Delayed fluorescence in photosynthesis

Abstract

Photosynthesis is a very efficient photochemical process. Nevertheless, plants emit some of the absorbed energy as light quanta. This luminescence is emitted, predominantly, by excited chlorophyll a molecules in the light-harvesting antenna, associated with Photosystem II (PS II) reaction centers. The emission that occurs before the utilization of the excitation energy in the primary photochemical reaction is called prompt fluorescence. Light emission can also be observed from repopulated excited chlorophylls as a result of recombination of the charge pairs. In this case, some time-dependent redox reactions occur before the excitation of the chlorophyll. This delays the light emission and provides the name for this phenomenon—delayed fluorescence (DF), or delayed light emission (DLE). The DF intensity is a decreasing polyphasic function of the time after illumination, which reflects the kinetics of electron transport reactions both on the (electron) donor and the (electron) acceptor sides of PS II. Two main experimental approaches are used for DF measurements: (a) recording of the DF decay in the dark after a single turnover flash or after continuous light excitation and (b) recording of the DF intensity during light adaptation of the photosynthesizing samples (induction curves), following a period of darkness. In this paper we review historical data on DF research and recent advances in the understanding of the relation between the delayed fluorescence and specific reactions in PS II. An experimental method for simultaneous recording of the induction transients of prompt and delayed chlorophyll fluorescence and decay curves of DF in the millisecond time domain is discussed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

Chl* :

Excited state of a chlorophyll molecule

DF:

Delayed (chlorophyll) fluorescence

ET:

Electron transport

Fo :

Fluorescence intensity when all the reaction centers are assumed to be open, at the “O” level

Fj :

Fluorescence intensity at ~3 ms

Fi :

Fluorescence intensity at ~30 ms

Fp :

Maximal measured fluorescence intensity, at the “P” level

IC:

Induction curve

L:

Delayed fluorescence intensity

P700 :

Primary (chlorophyll) electron donor of PS I

P680 :

Primary (chlorophyll) electron donor of PS II

Pheo:

Pheophytin on D1 protein of PS II

PF:

Prompt (chlorophyll) fluorescence

PQ:

Plastoquinone

PS:

Photosystem

QA :

Primary quinone (electron) acceptor of PS II

QB :

Secondary quinone (electron) acceptor of PS II

RC:

Reaction center

Z (also called Yz):

Secondary (electron) donor in PS II, Tyr-161 of the D1 protein of PS II

References

  1. Aartsma T, Matysik J (eds) (2008) Biophysical techniques in photosynthesis, vol II. Volume 26, Advances in photosynthesis and respiration (series ed, Govindjee). Springer, Dordrecht

    Google Scholar 

  2. Amesz J, Hoff AJ (eds) (1996) Biophysical techniques in photosynthesis. Volume 3, Advances in photosynthesis and respiration (series ed, Govindjee). Springer, Dordrecht

    Google Scholar 

  3. Amesz J, Van Gorkom HJ (1978) Delayed fluorescence in photosynthesis. Annu Rev Plant Physiol 29:47–66

    CAS  Article  Google Scholar 

  4. Arnold W, Thompson J (1956) Delayed light production by blue-green algae, red algae, and purple bacteria. J Gen Physiol 39:311–318

    PubMed  CAS  Article  Google Scholar 

  5. Arthur WE, Strehler BL (1957) Studies on the primary process in photosynthesis. I. Photosynthetic luminescence: Multiple reactants. Arch Biochem Biophys 70:507–526

    PubMed  CAS  Article  Google Scholar 

  6. Barber J, Kraan GPB (1970) Salt induced light emission from chloroplasts. Biochim Biophys Acta 197:49–95

    PubMed  CAS  Article  Google Scholar 

  7. Barber J, Neumann J (1974) An energy-conservation site between H2O and DBMIB: Evidence from msec delayed light and chlorophyll fluorescence studies in chloroplasts. FEBS Lett 40:186–189

    Article  Google Scholar 

  8. Berden-Zrimec M, Drinovec L, Molinari I, Zrimec A, Umani SF (2008) Delayed fluorescence as a measure of nutrient limitation in Dunaliella tertiolecta. J Photochem Photobiol B 92:13–18

    PubMed  CAS  Article  Google Scholar 

  9. Bilger W, Schreiber U (1990) Chlorophyll luminescence as an indicator of stress-induced damage to the photosynthetic apparatus. Effects of heat-stress in isolated chloroplasts. Photosynth Res 25:161–171

    CAS  Article  Google Scholar 

  10. Björn LO, Forsberg AS (1979) Imaging by delayed light emission (phytoluminography) as a method for detecting damage to the photosynthetic system. Physiol Plant 47:215–222

    Article  Google Scholar 

  11. Briantais J-M, Vernotte C, Picaud M, Krause GH (1980) Chlorophyll fluorescence as a probe for the determination of the photoinduced proton gradient in isolated chloroplasts. Biochim Biophys Acta 591:198–202

    PubMed  CAS  Article  Google Scholar 

  12. Buchta J, Grabolle M, Dau H (2007) Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements: method, rationale, and results on the activation energy of dioxygen formation. Biochim Biophys Acta 1767:565–574

    PubMed  CAS  Article  Google Scholar 

  13. Buchta J, Shutova T, Samuelsson G, Dau H (2008) Time-resolved delayed chlorophyll fluorescence to study the influence of bicarbonate on a green algae mutant Photosystem II. Allen JF, Gantt E, Golbeck JH, Osmond B (eds) pp 35–38. Springer, Dordrecht

  14. Chernev P, Goltsev V, Zaharieva I, Strasser RJ (2006) A highly restricted model approach quantifying structural and functional parameters of Photosystem II probed by the chlorophyll a fluorescence rise. Ecol Eng Environ Protect 5:19–29

    Google Scholar 

  15. Christen G, Reifarth F, Renger G (1998) On the origin of the ‘35-ms kinetics’ of P680 .+ reduction in photosystem II with an intact water oxidising complex. FEBS Lett 429:49–52

    PubMed  CAS  Article  Google Scholar 

  16. Christen G, Steffen R, Renger G (2000) Delayed fluorescence emitted from light harvesting complex II and Photosystem II of higher plants in the 100 ns–5 мs time domain. FEBS Lett 475:103–106

    PubMed  CAS  Article  Google Scholar 

  17. Christov IK, Stefanov D, Goltzev VN, Abrasheva P (2001) Effects of grapevine fanleaf and stem pitting viruses on the photosynthetic activity of grapevine plants grown in vitro. Russ J Plant Physiol 48:473–477

    CAS  Article  Google Scholar 

  18. Clayton RK (1969) Characteristics of prompt and delayed fluorescence from spinach chloroplasts. Biophys J 9:60–76

    PubMed  CAS  Article  Google Scholar 

  19. Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23

    CAS  Article  Google Scholar 

  20. Dau H, Hansen U-P (1989) Studies on the adaptation of intact leaves to changing light intensities by a kinetic analysis of chlorophyll fluorescence and oxygen evolution as measured by the photoacoustic signal. Photosynth Res 20:59–83

    CAS  Article  Google Scholar 

  21. Dau H, Sauer K (1996) Exciton equilibration and photosystem II exciton dynamics—a fluorescence study on photosystem II membrane particles of spinach. Biochim Biophys Acta 1273:175–190

    Article  Google Scholar 

  22. Desai TS, Rane SS, Tatake VG, Sane PV (1983) Identification of far-red induced relative increase in the decay of delayed light emission from photosynthetic membranes with thermoluminescence peak V appearing at 321 K. Biochim Biophys Acta 724:485–489

    CAS  Article  Google Scholar 

  23. Ellenson JL, Amundson RG (1982) Delayed light imaging for the early detection of plant stress. Science 215:1104–1106

    PubMed  Article  CAS  Google Scholar 

  24. Evans EH, Crofts AT (1973) The relationship between delayed fluorescence and the H+ gradient in chloroplasts. Biochim Biophys Acta 292:130–139

    PubMed  CAS  Article  Google Scholar 

  25. Fleishman DE (1971) Luminescence in photosynthetic bacteria. Photochem Photobiol 14:277–286

    Article  Google Scholar 

  26. Gaevsky NA, Morgun VN (1993) Use of variable and delayed chlorophyll fluorescence for the study of plant photosynthesis (in Russian). Fiziol Rast 40:136–145

    Google Scholar 

  27. Gekhman A (1988) Study of the kinetic characteristics of plant photoluminescence (research methods, equipment and results) (in Russian). Krasnoiarsk IBF SO AN USSR

  28. Goltsev V, Yordanov I (1997) Mathematical model of prompt and delayed chlorophyll fluorescence induction kinetics. Photosynthetica 33:571–586

    CAS  Google Scholar 

  29. Goltsev V, Ortoidze TV, Sokolov ZN, Matorin DN, Venediktov PS (1980) Delayed luminescence yield kinetics in flash illuminated green plants. Plant Sci Lett 19:339–346

    Article  Google Scholar 

  30. Goltsev V, Yordanov I, Stojanova T, Popov O (1987) High temperature damage and acclimation of the photosynthetic apparatus. II. The effect of mono- and divalent cations and pH on the temperature sensitivity of some functional characteristics of chloroplasts isolated from heat-acclimated and non-acclimated bean plants. Planta 170:478–488

    CAS  Article  Google Scholar 

  31. Goltsev V, Traikov L, Hristov V (1998) Effects of exogenous electron acceptors on kinetic characteristics of prompt and delayed fluorescence in atrazine inhibited thylakoid membranes. In: Garab G (ed) Photosynthesis: mechanisms, effects. Kluwer Academic Publishers, The Netherlands, pp 3885–3888

    Google Scholar 

  32. 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 225:171–183

    PubMed  CAS  Article  Google Scholar 

  33. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2004) Kinetics of millisecond delayed chlorophyll fluorescence as a probe of photosystem II function. In: Zrimec M, Zrimec A, Drobne D, Milani M (eds) Weak photon emission from living tissues: delayed luminescence—facts & perspectives. Institute of Physical Biology, Grosuplje, Slovenia, pp 18–23

    Google Scholar 

  34. Goltsev V, Chernev P, Zaharieva I, Lambrev P, Strasser R (2005) Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. Photosynth Res 84:209–215

    PubMed  CAS  Article  Google Scholar 

  35. Govindjee, Papageorgiou G (1971) Chlorophyll fluorescence and photosynthesis: fluorescence transients. In: Giese AC (ed) Photophysiology. Academic Press, New York, pp 1–46

    Google Scholar 

  36. Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, Orlando

    Google Scholar 

  37. Grabolle M, Dau H (2005) Energetics of primary and secondary electron transfer in Photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim Biophys Acta 1708:209–218

    PubMed  CAS  Article  Google Scholar 

  38. Grigoryev Y, Morgun V, Gold V, Gaevsky N (1982) Study of light-induced changes of ms-delayed light emission in pea chloroplasts (in Russian). Biofizika 27:973–976

    Google Scholar 

  39. Guo Y, Tan J (2009) A kinetic model structure for delayed fluorescence from plants. Biosystems 95:98–103

    PubMed  CAS  Article  Google Scholar 

  40. Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:660–694

    Google Scholar 

  41. Hideg E, Kobayashi M, Inaba H (1990) Ultraweak photoemission from dark-adapted leaves and isolated chloroplasts. FEBS Lett 275:121–124

    PubMed  CAS  Article  Google Scholar 

  42. Hideg E, Kobayashi M, Inaba H (1991) The far red induced slow component of delayed light from chloroplasts is emitted from photosystem-II-evidence from emission-spectroscopy. Photosynth Res 29:107–112

    CAS  Article  Google Scholar 

  43. Hipkins MF, Barber J (1974) Estimation of the activation energy for millisecond delayed fluorescence from uncoupled chloroplasts. FEBS Lett 42:289–292

    PubMed  CAS  Article  Google Scholar 

  44. Ireland CR, Long SP, Baker NR (1984) The relationship between carbon dioxide fixation and chlorophyll a fluorescence during induction of photosynthesis in maize leaves at different temperatures and carbon dioxide concentration. Planta 160:550–558

    CAS  Article  Google Scholar 

  45. Itoh S (1980) Correlation between the time course of millisecond delayed fluorescence and that of prompt fluorescence at low temperature in uncoupled spinach chloroplasts. Plant Cell Physiol 21:873–884

    CAS  Google Scholar 

  46. Itoh S, Murata N (1973) Correlation between delayed light emission and fluorescence of chlorophyll a in system II particles derived from spinach chloroplasts. Photochem Photobiol 18:209–218

    CAS  Article  Google Scholar 

  47. Itoh S, Murata N, Takamiya A (1971) Studies on the delayed light emission in spinach chloroplasts. I. Nature of two phases in development of the millisecond delayed light emission during intermittent illumination. Biochim Biophys Acta 245:109–120

    CAS  Article  Google Scholar 

  48. Jeans C, Schilistra MJ, Klug DR (2002) The temperature dependence of P680 + reduction in oxygen-evolving Photosystem II. Biochemistry 41:5015–5023

    PubMed  CAS  Article  Google Scholar 

  49. Joliot P, Joliot A, Bouges B, Barbieri G (1971) Studies of System II photocenters by comparative measurements of luminescence, fluorescence, and oxygen emission. Photochem Photobiol 14:287–305

    CAS  Article  Google Scholar 

  50. Jursinic P (1986) Delayed fluorescence: current concepts and status. In: Govindjee, Amesz J, Fork DJ (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 291–328

    Google Scholar 

  51. Jursinic P, Govindjee (1977) Temperature dependence of delayed light emission in the 6 to 340 microsecond range after a single flash in chloroplasts. Photochem Photobiol 26:617–628

    CAS  Article  Google Scholar 

  52. Jursinic P, Govindjee (1982) Effects of hydroxylamine and silicomolybdate on the decay of delayed light emission in the 6–100 μs range after a single 10 ns flash in pea thylakoids. Photosynth Res 3:161–177

    CAS  Article  Google Scholar 

  53. Jursinic P, Govindjee, Wraight CA (1978) Membrane potential and microsecond to millisecond delayed light emission after a single excitation flash in isolated chloroplasts. Photochem Photobiol 27:61–71

    Article  Google Scholar 

  54. Kalauzi A, Markovic D, Radenovic C (2006) Transients of delayed fluorescence induction signal and photosynthetic antennas: A possible relationship. Mathematical modeling approach. Russ J Plant Physiol 53:289–297

    CAS  Article  Google Scholar 

  55. Katsumata M, Koike T, Nishikawa M, Kazumura K, Tsuchiya H (2006) Rapid ecotoxicological bioassay using delayed fluorescence in the green alga Pseudokirchneriella subcapitata. Water Res 40:3393–3400

    PubMed  CAS  Article  Google Scholar 

  56. Katsumata M, Takeuchi A, Kazumura K, Koike T (2008) New feature of delayed luminescence: preillumination-induced concavity and convexity in delayed luminescence decay curve in the green alga Pseudokirchneriella subcapitata. J Photochem Photobiol B 90:152–162

    PubMed  CAS  Article  Google Scholar 

  57. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    CAS  Article  Google Scholar 

  58. Lambrev P, Goltsev V (2001) pH dependence of the effects of diuron, atrazine and dinoseb on the luminescent properties of thylakoid membranes. Bulg J Plant Physiol 27:80–95

    Google Scholar 

  59. Lang M, Lichtenthaler HK (1991) Changes in the blue-green and red fluorescence emission spectra of beech leaves during the autumnal chlorophyll breakdown. J Plant Physiol 138:550–553

    CAS  Google Scholar 

  60. Lavorel J (1973) Kinetics of luminescence in the 10–6 to 10–4 s range in Chlorella. Biochim Biophys Acta 325:213–229

    PubMed  CAS  Article  Google Scholar 

  61. Lavorel J (1975) Luminescence. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 223–317

    Google Scholar 

  62. Lavorel J, Dennery T (1982) The slow component of Photosystem II luminescence. A process with distributed rate constant? Biochim Biophys Acta 680:281–289

    CAS  Article  Google Scholar 

  63. Lavorel J, Lavergne J, Etienne AL (1982) A reflection of several problems of luminescence in photosynthetic systems. Photobiochem Photobiophys 3:287–314

    CAS  Google Scholar 

  64. Lavorel J, Breton J, Lutz M (1986) Methodological principles of measurment of light emitted by photosynthetic systems. In: Govindjee, Amesz J, Fork DJ (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 57–98

    Google Scholar 

  65. Lazar D (1999) Chlorophyll a fuorescence induction. Biochim Biophys Acta 1412:1–28

    PubMed  CAS  Article  Google Scholar 

  66. Li Q, Xing D, Jia L, Wang J (2007) Mechanism study on the origin of delayed fluorescence by an analytic modeling of the electronic reflux for photosynthetic electron transport chain. J Photochem Photobiol B 87:183–190

    PubMed  CAS  Article  Google Scholar 

  67. Malkin S (1979) Delayed luminescence. In: Trebst A, Avron M (eds) Photosynthesis I. Photosynthetic electron transport and photophosphorilation. Acad.Press, NY, pp 473–491

    Google Scholar 

  68. Malkin S, Barber J (1978) Induction patterns of delayed luminescence from isolated chloroplasts. I. Response of delayed luminescence to changes in the prompt fluorescence yield. Biochim Biophys Acta 502:524–541

    PubMed  CAS  Article  Google Scholar 

  69. Malkin S, Bilger W, Schreiber U (1994) The relationship between luminescence and fluorescence in tobacco leaves during the induction period. Photosynth Res 39:57–66

    CAS  Article  Google Scholar 

  70. Mar T, Brebner J, Roy G (1975) Induction kinetics of delayed light emission in spinach chloroplasts. Biochim Biophys Acta 376:345–353

    PubMed  CAS  Article  Google Scholar 

  71. Markovic DZ, Kalauzi A, Radenovic CN (2001) Delayed fluorescence induction transients: mathematical modelling based on the chosen kinetic models. Gen Physiol Biophys 20:303–313

    PubMed  CAS  Google Scholar 

  72. Milanov G, Stefanov D, Goltsev V, Batchvarova R (1997) Changes in the submilli- and millisecond kinetics of dark relaxation of delayed fluorescence in tobacco leaves under conditions of bacterial infection by Pseudomonas syringae pv. Tabaci. Bulg J Plant Physiol 23:35–42

    Google Scholar 

  73. Miloslavina Y, Szczepaniak M, Muller M, Sander J, Nowaczyk M, Rцgner M, Holzwarth AR (2006) Charge separation kinetics in intact Photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45:2436–2442

    PubMed  CAS  Article  Google Scholar 

  74. Mimuro M, Akimoto S, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta 1767:327–334

    PubMed  CAS  Article  Google Scholar 

  75. Mladenova I, Maini C, Mallegni P, Goltsev V, Vladova R, Vinarova K, Rocheva S (1998) Siapton—an amino-acid-based biostimulant reducing osmostress metabolic changes in maize. Agro-Food-Industry Hi-Tech 9:18–22

    CAS  Google Scholar 

  76. Monti M, Zrimec A, Beran A, Berden-Zrimec M, Drinovec L, Kosi G, Tamberlich F (2005) Delayed luminescence of Prorocentrum minimum under controlled conditions. Harmful Algae 4:643–650

    Article  Google Scholar 

  77. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht

  78. Pavlova E, Matorin D, Venedictov P (1978) Investigation of delayed fluorescence in leaves of woody plants grown under different illumination conditions. Soviet Plant Physiol 25:71–78

    Google Scholar 

  79. Plekhanov SE, Chemeris IK (2003) Early toxic effect of zinc, cobalt, and cadmium on photosynthetic activity of green alga Chlorella pyrenoidosa Chick S-39. Izvestiia Akademii nauk Ser Biol/RAN 5:610–616

    Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  81. Radenovic C, Markovic D, Jeremic M (1994) Delayed chlorophyll fluorescence in plant models. Photosynthetica 30:1–24

    CAS  Google Scholar 

  82. Robinson HH, Crofts AR (1983) Kinetics of the oxidation-reduction reactions of the photosystem II quinone acceptor complex, and the pathway for deactivation. FEBS Lett 153:221–226

    CAS  Article  Google Scholar 

  83. Rottenberg H (1977) Proton and ion transport across the thylakoid membranes. In: Trebst A, Avron M (eds) Photosynthesis I. Electron transport and photophosphorilation. Springer-Verlag, Berlin, pp 338–349

    Google Scholar 

  84. Ruby RH (1976) Delayed fluorescence from Chlorella: II. Effects of electron transport inhibitors DCMU and NH2OH. Photochem Photobiol 26:293–298

    Article  Google Scholar 

  85. Rutherford AW, Inoue Y (1984) Oscillation of delayed luminescence from PS II: recombination of S2QB and S3QB . FEBS Lett 165:163–170

    CAS  Article  Google Scholar 

  86. Rutherford AW, Govindjee, Inoue Y (1984) Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc Natl Acad Sci USA 81:1107–1111

    PubMed  CAS  Article  Google Scholar 

  87. Satoh K, Katoh S (1983) Induction kinetics of millisecond-delayed luminescence in intact Bryopsis chloroplasts. Plant Cell Physiol 24:953–962

    Google Scholar 

  88. 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 30:785–796

    CAS  Article  Google Scholar 

  89. Schansker G, Toth SZ, Strasser RJ (2006) Dark recovery of the Chl a fluorescence transient (OJIP) after light adaptation: the qT-component of non-photochemical quenching is related to an activated photosystem I acceptor side. Biochim Biophys Acta 1757:787–797

    PubMed  CAS  Article  Google Scholar 

  90. Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in Photosystem II. Biophys J 54:397–405

    PubMed  CAS  Article  Google Scholar 

  91. Schmidt W, Senger H (1987) Long-term delayed luminescence in Scenedesmus obliquus I. Spectral and kinetic properties. Biochim Biophys Acta 890:15–22

    CAS  Article  Google Scholar 

  92. Schreiber U, Schliwa U (1987) A solid-state, portable instrument for measurment of chlorophyll luminescence induction in plants. Photosynth Res 11:173–182

    Article  Google Scholar 

  93. Schreiber U, Bilger W, Hormann H, Neubauer C (2000) Chlorophyll fluorescence as a diagnostic tool: basics and some aspects of practical relevance. In: Raghavendra AS (ed) Photosynthesis: a comprehensive treatise. Cambridge University Press, Cambridge, pp 320–336

    Google Scholar 

  94. Shuvalov VA, Klimov VV (1976) The primary photoreactions in the complex cytochrome-P-890 P-760 (bacteriopheophytin 760) of Chromatium minutissimum at low redox potentials. Biochim Biophys Acta 440:587–599

    PubMed  CAS  Article  Google Scholar 

  95. Shuvalov VA, Litvin FF (1969) Mechanism of delayed light emission of plans leaves and energy storage in photosynthetic centers. Mol Biol (Moscow) 3:45–56

    Google Scholar 

  96. Sonneveld A, Rademaker H, Duysens LNM (1980a) Microsecond delayed fluorescence of photosystem II of photosynthesis in various algae: emission spectra and uphill energy transfer. FEBS Lett 113:323–327

    CAS  Article  Google Scholar 

  97. Sonneveld A, Duysens LNM, Moerdijk A (1980b) Magnetic field-induced increase in chlorophyll a delayed fluorescence of photosystem II: a 100- to 200-ns component between 4.2 and 300 K. Proc Natl Acad Sci USA 77:5889–5893

    PubMed  CAS  Article  Google Scholar 

  98. 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 37:392

    Article  Google Scholar 

  99. Stacy WT, Mar T, Swenberg CE, Govindjee (1971) An analysis of a triplet exciton model for the delayed light in Chlorella. Photochem Photobiol 14:197–219

    CAS  Article  Google Scholar 

  100. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    CAS  Article  Google Scholar 

  101. Strehler BL, Arnold W (1951) Light production by green plants. J Gen Physiol 34:809–820

    PubMed  CAS  Article  Google Scholar 

  102. Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of stress impact on plants’ vitality: applications in detecting and evaluating the beneficial role 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. Springer, Dordrecht, pp 679–703

    Google Scholar 

  103. Tyystjarvi 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 G, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 363–388

    Google Scholar 

  104. Valikhanov KM, Zakhidov EA, Zakhidova MA, Kasymdzhanov MA, Kurbanov SS, Nematov SK, Khabibullaev PK (2002) Kinetics of photoinhibition and delayed fluorescence in the plant photosynthetic system. Doklady Biochem Biophys 387:331–334

    CAS  Article  Google Scholar 

  105. Van Best JA, Duysens LNM (1977) A one microsecond component of chlorophyll luminescence suggesting a primary acceptor of system II of photosynthesis different from Q. Biochim Biophys Acta 459:187–206

    PubMed  Article  Google Scholar 

  106. Van Gorkom HJ, Donze M (1973) Charge accumulation in the reaction center of photosystem 2. Photochem Photobiol 17:333–342

    Article  Google Scholar 

  107. Velthuys BR, Amesz J (1975) Temperature and preillumination dependence of delayed fluorescence of spinach chloroplasts. Biochim Biophys Acta 376:162–168

    PubMed  CAS  Article  Google Scholar 

  108. Venediktov PS, Goltsev VN, Shinkarev VP (1980) The influence of electric diffusion potential on delayed fluorescence light curves of chloroplasts treated with DCMU. Biochim Biophys Acta 593:125–132

    PubMed  CAS  Article  Google Scholar 

  109. Veselovskii V, Veselova T (1990) Plant luminescence: theoretical and practical aspects (in Russian). Nauka, Moscow

    Google Scholar 

  110. Wong D, Govindjee, Jursinic P (1978) Analysis of microsecond fluorescence yield and delayed light emission changes after a single flash in pea chloroplasts: effects of mono-and divalent cations. Photochem Photobiol 28:963–974

    CAS  Article  Google Scholar 

  111. Wraight CA, Crofts AT (1971) Delayed fluorescence and the high-energy state of chloroplasts. Eur J Biochem 19:386–397

    PubMed  CAS  Article  Google Scholar 

  112. Yacobi YZ, Gerhardt V, Gonen-Zurgil Y, Sukenik A (1998) Delayed fluorescence excitation spectroscopy: a rapid method for qualitative and quantitative assessment of natural population of phytoplankton. Water Res 32:2577–2582

    CAS  Article  Google Scholar 

  113. Yordanov I, Goltsev V, Stojanova T, Venediktov P (1987) High temperature damage and acclimation of the photosynthetic apparatus. I. Temperature sensitivity of some photosynthetic parameters of chloroplasts isolated from acclimated and non-acclimated bean leaves. Planta 170:471–477

    Article  Google Scholar 

  114. Yordanov I, Goltsev V, Stefanov D, Chernev P, Zaharieva I, Kirova M, Gecheva V, Strasser RJ (2008) Preservation of PS II electron transport from senescence-induced inactivation in primary leaves after decapitation and defoliation of bean plants. J Plant Physiol 165:1954–1963

    PubMed  CAS  Article  Google Scholar 

  115. Zaharieva I, Goltsev V (2003) Advances on Photosystem II investigation by measurement of delayed chlorophyll fluorescence by a phosphoroscopic method. Photochem Photobiol 77:292–298

    PubMed  CAS  Article  Google Scholar 

  116. Zaharieva I, Velitchkova M, Goltsev V (1998) Effect of cholesterol and benzyl alcohol on prompt and delayed chlorophyll fluorescence in thylakoid membranes. Kluwer Academic Publishers, Netherlands, pp 1827–1830

    Google Scholar 

  117. Zaharieva I, St Taneva, Goltsev V (2001) Effect of temperature on the luminescent characteristics in leaves of arabidopsis mutants with decreased unsaturation of the membrane lipids. Bulg J Plant Physiol 27:3–18

    CAS  Google Scholar 

  118. Zankel KL (1971) Rapid delayed luminescence from chloroplasts: kinetic analysis of components; the relationship to the O2 evolving system. Biochim Biophys Acta 245:373–385

    PubMed  CAS  Article  Google Scholar 

  119. Zhang L, Xing D (2008) Rapid determination of the damage to photosynthesis caused by salt and osmotic stresses using delayed fluorescence of chloroplasts. Photochem Photobiol Sci 7:352–360

    PubMed  CAS  Article  Google Scholar 

  120. Zhang L-R, Xing D, Wang J-S, Zeng L-Z, Li Q (2007a) Light-induced delayed fluorescence as an indicator for UV-B radiation environment stress on plants. J Optoelectron Laser 18:878–881

    CAS  Google Scholar 

  121. Zhang L, Xing D, Wang J, Li L (2007b) Rapid and non-invasive detection of plants senescence using a delayed fluorescence technique. Photochem Photobiol Sci 6:635–641

    PubMed  CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank the Bulgarian National Science Fund, Project No. DO 02-137/15.12.2008 for the financial support. R.J.S acknowledges support by the Swiss National Science Foundation, Project Nr: 200021-116765. We thank Detelin Stefanov for critical reading of the manuscript. The paper was written while I.Z. was working at the Free University in Berlin on an Alexander von Humboldt fellowship. This review was edited by Govindjee. We thank him for many suggestions that have improved this review.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vasilij Goltsev.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Goltsev, V., Zaharieva, I., Chernev, P. et al. Delayed fluorescence in photosynthesis. Photosynth Res 101, 217–232 (2009). https://doi.org/10.1007/s11120-009-9451-1

Download citation

Keywords

  • Delayed (chlorophyll) fluorescence
  • Chlorophyll fluorescence
  • Photosystem II (PS II)
  • Reaction center
  • Charge recombination
  • Electron transport