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Photosynthesis Research

, Volume 113, Issue 1–3, pp 15–61 | Cite as

Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise

  • Alexandrina Stirbet
  • Govindjee
Review

Abstract

The fast (up to 1 s) chlorophyll (Chl) a fluorescence induction (FI) curve, measured under saturating continuous light, has a photochemical phase, the O–J rise, related mainly to the reduction of QA, the primary electron acceptor plastoquinone of Photosystem II (PSII); here, the fluorescence rise depends strongly on the number of photons absorbed. This is followed by a thermal phase, the J–I–P rise, which disappears at subfreezing temperatures. According to the mainstream interpretation of the fast FI, the variable fluorescence originates from PSII antenna, and the oxidized QA is the most important quencher influencing the O–J–I–P curve. As the reaction centers of PSII are gradually closed by the photochemical reduction of QA, Chl fluorescence, F, rises from the O level (the minimal level) to the P level (the peak); yet, the relationship between F and [QA ] is not linear, due to the presence of other quenchers and modifiers. Several alternative theories have been proposed, which give different interpretations of the O–J–I–P transient. The main idea in these alternative theories is that in saturating light, QA is almost completely reduced already at the end of the photochemical phase O–J, but the fluorescence yield is lower than its maximum value due to the presence of either a second quencher besides QA, or there is an another process quenching the fluorescence; in the second quencher hypothesis, this quencher is consumed (or the process of quenching the fluorescence is reversed) during the thermal phase J–I–P. In this review, we discuss these theories. Based on our critical examination, that includes pros and cons of each theory, as well mathematical modeling, we conclude that the mainstream interpretation of the O–J–I–P transient is the most credible one, as none of the alternative ideas provide adequate explanation or experimental proof for the almost complete reduction of QA at the end of the O–J phase, and for the origin of the fluorescence rise during the thermal phase. However, we suggest that some of the factors influencing the fluorescence yield that have been proposed in these newer theories, as e.g., the membrane potential ΔΨ, as suggested by Vredenberg and his associates, can potentially contribute to modulate the O–J–I–P transient in parallel with the reduction of QA, through changes at the PSII antenna and/or at the reaction center, or, possibly, through the control of the oxidation–reduction of the PQ-pool, including proton transfer into the lumen, as suggested by Rubin and his associates. We present in this review our personal perspective mainly on our understanding of the thermal phase, the J–I–P rise during Chl a FI in plants and algae.

Keywords

Bioenergetics Chlorophyll a fluorescence Fluorescence induction OJIP transient Mathematical modeling Photosynthesis Thermal phase 

Notes

Acknowledgments

We are highly thankful to Dusan Lazár for a thorough analysis of the manuscript. His comments and suggestions helped us to improve significantly our review. We are equally grateful to Wim Vredenberg, as his criticism was very helpful in bringing more clarity to some ideas expounded here, and his advice has helped us in organizing our paper a bit better than before. Yet, as this review is a personal perspective, we are responsible for all the views expressed here. Govindjee thanks the office of Information Technology of Life Sciences at the UIUC, Urbana, Illinois (Jeff Hass, Director) and the Department of Plant Biology (Feng-Sheng Hu, Head), UIUC, Urbana, IL, USA for support during the preparation of this paper; this review was finalized when Govindjee was a Visiting Professor of Life Sciences, at the Jawaharlal Nehru University, New Delhi, India. Govindjee gives special thanks to Lisa Boise and Martha Plummer for their support for years before their retirement in June 2012.

References

  1. Allakhverdiev SI, Tsuchiya T, Watabe K, Kojima A, Los DA, Tomo T, Klimov VV, Mimuro M (2011) Redox potentials of primary electron acceptor quinone molecule (QA) and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc Natl Acad Sci USA 108:198054–198058CrossRefGoogle Scholar
  2. Antal TK, Rubin AB (2008) In vivo analysis of chlorophyll a fluorescence induction. Photosynth Res 96:217–226PubMedCrossRefGoogle Scholar
  3. Antal TK, Osipov V, Matorin DN, Rubin AB (2011) Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B 102:169–173. doi: 10.1016/j.jphotobiol.2010.11.005 PubMedCrossRefGoogle Scholar
  4. Asada K (2000) The water–water cycle an alternative photon and electron sinks. Philos Trans R Soc Lond B 3555:1419–1431CrossRefGoogle Scholar
  5. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedCrossRefGoogle Scholar
  6. Baake E, Schlöder JP (1992) Modelling the fast fluorescence rise of photosynthesis. Bull Math Biol 54:999–1021Google Scholar
  7. Baake E, Strasser RJ (1990) A differential equation model for the description of the fast fluorescence rise (O–I–D–P-Transient) in leaves. In: Baltscheffsky M (ed) Current research in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 567–570Google Scholar
  8. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:659–668CrossRefGoogle Scholar
  9. Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Structure–function of the cytochrome b6f complex. Photochem Photobiol 84:1349–1358PubMedCrossRefGoogle Scholar
  10. Barber J (1980) Membrane surface charges and potentials in relation to photosynthesis. Biochim Biophys Acta 594:253–308PubMedCrossRefGoogle Scholar
  11. Barzda V, Vengris M, Valkunas L, van Grondelle R, van Amerongen H (2000) Generation of fluorescence quenchers from the triplet states of chlorophylls in the major light harvesting complex II from green plants. Biochemistry 39:10468–10477PubMedCrossRefGoogle Scholar
  12. Belyaeva NE, Lebedeva GV, Riznichenko GYu (2003) Kinetic model of primary photosynthetic processes in chloroplasts. Modeling of thylakoid membranes electric potential. In: Riznichenko GYu (ed) Mathematics computer education, vol 10. Progress-Traditsiya, Moscow, pp 263–276Google Scholar
  13. Belyaeva NE, Paschenko VZ, Renger G, Riznichenko GYu, 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 51:976–990CrossRefGoogle Scholar
  14. Belyaeva NE, Schmitt F-J, Steffen R, Paschenko VZ, Riznichenko GYu, Chemeris YuK, Renger G, 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 98:105–119PubMedCrossRefGoogle Scholar
  15. Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GYu, Rubin AB, Renger G (2011) PS II model based analysis of transient fluorescence yield measured on whole leaves of Arabidopsis thaliana after excitation with light flashes of different energies. BioSystems 103:188–195PubMedCrossRefGoogle Scholar
  16. Bennoun P (1970) Reoxidation of the fluorescence quencher “Q” in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Biochim Biophys Acta 216:357–363PubMedCrossRefGoogle Scholar
  17. Bennoun P, Joliot P (1969) Étude a la photooxydation de l’hydroxylamine par les chloroplastes d’épinards. Biochim Biophys Acta 189:85–94PubMedCrossRefGoogle Scholar
  18. Bilger W, Schreiber U (1990) Chlorophyll luminescence as an indicator of stress-induced damage to the photosynthetic apparatus. Effect of heat-stress in isolated chloroplasts. Photosynth Res 25:161–171CrossRefGoogle Scholar
  19. Björkman O, Demmig E (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504CrossRefGoogle Scholar
  20. Bjorn LO, Papageorgiou GC, Blankenship R, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98PubMedCrossRefGoogle Scholar
  21. Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science, OxfordCrossRefGoogle Scholar
  22. Böhme H, Cramer WA (1971) Plastoquinone mediates electron transport between cytochrome b-559 and cytochrome f in spinach chloroplasts. FEBS Lett 15:349–351PubMedCrossRefGoogle Scholar
  23. Böhme H, Reimer S, Trebst A (1971) On the role of plastoquinone in photosynthesis. The effect of dibromothymoquinone on non cyclic and cyclic electron flow systems in isolated chloroplasts. Z Naturforsch 26b:341–352Google Scholar
  24. Boisvert S, Joly D, Carpentier R (2006) Quantitative analysis of the experimental O–J–I–P chlorophyll fluorescence induction kinetics. Apparent activation energy and origin of each kinetic step. FEBS J 273:4770–4777PubMedCrossRefGoogle Scholar
  25. Bouges B (1971) Action de faibles concentrations d’hydroxylamine sur l’émission d’oxygène des algues Chlorella et des chloroplastes d’épinards. Biochim Biophys Acta 234:103–112PubMedCrossRefGoogle Scholar
  26. Boussac A, Sugiura M, Rappaport F (2011) Probing the quinone binding site of Photosystem II from Thermosynechococcus elongatus containing either PsbA1 or PsbA3 as the D1 protein through the binding characteristics of herbicides. Biochim Biophys Acta 1807:119–129PubMedCrossRefGoogle Scholar
  27. Bowes JM, Crofts AR (1981) Effect of 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone on the secondary electron acceptor B of photosystem II. Arch Biochem Biophys 209:682–686. doi: 10.1016/0003-9861(81)90329-5 PubMedCrossRefGoogle Scholar
  28. Bradbury M, Baker NR (1983) Analysis of the induction of chlorophyll fluorescence in leaves and isolated thylakoids: contributions of photochemical and non-photochemical quenching. Proc R Soc Lond B 220:251–264. doi: 10.1098/rspb.1983.0098 CrossRefGoogle Scholar
  29. Breton J (1982) The 692 nm fluorescence (F695) of chloroplasts at low temperature is emitted from the primary acceptor of photosystem II. FEBS Lett 147:16–20CrossRefGoogle Scholar
  30. Briantais J-M, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138PubMedCrossRefGoogle Scholar
  31. Briantais J-M, Vernotte C, Krause GH, Weis E (1986) Chlrophyll a fluorescence of higher plants: chloroplasts and leaves. In: Govindjee, Amesz J, Fork DJ (eds) Light emission by plants and bacteria. Academic Press, New York, pp 539–583Google Scholar
  32. Bruce D, Samson G, Carpenter C (1997) The origins of nonphotochemical quenching of chlorophyll fluorescence in photosynthesis. Direct quenching by P680+ in photosystem II enriched membranes at low pH. Biochemistry 36:749–775PubMedCrossRefGoogle Scholar
  33. 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 723:366–371CrossRefGoogle Scholar
  34. Bukhov NG, Govindachary S, Egorova EA, Joly D, Carpentier R (2003) N, N, NV, NV-Tetramethyl-p-phenylenediamnine 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
  35. Bulychev AA, Niyazova MM (1989) Modelling of potential-depending changes of chlorophyll fluorescence in the photosystem 2. Biofizika 34:63–67 (in Russian)Google Scholar
  36. Bulychev AA, Vredenberg WJ (1999) Light-triggered electrical events in the thylakoid membrane of plant chloroplasts. Phys Plantarum 105:577–584CrossRefGoogle Scholar
  37. Bulychev AA, Vredenberg WJ (2001) Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I. Bioelectrochemistry 54:157–168PubMedCrossRefGoogle Scholar
  38. Bulychev AA, Niyazova MM, Turovetsky VB (1986) Electro-induced changes of chlorophyll fluorescence in individual intact chloroplasts. Biochim Biophys Acta 850:218–225CrossRefGoogle Scholar
  39. Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b 559 in oxygen-evolving photosystem II. Biochemistry 31:11449–11459PubMedCrossRefGoogle Scholar
  40. Butler WL (1966) Fluorescence yield in photosynthetic systems and its relation to electron transport. Curr Top Bioenerg 1:49–73Google Scholar
  41. Butler WL (1972) On the primary nature of fluorescence yield changes associated with photosynthesis. Proc Natl Acad Sci USA 69:3420–3422PubMedCrossRefGoogle Scholar
  42. Butler WL (1980) Energy transfer between photosystem II units in a connected package model of the photochemical apparatus of photosynthesis. Proc Natl Acad Sci USA 77:4694–4701CrossRefGoogle Scholar
  43. Butler WL, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376:116–125PubMedCrossRefGoogle Scholar
  44. Butler WL, Strasser RJ (1977a) Does the rate of cooling affect fluorescence properties of chloroplasts at −196 °C. Biochim Biophys Acta 462:283–289PubMedCrossRefGoogle Scholar
  45. Butler WL, Strasser RJ (1977b) Effect of divalent cations on energy coupling between the light-harvesting chlorophyll a/b complex and PS II. In: Hall DA, Coombs J, Goodwin TW (eds) Photosynthesis 77. The Biochemical Society, London, pp 11–20Google Scholar
  46. Butler WL, Visser J, Simorts HL (1973) The kinetics of light-induced changes of C-550, cytochrome b559 and fluorescence yield in chloroplasts at low temperature. Biochim Biophys Acta 292:140–151PubMedCrossRefGoogle Scholar
  47. Byrdin M, Rimke I, Schlodder E, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–1007PubMedCrossRefGoogle Scholar
  48. Cao J, Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive photosystem-II in thylakoid membranes. Biochim Biophys Acta 1015:180–188PubMedCrossRefGoogle Scholar
  49. Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918PubMedCrossRefGoogle Scholar
  50. Cessna S, Demmig-Adams B, Adams WW III (2010) Exploring photosynthesis and plant stress using inexpensive chlorophyll fluorometers. JNRLSE 39:22–30Google Scholar
  51. Chen S, Yin C, Strasser RJ, Govindjee, Yang C, Qiang S (2012) Reactive oxygen species from chloroplasts contribute to 3-acetyl-5-isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana. Plant Physiol Biochem 52:38–51PubMedCrossRefGoogle Scholar
  52. Christen G, Reifarth F, Renger G (1998) On the origin of the ‘35-μs kinetics’ of P680+ reduction in photosystem II with an intact water oxidizing complex. FEBS Lett 249:49–52CrossRefGoogle Scholar
  53. Clegg RM, Sener M, Govindjee (2010) From Forster resonance energy transfer (FRET) to coherent resonance energy transfer (CRET) and back-A wheen o’mickles mak’s a muckle. In: Alfano RR (ed) Optical Biopsy VII, Proceedings of SPIE, vol 7561, SPIE, Bellingham, WA, pp 7561–7572. CID number: 75610C, 2010, 21 ppGoogle Scholar
  54. Codrea MC, Hakala-Yatkin M, Karlund-Marttila A, Nedbal L, Aittokallio T, Nevalainen OS, Tyystjärvi E (2010) Mahalanobis distance screening of Arabidopsis mutants with chlorophyll fluorescence. Photosynth Res 105:273–283PubMedCrossRefGoogle Scholar
  55. Cramer WA, Zhang H (2006) Consequences of the structure of the cytochrome b6f complex for its charge transfer pathways. Biochim Biophys Acta 1757:339–345PubMedCrossRefGoogle Scholar
  56. Cramer WA, Zhang H, Yan J, Kurrisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b6f complex. Ann Rev Biochem 75:769–790PubMedCrossRefGoogle Scholar
  57. Crofts AR (2004) The Q-cycle-a personal perspective. Photosynth Res 80:223–243PubMedCrossRefGoogle Scholar
  58. Crofts AR, Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185CrossRefGoogle Scholar
  59. Crofts AR, Robinson HH, Snozzi M (1984) Reactions of quinones at catalytic sites; a diffusional role in H-transfer. In: Sybesma C (ed) Advances in photosynthesis research, vol I. Martinus Nijhoff/Dr W Junk Publishers, The Hague, pp 461–468Google Scholar
  60. Cuni A, Xiong L, Sayre RT, Rappaport F, Lavergne J (2004) Modification of the pheophytin midpoint potential in Photosystem II: modulation of the quantum yield of charge separation and of charge recombination pathways. Phys Chem Chem Phys 6:4825–4831CrossRefGoogle Scholar
  61. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Nemann DS, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285PubMedCrossRefGoogle Scholar
  62. Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23CrossRefGoogle Scholar
  63. 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 1089:49–60CrossRefGoogle Scholar
  64. Dau H, Sauer K (1992) Electric field effect on the picosecond fluorescence of photosystem II and its relation to the energetics and kinetics of primary charge separation. Biochim Biophys Acta 1102:91–106CrossRefGoogle Scholar
  65. Dau H, Windecker R, Hansen UP (1991) Effect of light-induced changes in thylakoid voltage on chlorophyll fluorescence of Aegopodium podagraria leaves. Biochim Biophys Acta 1057:337–345CrossRefGoogle Scholar
  66. Delosme R (1967) Étude de l’induction de fluorescence des algues vertes et des chloroplastes au début d’une illumination intense. Biochim Biophys Acta 143:108–128PubMedCrossRefGoogle Scholar
  67. 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
  68. Delosme R, Joliot P (2002) Period four oscillations in chlorophyll a fluorescence. Photosynth Res 73:165–168PubMedCrossRefGoogle Scholar
  69. Den Haan GA, Duysons LNM, Egberts DJN (1974) Fluorescence yield kinetics in the microsecond range in Chlurella pyrenoidosa and spinach chloroplasts in the presence of hydroxylamine. Biochim Biophys Acta 368:409–421CrossRefGoogle Scholar
  70. Diner B, Joliot P (1976) Effect of the transmembrane electric field on the photochemical and quenching properties of photosystem II in vivo. Biochim Biophys Acta 423:479–498PubMedCrossRefGoogle Scholar
  71. Diner BA, Petrouleas V (1987) Q400, the non-heme iron of the Photosystem II iron-quinone complex. A spectroscopic probe of quinone and inhibitor binding to the reaction center. Biochim Biophys Acta 895:107–125CrossRefGoogle Scholar
  72. Duysens LMN, Sweers HT (1963) 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, University of Tokyo Press, Tokyo, pp 353–372Google Scholar
  73. Duysens LNM, van der Schatte-Olivier TE, den Haan GA (1972) Light induced quenching of the yield of chlorophyll a2 fluorescence, with microsecond back reaction stimulated by oxygen. In: Schenck GO (ed) Progress in photobiology, Proceedings of the VI International Congress on Photobiology held in Bochum 1972, Abstract No. 277Google Scholar
  74. Duysens LNM, Den Haan GA, Van Best JA (1975) Rapid reactions of photosystem II as studied by the kinetics of fluorescence and luminescence of chlorophyll a in Chlorella pyrenoidosa. In: Avron M (ed) Proceedings of the Third International Congress on Photosynthesis. Elsevier, Amsterdam, pp 1–21Google Scholar
  75. Eaton-Rye JJ, Govindjee (1988a) Electron transfer through the quinone acceptor complex of Photosystem II in bicarbonate-depleted spinach thylakoid membranes as a function of actinic flash number and frequency. Biochim Biophys Acta 935:237–247. doi: 10.1016/0005-2728(88)90220-4 CrossRefGoogle Scholar
  76. Eaton-Rye JJ, Govindjee (1988b) Electron transfer through the quinone acceptor complex of photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes. Biochim Biophys Acta 935:248–257. doi: 10.1016/0005-2728(88)90221-6 CrossRefGoogle Scholar
  77. Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) (2011) Photosynthesis: plastid biology, energy conversion and carbon assimilation, advances in photosynthesis and respiration, vol 34. Advances in photosynthesis and respiration (Series eds, Govindjee, Sharkey TD). Springer, DordrechtGoogle Scholar
  78. Eckert HJ, Renger G (1980) Photochemistry of the reaction centers of system II under repetitive flash group excitation in isolated chloroplasts. Photochem Photobiol 31:501–511. doi: 10.1111/j.1751-1097.1980.tb03736.x CrossRefGoogle Scholar
  79. Eckert HJ, Wiese N, Bernarding J, Eichler HJ, Renger G (1988) Analysis of the electron transfer from Phe to QA in PS II membrane fragments from spinach by time-resolved 325 nm absorption changes in the picosecond domain. FEBS Lett 240:153–158PubMedCrossRefGoogle Scholar
  80. Eftink MR (1991) Fluorescence quenching: theory and applications. In: Lakowicz JR (ed) Topics in fluorescence spectroscopy, principles, vol 2. Plenum, New York, pp 53–126CrossRefGoogle Scholar
  81. Erixon K, Butler WL (1971) The relationship between Q, C-550 and cytochrome b 559 in photoreactions at −196° in chloroplasts. Biochim Biophys Acta 234:381–389PubMedCrossRefGoogle Scholar
  82. Etienne AL, Lavergne J (1972) Action du m-dinitrobenzene sur la phase thermique d’induction de fluorescence en photosynthèse. Biochim Biophys Acta 283:268–278PubMedCrossRefGoogle Scholar
  83. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, NJGoogle Scholar
  84. Flexas J, Escalona J, Evain S, Gulias J, Moya M, Osmond CB, Medrano H (2002) Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water stress in C3 plants. Physiol Plantarum 114:231–240CrossRefGoogle Scholar
  85. Forster B, Osmond CB, Pogson BJ (2011) Lutein from deepoxidation of lutein epoxide replaces zeaxanthin to sustain an enhanced capacity for nonphotochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark. Plant Physiol 156:393–403PubMedCrossRefGoogle Scholar
  86. Gauthier A, Joly D, Boisvert S, Carpentier R (2010) Period-four modulation of photosystem II primary quinone acceptor (QA) reduction/oxidation kinetics in thylakoid membranes. Photochem Photobiol 86:1064–1070PubMedCrossRefGoogle Scholar
  87. Genty B, Wonders J, Baker NR (1990) Nonphotochemical quenching of F0 in leaves is emission wavelength dependent. Consequences for quenching analysis and its interpretation. Photosynth Res 26:133–139CrossRefGoogle Scholar
  88. Gibasiewicz K, Dobek A, Breton J, Leibl W (2001) Modulation of primary radical pair kinetics and energetics in photosystem II by the redox state of the quinone electron acceptor Q(A). Biophys J 80:1617–1630PubMedCrossRefGoogle Scholar
  89. Gilmore AM, Itoh S, Govindjee (2000) Global spectral kinetic analysis of room temperature chlorophyll a fluorescence from light harvesting antenna mutants of barley. Philos Trans Roy Soc Lond B 335:1–14Google Scholar
  90. Goltsev V, Yordanov I (1997) Mathematical model of prompt and delayed chlorophyll fluorescence induction kinetics. Photosynthetica 33:571–586Google Scholar
  91. Goltsev V, Zaharieva I, Lambrev P, Yordanov I, Strasser R (2003) Simultaneous analysis of prompt and delayed chlorophyll a fluorescence in leaves during the induction period of dark to light adaptation. J Theor Biol 225:171–183PubMedCrossRefGoogle Scholar
  92. Goltsev V, Chernev P, Zaharieva I, Lambrev P, Strasser R (2005) Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. Photosynth Res 84:209–215PubMedCrossRefGoogle Scholar
  93. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101:217–232PubMedCrossRefGoogle Scholar
  94. Goth CH, Schreiber U, Hedrich R (1999) New approach of monitoring changes in chlorophyll-a fluorescence of single guard-cells and protoplasts in response to physiological stimuli. Plant Cell Environ 22:1057–1070CrossRefGoogle Scholar
  95. Govindjee (1990) Photosystem II heterogeneity: the acceptor side. Photosynth Res 25:151–160CrossRefGoogle Scholar
  96. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160CrossRefGoogle Scholar
  97. 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. Springer, Dordrecht, pp 1–41Google Scholar
  98. Govindjee, Jursinic P (1979) Photosynthesis and fast changes in light emission by green plants. Photochem Photobiol Rev 4:125–205CrossRefGoogle Scholar
  99. Govindjee, Papageorgiou GC (1971) Chlorophyll fluorescence and photosynthesis: fluorescence transients. Photophysiology 6:1–50Google Scholar
  100. Govindjee, Satoh K (1986) Fluorescence properties of chlorophyll b- and chlorophyll c-containing algae. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 497–537Google Scholar
  101. Govindjee, Seufferheld M (2002) Non-photochemical quenching of chlorophyll a fluorescence: early history and characterization of two xanthophyll cycle mutants of Chlamydomonas Reinhardtii. Funct Plant Biol 29:1141–1155CrossRefGoogle Scholar
  102. Govindjee, Ichimura S, Cederstrand C, Rabinowitch E (1960) Effect of combining far-red light with shorter wave light on the excitation of fluorescence in Chlorella. Arch Biochem Biophys 89:322–323PubMedCrossRefGoogle Scholar
  103. Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, OrlandoGoogle Scholar
  104. Govindjee, Kern J, Messinger J, Whitmarsh J (2010) Photosystem II. In: Encyclopedia of life sciences (ELS). Wiley, Chichester. doi: 10.1002/9780470015902.a0000669.pub2
  105. Graan T, Ort DR (1983) Initial events in the regulation of electron transfer in chloroplasts. The role of the membrane potential. J Biol Chem 258:2831–2836PubMedGoogle Scholar
  106. Grabolle M, Dau H (2007) Efficiency and role of loss processes in light-driven water oxidation by PSII. Physiol Plant 131:50–63PubMedCrossRefGoogle Scholar
  107. Gross EL, Hess SC (1973) Monovalent cation induced inhibition of chlorophyll a fluorescence: antagonism by divalent cations. Arch Biochem Biophys 159:832–836CrossRefGoogle Scholar
  108. Guissé B, Srivastava A, Strasser RJ (1995) The polyphasic rise of the chlorophyll a fluorescence (O–K–J–I–P) in heat stressed leaves. Arch Sci Genève 48:147–160Google Scholar
  109. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  110. Haldimann P, Tsimilli-Michael M (2005) Non-photochemical quenching of chlorophyll a fluorescence by oxidized plastoquinone: new evidences based on modulation of the redox state of the endogenous plastoquinone pool in broken spinach chloroplasts. Biochim Biophys Acta 1706:239–249PubMedCrossRefGoogle Scholar
  111. Hansen U-P, Dau H, Brüning B, Fritsch T, Moldaenke C (1991) Linear analysis applied to the comparative study of the I-D-P phase of chlorophyll fluorescence as induced by actinic PS-II light, PS-I light and changes in CO2-concentration. Photosynth Res 28:119–130CrossRefGoogle Scholar
  112. Heber U, Kobayashi Y, Leegood RC, Walker DA (1985) Low fluorescence yield in anaerobic chloroplasts and stimulation of chlorophyll a fluorescence by oxygen and inhibitors that block electron flow between photosystem II and I. Proc Royal Soc B London 225:41–53CrossRefGoogle Scholar
  113. Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926PubMedCrossRefGoogle Scholar
  114. Homann P (1969) Cation effects on the fluorescence of isolated chloroplasts. Plant Physiol 44:932–936PubMedCrossRefGoogle Scholar
  115. Horton P, Bowyer JR (1990) Chlorophyll fluorescence transients. In: Harwood J, Bowyer JR (eds) Methods in plant biochemistry. Academic Press, London, pp 259–296Google Scholar
  116. Hsu B-D (1992) A theoretical study on the fluorescence induction curve of spinach thylakoids in the absence of DCMU. Biochim Biophys Acta 1140:30–36CrossRefGoogle Scholar
  117. Hsu B-D (1993) Evidence for the contribution of the S-state transitions of oxygen evolution to the initial phase of fluorescence induction. Photosynth Res 36:81–88. doi: 10.1007/BF00016272 CrossRefGoogle Scholar
  118. Ilik P, Schansker G, Kotabova E, Vaczi P, Strasser RJ, Bartak M (2006) A dip in the chlorophyll fluorescence induction at 0.2–2 s in Trebouxia-possesing lichens reflects a fast reoxidation of photosystem I. A comparison with higher plants. Biochim Biophys Acta 1757:12–20PubMedCrossRefGoogle Scholar
  119. Itoh S (1980) Correlation between the time coarse of millisecond delayed fluorescence and that of prompt fluorescence at low temperature in uncoupled spinach chloroplasts. Plant Cell Physiol 21:873–884Google Scholar
  120. Jablonsky J, Lazár D (2008) Evidence for intermediate S-states as initial phase in the process of oxygen-evolving complex oxidation. Biophys J 94:2725–2736PubMedCrossRefGoogle Scholar
  121. Jablonsky J, Susila P, Lazar D (2008) Impact of dimeric organization of enzyme on its function: the case of photosynthetic water splitting. Bioinformatics 24:2755–2759PubMedCrossRefGoogle Scholar
  122. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389PubMedCrossRefGoogle Scholar
  123. Johnson GN, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229:202–207CrossRefGoogle Scholar
  124. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322PubMedCrossRefGoogle Scholar
  125. Joliot A, Joliot P (1964) Étude cinétique de la réaction photochimique libérant l’oxygène au cours de la photosynthèse. CR Acad Sci Paris 258:4622–4625 (in French)Google Scholar
  126. Joliot P, Joliot A (1973) Different types of quenching involved in photosystem II centers. Biochim Biophys Acta 305:302–316CrossRefGoogle Scholar
  127. Joliot P, Joliot A (1977) Evidence for a double hit process in photosystem II based on fluorescence studies. Biochim Biophys Acta 462:559–574PubMedCrossRefGoogle Scholar
  128. Joliot P, Joliot A (1979) Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. Biochim Biophys Acta 546:93–105PubMedCrossRefGoogle Scholar
  129. Joliot P, Joliot A (1981a) A photosystem II electron acceptor which is not a plastoquinone. FEBS Lett 134:155–158CrossRefGoogle Scholar
  130. Joliot P, Joliot A (1981b) Characterization of photosystem II centers by polarographic, spectroscopic and fluorescence methods. In: Akoyunoglou G (ed) Photosynthesis III. Balaban International Science Services, Philadelphia, pp 885–899Google Scholar
  131. Joliot P, Joliot A, Johnson G (2006) Cyclic electron transfer around photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin: ferredoxin oxidoreductase. Advances in photosynthesis and respiration, vol 24. Springer, Dordrecht, pp 639–656Google Scholar
  132. Joly D, Carpentier R (2009) Sigmoidal reduction kinetics of the photosystem II acceptor side in intact photosynthetic materials during fluorescence induction. Photochem Photobiol Sci 8:167–173. doi: 10.1039/B815070B PubMedCrossRefGoogle Scholar
  133. Joshi MK, Mohanty P (2004) Chlorophyll fluorescence as a probe of heavy metal ion toxicity in plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 637–661Google Scholar
  134. Jursinic P (1986) Delayed fluorescence: current concepts and status. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 291–328Google Scholar
  135. Jursinic P, Govindjee (1977) The rise in chlorophyll a fluorescence yield and decay in delayed light emission in Tris-washed chloroplasts in the 6–100 μs time range after an excitation flash. Biochim Biophys Acta 461:253–267PubMedCrossRefGoogle Scholar
  136. Jursinic P, Govindjee, Wraight CA (1978) Membrane potential and microsecond to millisecond delayed light emission after a single excitation flash on isolated chloroplasts. Photochem Photobiol 27:61–71CrossRefGoogle Scholar
  137. Kautsky H, Hirsch A (1931) Neue Versuche zur Kohlensaureassimilation. Naturwissenschaften 19:964CrossRefGoogle Scholar
  138. Kautsky H, Appel W, Amann H (1960) Chlorophyllfluorescenzkurve und Kohlensäureassimilation: XIII. Die fluorescenzkurve und die Photochemie der Pflanze. Biochem Z 332:277–292PubMedGoogle Scholar
  139. Ke B (2001) Photosynthesis: photobiochemistry and photobiophysics. Advances in photosynthesis and respiration (Series ed, Govindjee), vol 9. Kluwer Academic, DordrechtGoogle Scholar
  140. Kern J, Renger G (2007) Photosystem II: structure and mechanism of the water: plastoquinone oxidoreductase. Photosynth Res 94:183–202PubMedCrossRefGoogle Scholar
  141. Keuper HJK, Sauer K (1989) Effect of photosystem II reaction center closure on nanosecond relaxation kinetics. Photosynth Res 20:85–103CrossRefGoogle Scholar
  142. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115PubMedCrossRefGoogle Scholar
  143. Klevanik AV, Klimov VV, Shuvalov VA, Krasnovskii AA (1977) Reduction of pheophytin in the light reaction of Photosystem II of higher plant. Dokl Akad Nauk SSSR 236:241–244 (in Russian)Google Scholar
  144. Klimov VV (2003) Discovery of pheophytin function in the photosynthetic energy conversion as the primary electron acceptor of Photosystem II. Photosynth Res 76:247–253PubMedCrossRefGoogle Scholar
  145. Klimov VV, Klevanik AV, Shuvalov VA, Krasnovsky AA (1977) Reduction of pheophytin in the primary light reaction of photosystem II. FEBS Lett 82:183–186PubMedCrossRefGoogle Scholar
  146. Klimov VV, Allakhverdiev SI, Pashchenko VZ (1978) Measurement of the activation energy and lifetime of fluorescence of photosystem 2 chlorophyll. Dokl Akad Nauk SSSR 242:1204–1207 (in Russian)Google Scholar
  147. Klimov VV, Dolan E, Ke B (1980) EPR properties of an intermediary electron acceptor (pheophytin) in photosystem II reaction centers at cryogenic temperatures. FEBS Lett 112:97–100CrossRefGoogle Scholar
  148. Klimov VV, Shuvalov VA, Heber U (1985) Photoreduction of pheophytin as a result of electron donation from the water splitting system to photosystem II reaction centers. Biochim Biophys Acta 809:345–350CrossRefGoogle Scholar
  149. Klimov VV, Allakhverdiev SI, Ladygin VG (1986) Photoreduction of pheophytin in photosystem II of the whole cells of green algae and cyanobacteria. Photosynth Res 10:355–361CrossRefGoogle Scholar
  150. Klughammer C, Schreiber U (1998) Measuring P700 absorbance changes in the near infrared spectral region with a dual wavelength pulse modulation system. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol V. Kluwer, Dordrecht, pp 4357–4360Google Scholar
  151. Klughammer C, Schreiber U (2008) Non-photochemical fluorescence quenching and quantum yields in PS I and PS II: analysis of heat-induced limitations using Maxi-Imaging-PAM and Dual-PAM-100. PAM Appl Notes 1:15–18Google Scholar
  152. Koblizek M, Kaftan D, 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
  153. Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution I. A linear four step mechanism. Photochem Photobiol 11:457–475PubMedCrossRefGoogle Scholar
  154. Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106PubMedCrossRefGoogle Scholar
  155. Kolber Z, Klimov D, Ananyev G, Rascher U, Berry J, Osmond B (2005) Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of photosynthesis in terrestrial vegetation. Photosynth Res 84:121–129PubMedCrossRefGoogle Scholar
  156. Kramer DM, Crofts AR (1996) Control and measurement of photosynthetic electron transport in vivo. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publ, Dordrecht, pp 25–66Google Scholar
  157. Kramer DM, DiMarco G, 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. Kluwer Academic Publ, Dordrecht, pp 147–150Google Scholar
  158. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  159. Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of photosystem II. Photosynth Res 37:117–130CrossRefGoogle Scholar
  160. Kroon BMA, Thoms S (2006) From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth Mates. J Phycol 42:593–609CrossRefGoogle Scholar
  161. Küpper H, Šetlík I, Trtílek M, Nedbal L (2000) A microscope for two-dimensional measurements of in vivo chlorophyll fluorescence kinetics using pulsed measuring radiation, continuous actinic radiation, and saturating flashes. Photosynthetica 38:553–570CrossRefGoogle Scholar
  162. Kurreck J, Schödel R, 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
  163. Laisk A, Eichelmann H, Oja V (2006a) C3 photosynthesis in silico. Photosynth Res 90:45–46PubMedCrossRefGoogle Scholar
  164. Laisk A, Eichelmann H, Oja V, Rasulov B, Rämma H (2006b) Photosystem II cycle and alternative electron flow in leaves. Plant Cell Physiol 47:972–983PubMedCrossRefGoogle Scholar
  165. Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48:1575–1588PubMedCrossRefGoogle Scholar
  166. Laisk A, Nedbal L, Govindjee (eds) (2009a) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Advances in photosynthesis and respiration, vol 29. Springer, DordrechtGoogle Scholar
  167. Laisk A, Eichelmann H, Oja V (2009b) Leaf C3 photosynthesis in silico: integrated carbon/nitrogen metabolism. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Advances in photosynthesis and respiration, vol 29. Springer, Dordrecht, pp 295–322Google Scholar
  168. Laisk A, Talts E, Oja V, Eichelmann H, Peterson RB (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95PubMedCrossRefGoogle Scholar
  169. Latimer P, Bannister TT, Rabinowitch E (1956) Quantum yields of fluorescence of plant pigments. Science 124:585–586PubMedCrossRefGoogle Scholar
  170. Latimer P, Bannister TT, Rabinowitch E (1957) The absolute quantum yield of fluorescence of photosynthetically active pigment. In: Gaffron H et al (eds) Research in photosynthesis. Wiley, New York, pp 107–112Google Scholar
  171. Lavergne J, Leci E (1993) Properties of inactive photosystem II centers. Photosynth Res 38:323–343CrossRefGoogle Scholar
  172. Lavergne J, Rappaport F (1998) Stabilization of charge separation and photochemical misses in photosystem II. Biochemistry 37:7899–7906PubMedCrossRefGoogle Scholar
  173. 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 photosynthetic units. Biophys J 68:2474–2492PubMedCrossRefGoogle Scholar
  174. Lavorel J (1959) Induction of fluorescence in quinone poisoned Chlorella cells. Plant Physiol 34:204–209PubMedCrossRefGoogle Scholar
  175. Lavorel J (1962) Hétérogénéité de la chlorophylle in vivo I. Spectres d’émission de fluorescence. Biochim Biophys Acta 60:510–523PubMedCrossRefGoogle Scholar
  176. Lavorel J (1975) Luminescence. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 223–317Google Scholar
  177. Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28PubMedCrossRefGoogle Scholar
  178. 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 220:469–503PubMedCrossRefGoogle Scholar
  179. Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30Google Scholar
  180. 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 47:483–498CrossRefGoogle Scholar
  181. Lazár D, Jablonsky J (2009) 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 257:260–269Google Scholar
  182. 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 28:468–477PubMedCrossRefGoogle Scholar
  183. Lazár D, Schansker G (2009) Models of chlorophyll a fluorescence transients. In: Laisk, Nedbal AL, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Advances in photosynthesis and respiration, vol 29. Springer, Dordrecht, pp 85–123Google Scholar
  184. Lazár D, Nauš J, Matoušková M, Flašarová M (1997) Mathematical modeling of changes in chlorophyll fluorescence induction caused by herbicides. Pestic Biochem Physiol 57:200–210CrossRefGoogle Scholar
  185. Lazár D, Tomek P, Ilik P, Naus J (2001) Determination of the antenna heterogeneity of photosystem II by direct simultaneous fitting of several fluorescence rise curves measured with DCMU at different light intensities. Photosynth Res 68:247–257PubMedCrossRefGoogle Scholar
  186. Lazár D, Ilík P, Kruk J, Strzałka K, Nauš J (2005) A theoretical study on effect of the initial redox state of cytochrome b559 on maximal chlorophyll fluorescencelevel (FM): implications for photoinhibition of photosystem II. J Theor Biol 233:287–300PubMedCrossRefGoogle Scholar
  187. Lebedeva GV, Belyaeva NE, Riznichenko GY, Rubin AB, Demin OV (2000) Kinetic model of photosystem II of higher green plants. Russ J Phys Chem 74:1702–1710Google Scholar
  188. Lebedeva GV, Belyaeva NE, Demin OV, Riznichenko GY, Rubin AB (2002) A kinetic model of primary photosynthetic processes. Description of the fast phase of chlorophyll fluorescence induction under different light intensities. Biofizika 47:1044–1058PubMedGoogle Scholar
  189. Leibl W, Breton J, Deprez J, Trissl HW (1989) Photoelectric study on the kinetics of trapping and charge stabilization in oriented PS II membranes. Photosynth Res 22:257–275CrossRefGoogle Scholar
  190. Logan BA, Adams WW III, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Funct Plant Biol 34:853–859CrossRefGoogle Scholar
  191. Long SP, Postl WF, Bolhar-Nordenkampf HR (1993) Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic groupings. Planta 189:226–234CrossRefGoogle Scholar
  192. Malkin S (1966) Fluorescence induction studies in isolated chloroplasts. II. Kinetic analysis of the fluorescence intensity dependence on time. Biochim Biophys Acta 126:432–442Google Scholar
  193. Malkin S, Kok B (1966) Fluorescence induction studies in isolated chloroplasts. I-Number of components involved in the reaction and quantum yields. Biochim Biophys Acta 126:413–432PubMedCrossRefGoogle Scholar
  194. Malkin S, Wong D, Govindjee, Merkelo H (1980) Parallel measurements on fluorescence life-time and intensity changes from leaves during the fluorescence induction. Photobiochem Photobiophys 1:83–89Google Scholar
  195. Malkin S, Armond PA, Mooney HA, Fork DC (1981) Photosystem II photosynthetic unit sizes from fluorescence induction in leaves. Plant Physiol 67:570–579PubMedCrossRefGoogle Scholar
  196. Malkin S, Bilger W, Schreiber U (1994) The relationship between millisecond luminescence and fluorescence in tobacco leaves during the induction period. Photosynth Res 39:57–66CrossRefGoogle Scholar
  197. Mauzerall DC (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
  198. Mauzerall DC (1976) Fluorescence and multiple excitation in photosynthetic systems. J Phys Chim 80:2306–2309CrossRefGoogle Scholar
  199. Mauzerall DC (1978) Multiple excitation and the yield of chlorophyll a fluorescence in photosynthetic system. Photochem Photobiol 28:991–998CrossRefGoogle Scholar
  200. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  201. McConnell IL, Eaton-Rye JJ, van Rensen JJS (2011) Regulation of Photosystem II electron transport by bicarbonate. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration, vol 34 (Series eds, Govindjee, Sharkey TD). Springer, DordrechtGoogle Scholar
  202. McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967PubMedCrossRefGoogle Scholar
  203. Mehta P, Allakhverdiev SI, Jajoo A (2010) Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth Res 105:249–255PubMedCrossRefGoogle Scholar
  204. Mehta P, Kraslavsky V, Bharti S, Allakhverdiev SI, Jajoo A (2011) Analysis of salt stress induced changes in photosystem II heterogeneity by prompt fluorescence and delayed fluorescence in wheat (Triticum aestivum) leaves. J Photochem Photobiol B 104:308–313PubMedCrossRefGoogle Scholar
  205. Meiburg RF, van Gorkom HJ, van Dorssen RJ (1983) Excitation trapping and charge separation in photosystem II in the presence of an electric field. Biochim Biophys Acta 724:352–358CrossRefGoogle Scholar
  206. Melis A, Homann PH (1975) Kinetic analysis of the fluorescence induction in 3-(3,4-dichlorophenyl)-l,l-dimethylurea poisoned chloroplasts. Photochem Photobiol 21:431–437CrossRefGoogle Scholar
  207. Melis A, Homann PH (1976) Heterogeneity of photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350PubMedCrossRefGoogle Scholar
  208. Melis A, Schreiber U (1979) The kinetic relationship between the C-550 absorbance change, the reduction of Q(ΔA 320) and the variable fluorescence yield change in chloroplasts at room temperature. Biochim Biophys Acta 547:47–57. doi: 10.1016/0005-2728(79)90094-X PubMedCrossRefGoogle Scholar
  209. Miyake C, Yokota A (2001) Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiol 42:508–515PubMedCrossRefGoogle Scholar
  210. Miyake C, Yonekura K, Kobayashi Y, Yokota A (2002) Cyclic electron flow within PSII functions in intact chloroplasts from spinach leaves. Plant Cell Physiol 43:951–957PubMedCrossRefGoogle Scholar
  211. Mohanty P, Govindjee (1973) Light-induced changes in the fluorescence yield of chlorophyll a in Anacystis nidulans. II. The fast changes and the effect of photosynthetic inhibitors on both the fast and slow fluorescence induction. Plant Cell Physiol 14:611–629Google Scholar
  212. 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 1657:33–46PubMedCrossRefGoogle Scholar
  213. 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. doi: 10.1016/j.bbabio.2004.04.003 PubMedCrossRefGoogle Scholar
  214. 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
  215. Moya I, Cernovic ZG (2004) Remote sensing of chlorophyll fluorescence: Instrumentation and analysis. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 429–445Google Scholar
  216. Munday JC Jr, Govindjee (1969a) 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 9:1–21PubMedCrossRefGoogle Scholar
  217. Munday JC Jr, Govindjee (1969b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. IV. The effect of preillumination on the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:22–35PubMedCrossRefGoogle Scholar
  218. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371PubMedCrossRefGoogle Scholar
  219. Murata N (1969a) Control of excitation transfer in photosynthesis. I. Light-induced changes of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251PubMedCrossRefGoogle Scholar
  220. Murata N (1969b) Control of excitation energy transfer in photosynthesis. II. Magnesium ion dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim Biophys Acta 189:171–181PubMedCrossRefGoogle Scholar
  221. Murata N, Nishimura M, Takamiya A (1966) Fluorescence of chlorophyll in photosynthetic systems. II. Induction of fluorescence in isolated spinach chloroplasts. Biochim Biophys Acta 120:23–33PubMedCrossRefGoogle Scholar
  222. Nedbal L, Trtilek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of Photosystem II. J Photochem Photobiol B 48:154–157Google Scholar
  223. 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. Zeit Naturforschung 42c:1246–1254Google Scholar
  224. Nuijs AM, van Gorkom HJ, Plijter JJ, Duysens LNM (1986) Primary-charge separation and excitation of chlorophyll a in photosystem II particles from spinach as studied by picosecond absorbance-difference spectroscopy. Biochim Biophys Acta 848:167–175CrossRefGoogle Scholar
  225. Ohashi S, Miyashita H, Okada N, Iemura T, Watanabe T, Kobayashi M (2008) Unique photosystems in Acaryochloris marina. Photosynth Res 98:141–149PubMedCrossRefGoogle Scholar
  226. Okayama S, Butler WL (1972) The influence of cytochrome b 559 on the fluorescence yield of chloroplasts at low temperature. Biochim Biophys Acta 267:523–527PubMedCrossRefGoogle Scholar
  227. Okegawa Y, Kobayashi Y, Shikanai T (2010) Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. Plant J 63:458–468CrossRefGoogle Scholar
  228. Osmond CB, Forster B (2006) Photoinhibition: then and now. In: Demmig-Adams B, Adams W, Mattoo A (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, Netherlands, pp 11–22CrossRefGoogle Scholar
  229. Osmond CB, Schwartz O, Gunning B (1999) Photoinhibitory printing on leaves, visualized by chlorophyll fluorescence imaging and confocal microscopy, is due to diminished fluorescence from grana. Aust J Plant Physiol 26:717–724CrossRefGoogle Scholar
  230. Oxborough K, Baker NR (1997) An instrument capable of imaging chlorophyll-a fluorescence from intact leaves at very low irradiance and at cellular and subcellular levels of organization. Plant Cell Environ 20:1473–1483CrossRefGoogle Scholar
  231. Papageorgiou GC (1975) Chlorophyll fluorescence: an intrinsic probe of photosynthesis. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 319–372Google Scholar
  232. Papageorgiou GC (2011) Fluorescence emission from the photosynthetic apparatus. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration, vol 34 (Series eds, Govindjee, Sharkey TD). Springer, Dordrecht, p 29. doi: 10.1007/978-94-007-1579-0_18
  233. Papageorgiou GC, Govindjee (1968a) Light induced changes in the fluorescence yield of chlorophyll a in vivo. I. Anacystis nidulans. Biophys J 8:299–1315Google Scholar
  234. Papageorgiou GC, Govindjee (1968b) Light induced changes in the fluorescence yield of chlorophyll a in vivo. II. Chlorella pyrenoidosa. Biophys J 8:1316–1328PubMedCrossRefGoogle Scholar
  235. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, DordrechtGoogle Scholar
  236. Papageorgiou GC, Govindjee (2011) Photosystem II fluorescence: slow changes—scaling from the past. J Photochem Photobiol B: Biol 104:258–270. doi: 10.1016/j.jphotobiol.2011.03.008 CrossRefGoogle Scholar
  237. Papageorgiou GC, Tsimilli-Michael M, 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
  238. Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106:19–31PubMedCrossRefGoogle Scholar
  239. Peterson RB, Oja V, Laisk A (2001) Chlorophyll fluorescence at 680 and 730 nm and leaf photosynthesis. Photosynth Res 70:185–196PubMedCrossRefGoogle Scholar
  240. Petrouleas V, Diner BA (1987) Light-induced oxidation of the acceptor-side Fe(II) of photosystem-II by exogenous quinones acting through the QB binding-site.1. Quinones, kinetics and pH-dependence. Biochim Biophys Acta 893:126–137CrossRefGoogle Scholar
  241. Pfündel E (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195CrossRefGoogle Scholar
  242. Pospíšil P, Dau H (2000) Chlorophyll fluorescence transients of photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution. Photosynth Res 65:41–52PubMedCrossRefGoogle Scholar
  243. Pospíšil P, Dau H (2002) Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients. Biochim Biophys Acta 1554:94–100PubMedCrossRefGoogle Scholar
  244. Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395–410CrossRefGoogle Scholar
  245. Rappaport F, Blanchard-Desce M, Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184:178–192CrossRefGoogle Scholar
  246. Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41:8518–8527PubMedCrossRefGoogle Scholar
  247. Rappaport F, Cuni A, Xiong L, Sayre R, Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88:1948–1958PubMedCrossRefGoogle Scholar
  248. Rappaport F, Beal D, Joliot A, Joliot P (2007) On the advantages of using green light to study fluorescence yield changes in leaves. Biochim Biophys Acta 1767:56–65PubMedCrossRefGoogle Scholar
  249. Renger G (2010) The light reactions of photosynthesis. Curr Sci 98:1305–1319Google Scholar
  250. Renger G (2011) Photosynthetic water splitting: apparatus and mechanism. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration, vol 34 (Series eds, Govindjee, Sharkey TD). Springer, Dordrecht, p 51. doi: 10.1007/978-94-007-1579-0_17
  251. Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Berlin, pp 139–175Google Scholar
  252. Renger T, Schlodder E (2010) Primary photochemical processes in photosystem II: bridging the gap between crystal structure and optical spectra. Chem Phys Chem 11:1141–1153PubMedCrossRefGoogle Scholar
  253. Renger G, Schreiber U (1986) Practical applications of fluorometric methods to algae and higher plant research. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, New York, pp 587–620Google Scholar
  254. Renger G, Schulze A (1985) Quantitative analysis of fluorescence induction curves in isolated spinach chloroplasts. Photobiochem Photobiophys 9:79–87Google Scholar
  255. Renger G, Eckert HJ, Bergmann A, Bernarding J, Liu B, Napiwotzki A, Reifarth F, Eichler HJ (1995) Fluorescence and spectroscopic studies on exciton trapping and electron transfer in photosystem II of higher plants. Aust J Plant Physiol 22:167–181CrossRefGoogle Scholar
  256. Riznichenko G, Lebedeva G, Demin O, Rubin A (1999) Kinetic mechanisms of biological regulation in photosynthetic organisms. J Biol Phys 25:177–192CrossRefGoogle Scholar
  257. Riznichenko G, Lebedeva G, Demin O, Belyaeva NE, Rubin A (2000) Levels of regulation of photosynthetic processes. Biofizika 45:440–448Google Scholar
  258. Riznichenko GYu, Belyaeva NE, Kovalenko IB, Rubin AB (2009) Mathematical and computer modeling of primary photosynthetic processes. Biophysics 54:10–22CrossRefGoogle Scholar
  259. Robinson HH, Crofts AR (1984) Kinetics of proton uptake and the oxidation-reduction reactions of the quinone acceptor complex of photosystem II from pea chloroplasts. In: Sybesma C (ed) Advances in photosynthesis research, vol 1. Nijhoff M, Junk W Publishers, The Hague, pp 477–480Google Scholar
  260. Roelofs TA, Holzwarth AR (1990) In search of a putative long lived relaxed radical pair state in closed photosystem II. Kinetic modeling of picosecond fluorescence data. Biophys J 57:1141–1153PubMedCrossRefGoogle Scholar
  261. Roelofs TA, Lee C-H, Holzwarth AR (1992) Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts. A new approach to the characterization of the primary processes in photosystem II α- and β-units. Biophys J 61:1147–1163PubMedCrossRefGoogle Scholar
  262. Roháček K, Soukupová J, Barták M (2008) Chlorophyll fluorescence: a wonderful tool to study plant physiology and plant stress. Research Signpost, India, pp 41–104Google Scholar
  263. Rosenqvist E, van Kooten O (2003) Chlorophyll fluorescence: a general description and nomenclature. In: DeEll JR, Toivonen PMA (eds) Practical applications of chlorophyll fluorescence in plant biology. Kluwer Academic Publishers, Dordrecht, pp 31–78CrossRefGoogle Scholar
  264. Rottgers R (2007) Comparison of different variable chlorophyll a fluorescence techniques to determine photosynthetic parameters of natural phytoplankton. Deep-Sea Res I 54:437–451CrossRefGoogle Scholar
  265. Rubin AB, Riznichenko GYu (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. Springer, Dordrecht, pp 151–176Google Scholar
  266. Safranek D, Cerveny J, Klement M, Pospisilova J, Brim L, Lazár D, Nedbal L (2011) E-photosynthesis: web-based platform for modeling of complex photosynthetic processes. Biosystems 103:115–124. doi: 10.1016/j.biosystems.2010.10.013 PubMedCrossRefGoogle Scholar
  267. Samson G, Bruce D (1996) Origins of the low yield of chlorophyll a fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta 1276:147–153CrossRefGoogle Scholar
  268. Samson G, Prášil O, Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 37:163–182CrossRefGoogle Scholar
  269. Satoh K (1981) Fluorescence induction and activity of ferredoxin-NADP+ reductase in Bryopsis chloroplasts. Biochim Biophys Acta 638:327–333CrossRefGoogle Scholar
  270. Satoh K, Katoh S (1983) Induction kinetics of millisecond delayed luminescence in intact Bryopsis chloroplasts. Plant Cell Physiol 24:953–962Google Scholar
  271. Satoh K, Strasser R, Butler WL (1976) A demonstration of energy transfer from photosystem II to photosystem I in chloroplasts. Biochim Biophys Acta 440:337–345PubMedCrossRefGoogle Scholar
  272. Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151PubMedCrossRefGoogle Scholar
  273. Schansker G, Srivastava A, Govindjee, Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785–796CrossRefGoogle Scholar
  274. 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 1706:250–261PubMedCrossRefGoogle Scholar
  275. 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 1757:787–797PubMedCrossRefGoogle Scholar
  276. 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 945–949CrossRefGoogle Scholar
  277. Schansker G, Tóth ZS, 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 1807:1032–1043PubMedCrossRefGoogle Scholar
  278. Schatz GH, Holzwarth AR (1986) Mechanisms of chlorophyll fluorescence revisited: prompt or delayed emission from photosystem II with closed reaction centers? Photosynth Res 10:309–318CrossRefGoogle Scholar
  279. Schatz GH, Brock H, Holzwarth AR (1987) Picosecond kinetics of fluorescence and absorbance changes in photosystem II particles excited at low photon density. Proc Natl Acad Sci USA 84:9414–9418CrossRefGoogle Scholar
  280. Schatz GH, Brock H, Holzwarth AR (1988) A kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405PubMedCrossRefGoogle Scholar
  281. 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 187–190CrossRefGoogle Scholar
  282. Schmidt W, Schneckenburger H (1995) Induction kinetics of delayed luminescence in photosynthetic organisms as measured by an LED-based phosphorimeter. Photochem Photobiol 62:745–750CrossRefGoogle Scholar
  283. Schreiber U (1986) Detection of rapid induction kinetics with a new type of high frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272CrossRefGoogle Scholar
  284. Schreiber U (1998) Chlorophyll fluorescence: new instruments for special applications. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol V. Kluwer Academic Publishers, Dordrecht, pp 4253–4258Google Scholar
  285. Schreiber U (2002) Assessment of maximal fluorescence yield: donor-side dependent quenching and QB-quenching. In: Van Kooten O, Snel JFH (eds) Plant spectrofotometry: applications and basic research. Rozenberg Publishers, Amsterdam, pp 23–47Google Scholar
  286. 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. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 279–319Google Scholar
  287. Schreiber U, Krieger A (1996) Two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett 397:131–135PubMedCrossRefGoogle Scholar
  288. Schreiber U, Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the Photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c:1255–1264Google Scholar
  289. Schreiber U, Neubauer C (1989) Correlation between dissipative fluorescence quenching at photosystem II and 50 μs recombination luminescence. FEBS Lett 258:339–342CrossRefGoogle Scholar
  290. Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energisation and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293CrossRefGoogle Scholar
  291. Schreiber U, Schliwa U (1987) A solid state instrument for measurement of chlorophyll fluorescence induction in plants. Photosynth Res 11:173–182CrossRefGoogle Scholar
  292. Schreiber U, Vidaver W (1974) Chlorophyll fluorescence induction in anaerobic Scenedesmus obliquus. Biochim Biophys Acta 368:97–112PubMedCrossRefGoogle Scholar
  293. Schreiber U, Vidaver W (1976) The I-D fluorescence transient. An indicator of rapid energy distribution changes in photosynthesis. Biochim Biophys Acta 440:205–214PubMedCrossRefGoogle Scholar
  294. Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z Naturforsch 43c:686–698Google Scholar
  295. Schreiber U, Neubauer C, Klughammer C (1989) Devices and methods for room-temperature fluorescence analysis. Philos Trans R Soc Lond B 323:241–251CrossRefGoogle Scholar
  296. Schweitzer RH, Brudvig GW (1997) Fluorescence quenching by chlorophyll cations in photosystem II. Biochemistry 36:11351–11359PubMedCrossRefGoogle Scholar
  297. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217PubMedCrossRefGoogle Scholar
  298. Shinkarev VP, Govindjee (1993) Insight into the relationship of chlorophyll a fluorescence yield to the concentration of its natural quenchers in oxygenic photosynthesis. Proc Natl Acad Sci USA 90:7466–7469PubMedCrossRefGoogle Scholar
  299. Shinopoulos KE, Brudvig GW (2011) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta. doi: 10.1016/j.bbabio.2011.08.002 PubMedGoogle Scholar
  300. Shuvalov VA, Klimov VV (1976) The primary photoreactions in the complex cytochrome-P-890∙P-760 (bacteriopheophytin760) of Chromatium minutissimum at low redox potentials. Biochim Biophys Acta 440:587–599PubMedCrossRefGoogle Scholar
  301. Shuvalov VA, Klimov VV, Dolan E, Parson WW, Ke B (1980) Nanosecond fluorescence and absorbance changes in photosystem II at low redox potential. Pheophytin as an intermediary electron acceptor. FEBS Lett 118:279–282CrossRefGoogle Scholar
  302. Snel JFH, Dassen HHA (2000) Measurement of light and pH dependence of single-cell photosynthesis by fluorescence microscopy. J Fluoresc 10:269–273CrossRefGoogle Scholar
  303. Sorokin EM (1985) The induction curve of chlorophyll a fluorescence in DCMU-treated chloroplasts and its properties. Photobiochem Photobiophys 9:3–19Google Scholar
  304. Srivastava A, Strasser RJ, Govindjee (1995) Differential effects of dimethylbenzoquinone and dichlorobenzoquinone on chlorophyll fluorescence transient in spinach thylakoids. J Photochem Photobiol B Biol 31:163–169CrossRefGoogle Scholar
  305. Srivastava A, Strasser RJ, Govindjee (1999) Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37:365–392CrossRefGoogle Scholar
  306. Steffen R (2003) Time-resolved spectroscopic investigations of photosystem II. Ph.D Thesis, Technischen Universität BerlinGoogle Scholar
  307. 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. doi: 10.1021/bi0011779 PubMedCrossRefGoogle Scholar
  308. Steffen R, Eckert H-J, Kelly AA, Dörmann P, Renger G (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana by time-resolved fluorometric analysis. Biochemistry 44:3123–3133. doi: 10.1021/bi0484668 PubMedCrossRefGoogle Scholar
  309. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B: Biol 104:236–257CrossRefGoogle Scholar
  310. Stirbet A, Strasser JR (1995) Numerical simulation of the fluorescence induction in plants. Archs Sci Geneve 48:41–60Google Scholar
  311. Stirbet A, Strasser RJ (1996) Numerical simulation of the in vivo fluorescence in plants. Math Comp Sim 42:245–253CrossRefGoogle Scholar
  312. Stirbet A, Strasser RJ (2001) The possible role of pheophytin in the fast fluorescence rise OKJIP. In: Proceedings of the 12th International Congress on Photosynthesis, CSIRO Publishing, Colingwood.Google Scholar
  313. Stirbet A, Govindjee, Strasser BJ, Strasser RJ (1998) Chlorophyll a flurescence induction in higher plants: modelling and numerical simulation. J Theor Biol 193:131–151CrossRefGoogle Scholar
  314. Strasser RJ (1978) The grouping model of plant photosynthesis. In: Argyroudi-Akoyunoglou JH, Akoyunoglou G (eds) Chloroplast development. Elsevier Biomedical, Amsterdam, pp 513–538Google Scholar
  315. Strasser RJ (1981) The grouping model of plant photosynthesis: heterogeneity of photosynthetic units in thylakoids. In: Akoyunoglou G (ed) Photosynthesis: Proceedings of the Vth International Congress on Photosynthesis, Halkidiki, Greece 1980, Structure and Molecular Organisation of the Photosynthetic Apparatus, vol III. Balaban International Science Services, Philadelphia, pp 727–737Google Scholar
  316. 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
  317. Strasser RJ, Govindjee (1992) On the O–J–I–P fluorescence transients in leaves and D1 mutants of Chlamydomonas reinhardtii. In: Murata N (ed) Research in photosynthesis, vol II. Kluwer Academic Publishers, Dordrecht, pp 29–32Google Scholar
  318. Strasser RJ, Stirbet A (1998) Heterogeneity of photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O–J–I–P). Math Comput Simul 48:3–9CrossRefGoogle Scholar
  319. Strasser RJ, Stirbet A (2001) 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 Simul 56:451–461CrossRefGoogle Scholar
  320. 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 5. Kluwer Academic, The Netherlands, pp 977–980Google Scholar
  321. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42CrossRefGoogle Scholar
  322. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 443–480Google Scholar
  323. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 321–362Google Scholar
  324. Strasser RJ, Tsimilli-Michael M, Dangre D, Rai M (2007) Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. In: Varma A, Oelmüler R (eds) Advanced techniques in soil microbiology, soil biology. Springer, Berlin, pp 319–341CrossRefGoogle Scholar
  325. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326PubMedCrossRefGoogle Scholar
  326. Suggett DJ, Borowitzka MA, Prášil O (eds) (2010) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Developments in applied phycology, vol 4, 1st edn. Springer, DordrechtGoogle Scholar
  327. Sušila P, Lazár D, Ilík P, Tomek P, Nauš J (2004) The gradient of exciting radiation within a sample affects relative heights of steps in the fast chlorophyll a fluorescence rise. Photosynthetica 42:161–172CrossRefGoogle Scholar
  328. Thompson LK, Brudvig GW (1988) Cytochrome b-559 may function to protect photosystem II from photoinhibition. Biochemistry 27:6653–6658PubMedCrossRefGoogle Scholar
  329. Tomek P, Lazár D, Ilík P, Nauš J (2001) On the intermediate steps between the O and P steps in chlorophyll a fluorescence rise measured at different intensities of exciting light. Aust J Plant Physiol 28:1151–1160Google Scholar
  330. Tomek P, Ilík P, Lazár D, Štroch M, Nauš J (2003) On the determination of QB-non-reducing photosystem II centers from chlorophyll a fluorescence induction. Plant Sci 164:665–670CrossRefGoogle Scholar
  331. Tóth SZ, Schansker G, Strasser RJ (2005) In intact leaves, the maximum fluorescence level (FM) is independent of the redox state of the plastoquinone pool: a DCMU-inhibition study. Biochim Biophys Acta 1708:275–282PubMedCrossRefGoogle Scholar
  332. 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 1767:295–305PubMedCrossRefGoogle Scholar
  333. Tóth SZ, Schansker G, Strasser RJ (2007b) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203PubMedCrossRefGoogle Scholar
  334. Trebst A, Hart E, Draber W (1970) On a new inhibitor of photosynthetic electron transport. Z Naturforsch 25b:1157–1159Google Scholar
  335. Trissl H-W (2002) Theory of fluorescence induction: an introduction. http://www.biologie.uni-osnabrueck.de/biophysik/Trissl/teaching/teaching.html
  336. Trissl H-W, 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
  337. Trissl H-W, Gao Y, Wulf K (1993) Theoretical fluorescence induction curves derived from coupled differential equations describing the primary photochemistry of photosystem II by excition–radical pair equilibrium. Biophys J 64:974–988PubMedCrossRefGoogle Scholar
  338. Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art. Genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Dordrecht, pp 679–703Google Scholar
  339. Tyystjärvi E, Vass I (2004) Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: relation of prompt fluorescence to delayed light emission and thermoluminescence. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 363:388Google Scholar
  340. Tyystjärvi E, Rantamäki S, Tyystjärvi J (2009) Connectivity of photosystem II is the physical basis of retrapping in photosynthetic thermoluminescence. Biophys J 96:3735–3743PubMedCrossRefGoogle Scholar
  341. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  342. Van der Weij-de Wit CD, Dekker JP, van Grondelle R, van Stokkum IHM (2011) Charge separation is virtually irreversible in photosystem II core complexes with oxidized primary quinone acceptor. J Phys Chem 115:3947–3956CrossRefGoogle Scholar
  343. van Gorkom HJ (1986) Fluorescence measurements in the study of photosystem II electron transport. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, Ontario, pp 267–289Google Scholar
  344. van Gorkom HJ, Pulles MPJ, Etienne A-L (1978) Fluorescence and absorbance changes in Tris-washed chloroplasts. In: Metzner H (ed) Photosynthetic oxygen evolution. Academic Press, London, pp 135–145Google Scholar
  345. van Rensen JJS, Vredenberg WJ (2011) Adaptation of photosystem II to high and low light in wild-type and triazine-resistant Canola plants: analysis by a fluorescence induction algorithm. Photosynth Res 108:191–200PubMedCrossRefGoogle Scholar
  346. Vasilev S, Bruce D (1998) Non-photochemical 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
  347. Velthuys BR (1981) Electron dependent competition between plastoquinone and inhibitors for the binding to PSII. FEBS Lett 126:277–281CrossRefGoogle Scholar
  348. Velthuys BR, Amesz J (1974) Charges accumulation at the reducing side of system 2 of photosynthesis. Biochim Biophys Acta 333:85–94. doi: 10.1016/0005-2728(74)90165-0 PubMedCrossRefGoogle Scholar
  349. Vermaas WFJ, Govindjee (1981) The acceptor side of photosystem II in photosynthesis. Photochem Photobiol 34:775–793Google Scholar
  350. Vermaas WFJ, Renger G, Dohnt G (1984) The reduction of the oxygen evolving system in chloroplasts by thylakoid components. Biochim Biophys Acta 764:194–202CrossRefGoogle Scholar
  351. Vernotte C, Etienne AL, Briantais J-M (1979) Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545:519–527PubMedCrossRefGoogle Scholar
  352. Vredenberg WJ (2000) A Three-State Model for Energy Trapping and Chlorophyll Fluorescence in Photosystem II Incorporating Radical Pair Recombination. Biophys J 79:26–38PubMedCrossRefGoogle Scholar
  353. Vredenberg WJ (2004) System analysis of 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. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 133–172Google Scholar
  354. Vredenberg WJ (2008a) Algorithm for analysis of OJDIP fluorescence induction curves in terms of photo- and electrochemical events in photosystems of plant cells: derivation and application. J Photochem Photobiol B 91:58–65PubMedCrossRefGoogle Scholar
  355. Vredenberg WJ (2008b) 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 96:83–97PubMedCrossRefGoogle Scholar
  356. Vredenberg WJ (2009) Kinetic models of photosystem II should accommodate the effect on donor side quenching on variable fluorescence in the microsecond time range. Photosynth Res 102:99–101Google Scholar
  357. Vredenberg WJ (2011) Kinetic analysis and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. BioSystems 103:139–151CrossRefGoogle Scholar
  358. Vredenberg WJ, Bulychev AA (2002) Photoelectrochemical control of photosystem II chlorophyll fluorescence in vivo. Bioelectrochem 57:123–128CrossRefGoogle Scholar
  359. Vredenberg WJ, Bulychev AA (2003) Photoelectric effects on chlorophyll fluorescence of photosystem II in vivo. Kinetics in the absence and presence of valinomycin. Bioelectrochemistry 60:87–95PubMedCrossRefGoogle Scholar
  360. Vredenberg WJ, Duysens LNM (1963) Transfer and trapping of excitation energy from bacteriochlorophyll to a reaction center during bacterial photosynthesis. Nature 197:355–357PubMedCrossRefGoogle Scholar
  361. Vredenberg W, Prášil O (2009) Modeling of chlorophyll a fluorescence kinetics in plant cells: derivation of a descriptive algorithm. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico: understanding complexity from molecules to ecosystems. Advances in photosynthesis and respiration, vol 29. Springer, Dordrecht, pp 125–149Google Scholar
  362. Vredenberg WJ, Rodrigues GC, 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: PS2001 Proceedings: 12th International Congress on Photosynthesis, S14-10, CSIRO Publishing, Melbourne (CD-ROM)Google Scholar
  363. Vredenberg WJ, Kasalicky V, Durchan M, 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
  364. Vredenberg WJ, Durchan M, Prášil O (2007) On the chlorophyll a fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains. Photosynth Res 93:183–192PubMedCrossRefGoogle Scholar
  365. Vredenberg WJ, Durchan M, Prášil O (2012) The analysis of PS II photochemical activity using single and multi-turnover excitations. J Photochem Photobiol B: Biol 107:45–54CrossRefGoogle Scholar
  366. Wong D, Govindjee (1979) Antagonistic effects of mono- and divalent cations on polarization of chlorophyll fluorescence in thylakoids and changes in excitation energy transfer. FEBS Lett 97:373–377. doi: 10.1016/0014-5793(79)80124-6 CrossRefGoogle Scholar
  367. Wong D, Govindjee (1981) Action spectra of cation effects on the fluorescence polarization and intensity in thylakoids at room temperature. Photochem Photobiol 33:103–108CrossRefGoogle Scholar
  368. Wraight CA, Crofts AR (1970) Energy-dependent quenching of chlorophyll a fluorescence in isolated chloroplasts. Eur J Biochem 17:319–327PubMedCrossRefGoogle Scholar
  369. Wraight CA, Crofts AR (1971) Delayed fluorescence and the high-energy state of chloroplasts. Eur J Biochem 19:386–397PubMedCrossRefGoogle Scholar
  370. Xu C, Auger J, Govindjee (1990) Chlorophyll a fluorescence measurements of isolated spinach thylakoids using single-laser-based flow cytometry. Cytometry 11:349–358PubMedCrossRefGoogle Scholar
  371. 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 74:251–257PubMedCrossRefGoogle Scholar
  372. Yamashita T, Butler WL (1968a) Photoreduction and photophosphorylation with tris washed chloroplasts. Plant Physiol 43:1978–1986PubMedCrossRefGoogle Scholar
  373. Yamashita T, Butler WL (1968b) Inhibition of chloroplasts by UV-irradiation and heat treatment. Plant Physiol 43:2037–2040PubMedCrossRefGoogle Scholar
  374. Yamashita T, Butler WL (1969) Photooxidation by photosystem II of Tris washed chloroplasts. Plant Physiol 44:1342–1346PubMedCrossRefGoogle Scholar
  375. Yan J, Kurisu G, Cramer WA (2006) Intraprotein transfer of the quinone analogue inhibitor 2,5-dibromo-3-methyl-6-isopropyl-pbenzoquinone in the cytochrome b6f complex. Proc Natl Acad Sci USA 103:69–74PubMedCrossRefGoogle Scholar
  376. Zankel KL (1973) Rapid fluorescence changes observed in chloroplasts: their relationship to the O2 evolving system. Biochim Biophys Acta 325:138–148PubMedCrossRefGoogle Scholar
  377. Zheng C, Davis ME, McCammon JA (1990) Electric field distribution inside the bacterial photosynthetic reaction center of Rhodopseudomonas viridis. Chem Phys Lett 173:246–252CrossRefGoogle Scholar
  378. 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 223:114–133PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Newport NewsUSA
  2. 2.Department of Plant Biology, Department of Biochemistry and Center of BiophysicsUniversity of IllinoisUrbanaUSA
  3. 3.School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia

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