, Kononenko AA, Garab GI, Faludi-Daniel Á (1984) Role of electric polarization in the thermoluminescence of chloroplasts. Photochem Photobiol 40:119–125Google Scholar
  51. 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 79:209–218PubMedGoogle Scholar
  52. 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 1319:91–98Google Scholar
  53. 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 37:17339–17344PubMedGoogle Scholar
  54. 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 63:171–182PubMedGoogle Scholar
  55. 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 1807:1022–1031PubMedGoogle Scholar
  56. Lavergne J (1982) Two types of primary acceptors in chloroplasts photosystem II. I. Different recombination properties. Photobiochem Photobiophys 3:257–271Google Scholar
  57. 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 220:469–503PubMedGoogle Scholar
  58. 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 47:483–498Google Scholar
  59. 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 28:468–477PubMedGoogle Scholar
  60. 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 85–123Google Scholar
  61. 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 122–130Google Scholar
  62. 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 429:71–80PubMedGoogle Scholar
  63. 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 7:1337–1343PubMedGoogle Scholar
  64. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence— a practical guide. J Exp Bot 51:659–668PubMedGoogle Scholar
  65. 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 84:8424–8428PubMedCentralPubMedGoogle Scholar
  66. McMahon BH, Müller JD, Wraight CA, Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74:2567–2587PubMedCentralPubMedGoogle Scholar
  67. Melis A (1985) Functional properties of photosystem IIß in spinach chloroplasts. Biochim Biophys Acta 808:334–342Google Scholar
  68. Melis A, Homann PH (1975) Kinetic analysis of the fluorescence induction in 3-(3,4- dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts. Photochem Photobiol 21:431–437Google Scholar
  69. Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350PubMedGoogle Scholar
  70. 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 1657:33–46PubMedGoogle Scholar
  71. 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 1657:47–60PubMedGoogle Scholar
  72. 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 61:674–680Google Scholar
  73. 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 595–598Google Scholar
  74. 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 9:1–21PubMedCentralPubMedGoogle Scholar
  75. Nagy L, Maroti P, Terazima M (2008) Spectrally silent light induced conformation change in photosynthetic reaction centers. FEBS Lett 582:3657–3662PubMedGoogle Scholar
  76. 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:1246–1254Google Scholar
  77. 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 35:265–274PubMedGoogle Scholar
  78. Osváth S, Meszéna G, Barzda V, Garab G (1994) Trapping magnetically oriented chloroplast thylakoid membranes in gels for electric measurements. J Photochem Photobiol, B 26:287–292Google Scholar
  79. Paillotin G (1976) Movement of excitations in photosynthetic domains of photosystem II. J Theor Biol 58:237–252Google Scholar
  80. Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19., Advances in photosynthesis and respiration. Springer, Dordrecht 818 ppGoogle Scholar
  81. 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 177–206Google Scholar
  82. Pospíšil P, Dau H (2002) Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients. Biochim Biophys Acta 1554:94–100PubMedGoogle Scholar
  83. Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around Photosystem II in vivo. Photosynth Res 48:395–410PubMedGoogle Scholar
  84. 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 635:132–148PubMedGoogle Scholar
  85. 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 130:4431–4446PubMedGoogle Scholar
  86. 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 477–480Google Scholar
  87. 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 151–176Google Scholar
  88. 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 1276:147–153Google Scholar
  89. Samson G, Prášil O, Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 37:163–182Google Scholar
  90. Satoh K (1981) Fluorescence induction and activity of ferredoxin-NADP+ reductase in Bryopsis chloroplasts. Biochim Biophys Acta 638:327–333Google Scholar
  91. Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151PubMedGoogle Scholar
  92. Schansker G, van Rensen JJS (1999) Performance of active photosystem II centers in photoinhibited pea leaves. Photosynth Res 62:175–184Google Scholar
  93. 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 1706:250–261PubMedGoogle Scholar
  94. 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 1757:787–797PubMedGoogle Scholar
  95. 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 951–955Google Scholar
  96. 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 1807:1032–1043PubMedGoogle Scholar
  97. 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 187–190Google Scholar
  98. Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272PubMedGoogle Scholar
  99. 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 23–47Google Scholar
  100. 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 279–319Google Scholar
  101. Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293PubMedGoogle Scholar
  102. Schreiber U, Neubauer C, Klughammer C (1989) Devices and methods for room-temperature fluorescence analysis. Philos Trans R Soc Lond B 323:241–251Google Scholar
  103. 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 22:209–220Google Scholar
  104. 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 88:412–421PubMedCentralPubMedGoogle Scholar
  105. Sokolove PM, Marsho TV (1979) The effect of valinomycin on electron transport in intact spinach chloroplasts. FEBS Lett 100:179–184PubMedGoogle Scholar
  106. 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 40:173–180PubMedGoogle Scholar
  107. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61PubMedGoogle Scholar
  108. 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 513–524Google Scholar
  109. 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 423–426Google Scholar
  110. 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 977–980Google Scholar
  111. 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 321–362Google Scholar
  112. Szczepaniak M, Sugiura M, Holzwarth AR (2008) The role of TyrD in the electron transfer kinetics in photosystem II. Biochim Biophys Acta 1777:1510–1517PubMedGoogle Scholar
  113. 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 96:621–631PubMedCentralPubMedGoogle Scholar
  114. 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 31:469–477Google Scholar
  115. 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 1708:275–282PubMedGoogle Scholar
  116. 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 162:181–194PubMedGoogle Scholar
  117. 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 1767:295–305PubMedGoogle Scholar
  118. Tóth SZ, Schansker G, Strasser RJ (2007b) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203PubMedGoogle Scholar
  119. 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 149:1568–1578PubMedCentralPubMedGoogle Scholar
  120. 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 22:183–193Google Scholar
  121. van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150PubMedGoogle Scholar
  122. van Wijk KJ, Krause GH (1991) O2-dependence of photoinhibition at low temperature in intact protoplasts of Locusta valerianella L. Planta 186:135–142PubMedGoogle Scholar
  123. 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 37:11046–11054PubMedGoogle Scholar
  124. Vernotte C, Etienne AL, Briantais J-M (1979) Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545:519–527PubMedGoogle Scholar
  125. Vredenberg WJ (2000) A three-state model for energy trapping and chlorophyll fluorescence in photosystem II incorporating radical pair recombination. Biophys J 79:26–38PubMedCentralPubMedGoogle Scholar
  126. 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 133–172Google Scholar
  127. 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 96:83–97PubMedGoogle Scholar
  128. Vredenberg WJ (2011) Kinetic analysis and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. Biosystems 103:138–151PubMedGoogle Scholar
  129. Vredenberg WJ, Bulychev AA (2002) Photo-electrochemical control of photosystem II chlorophyll fluorescence in vivo. Bioelectrochemistry 57:123–128PubMedGoogle Scholar
  130. Vredenberg WJ, Bulychev A (2003) Photoelectric effects on chlorophyll fluorescence of photosystem II in vivo. Kinetics in the absence and presence of valinomycin. Bioelectrochemistry 60:87–95PubMedGoogle Scholar
  131. 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 1757:173–181PubMedGoogle Scholar
  132. 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 93:183–192PubMedGoogle Scholar
  133. Vredenberg W, Durchan M, Prášil O (2012) The analysis of PS II photochemical activity using single and multi-turnover excitations. J Photochem Photobiol, B 107:45–54Google Scholar
  134. Wientjes E, Croce R (2012) PMS: photosystem I electron donor or fluorescence quencher. Photosynth Res 111:185–191PubMedCentralPubMedGoogle Scholar
  135. 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 74:251–257PubMedGoogle Scholar
  136. 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 223:114–133PubMedGoogle Scholar
  137. 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 138:59–76Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of Plant Biology, Biological Research Center Szeged, Hungarian Academy of SciencesSzegedHungary
  2. 2.Max-Planck-Institute for Chemical Energy ConversionMülheim an der RuhrGermany

Personalised recommendations