Abstract
The light-induced/dark-reversible changes in the chlorophyll (Chl) a fluorescence of photosynthetic cells and membranes in the μs-to-several min time window (fluorescence induction, FI; or Kautsky transient) reflect quantum yield changes (quenching/de-quenching) as well as changes in the number of Chls a in photosystem II (PS II; state transitions). Both relate to excitation trapping in PS II and the ensuing photosynthetic electron transport (PSET), and to secondary PSET effects, such as ion translocation across thylakoid membranes and filling or depletion of post-PS II and post-PS I pools of metabolites. In addition, high actinic light doses may depress Chl a fluorescence irreversibly (photoinhibitory lowering; q(I)). FI has been studied quite extensively in plants an algae (less so in cyanobacteria) as it affords a low resolution panoramic view of the photosynthesis process. Total FI comprises two transients, a fast initial (OPS; for Origin, Peak, Steady state) and a second slower transient (SMT; for Steady state, Maximum, Terminal state), whose details are characteristically different in eukaryotic (plants and algae) and prokaryotic (cyanobacteria) oxygenic photosynthetic organisms. In the former, maximal fluorescence output occurs at peak P, with peak M lying much lower or being absent, in which case the PSMT phases are replaced by a monotonous PT fluorescence decay. In contrast, in phycobilisome (PBS)-containing cyanobacteria maximal fluorescence occurs at M which lies much higher than peak P. It will be argued that this difference is caused by a fluorescence lowering trend (state 1 → 2 transition) that dominates the FI pattern of plants and algae, and correspondingly by a fluorescence increasing trend (state 2 → 1 transition) that dominates the FI of PBS-containing cyanobacteria. Characteristically, however, the FI pattern of the PBS-minus cyanobacterium Acaryochloris marina resembles the FI patterns of algae and plants and not of the PBS-containing cyanobacteria.
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Abbreviations
- APC:
-
Allophycocyanin
- Ax:
-
Antheraxanthin
- Chl:
-
Chlorophyll
- CPC:
-
C-phycocyanin
- DCMU:
-
3-(3,4-Dichlorophenyl)-1,4-dimethyl urea
- FI:
-
Fluorescence induction
- LHC:
-
Light harvesting complex
- PBP:
-
Phycobiliprotein
- PBS:
-
Phycobilisome
- Pheo:
-
Pheophytin a
- PQ:
-
Plastoquinone pool
- PS I, PS II:
-
Photosystem I, Photosystem II
- PSET:
-
Photosynthetic electron transport
- q(E):
-
Quenching due to membrane energization processes
- q(N)/de-q(N):
-
Nonphotochemical quenching/de-quenching processes
- q(P)/de-q(P):
-
Photochemical quenching/de-quenching processes
- q(T1 → 2)/q(T2 → 1):
-
Fluorescence lowering/increase due to state 1 → 2 and state 2 → 1 transitions
- q(I):
-
Fluorescence lowering due to photoinhibitory processes
- q(ΔpH):
-
Fluorescence quenching due to transmembrane ΔpH
- RC I, RC II:
-
Reaction centers of PS I, PS II
- RSET:
-
Respiratory electron transport
- Zx:
-
Zeaxanthin
References
Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326
Allen JF, Mullineaux CW (2004) Probing the mechanism of state transitions in oxygenic photosynthesis by chlorophyll fluorescence spectroscopy. Kinetics and imaging. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 447–461
Arnon DI, Tsujimoto HY, McSwain BD (1965) Quenching of chloroplast fluorescence by photosynthetic phosphorylation and electron transfer. Proc Natl Acad Sci USA 54:927–934
Bannister TT, Rice G (1968) Parallel time courses of oxygen evolution and chlorophyll fluorescence. Biochim Biophys Acta 162:555–580
Barber J (1976) Ionic regulation in intact chloroplasts and its effect on primary photosynthetic processes. In: Barber J (ed) The intact chloroplast, topics in photosynthesis vol 1. Elsevier, Amsterdam, pp 89–134
Barber J (1982) Influence of surface charges on thylakoid structure and function. Ann Rev Plant Physiol 33:261–295
Barber J (2004) Engine of life and big bang of evolution: a personal perspective. Photosynth Res 80:137–144
Barber J, Telfer A, Nicolson J (1974) Evidence for divalent cation movement within isolated whole chloroplasts from studies with ionophore A23187. Biochim Biophys Acta 357:161–165
Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352–4356
Boichenko VA, Klimov VV, Miyashita H, Miyachi S (2000) Functional characteristics of chlorophyll d-predominating photosynthetic apparatus in intact cells of Acaryochloris marina. Photosynth Res 65:269–277
Bradbury M, Baker NE (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of Photosystem II electron acceptors and fluorescence emission from Photosystems I and II. Biochim Biophys Acta 635:542–551
Bradbury M, Baker NR (1984) A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves. Biochim Biophys Acta 765:275–281
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 548:128–138
Briantais JM, Vernotte C, Krause GH, Weis E (1986) Chlorophyll a flurescence of higher plants: chloroplasts and leaves. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, New York, pp 539–583
Bruce D, Vasil’ev S (2004) Excess light stress: multiple dissipative processes of excess excitation. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 497–523
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 36:749–755
Bukhov NG, Carpentier R (2004) Effects of water stress on the photosynthetic efficiency of plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 623–635
Butler WL (1972) On the primary nature of fluorescence yield changes associated with photosynthesis. Proc Natl Acad Sci USA 69:3420–3442
Butler WL, Strasser RJ (1977) Tripartite model for the photochemical apparatus of green plant photosynthesis. Proc Natl Acad Sci USA 74:3382–3385
Byrdin M, Rimke I, Schlodder R, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in Photosystem I from Synechococcus elongatus with P700 reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–1007
Campbell D, Öquist G (1996) Predicting light acclimation in cyanobacteria from nonphotochemical quenching of Photosystem II fluorescence, which reflects state transitions in these organisms. Plant Physiol 111:1293–1298
Cao J, Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochim Biophys Acta 1015:180–188
Crofts AR, Yerkes CT (1994) A molecular mechanism for qE-quenching. FEBS Lett 352:265–270
Dau H (1994) Molecular mechanisms and quantitative models of variable Photosystem II fluorescence. Photochem Photobiol 60:1–23
Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39
Delosme R (1967) Étude de l’induction de fluorescence des algues vertes et des chloroplastes au debut d’une illumination intense. Biochim Biophys Acta 143:108–128
Den Haan GA, Duysens LNM, Egberts DJN (1974) Fluorescence yield kinetics in the microsecond-range in Chlorella pyrenoidosa and spinach chloroplasts in the presence of hydroxylamine. Biochim Biophys Acta 368:409–421
Deprez J, Dobek A, Geacintov NE, Paillotin G, Breton J (1983) Probing fluorescence induction in chloroplasts on a nanosecond time scale utilizing picosecond laser pulse pairs. Biochim Biophys Acta 725:444–454
Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (eds) Studies on microalgae and photosynthetic bacteria. University of Tokyo Press, pp 353–371
Falkowski PG, Kolber Z, Mauzerall D (1994) A comment on the call to throw away your fluorescence induction apparatus. Biophys J 66:923–928
Falkowski PG, Koblizek M, Gorbunov M, Kolber Z (2004) Development and application of variable chlorophyll fluorescence techniques in marine ecosystems. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 757–778
Finazzi G, Johnson GN, Dall’Osto L, Joliot P, Wollman F-A, Bassi R (2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc Natl Acad Sci USA 101:12375–12380
Forbush B, Kok B (1968) Reaction between primary and secondary electron acceptors of Photosystem II of photosynthesis. Biochim Biophys Acta 162:243–253
Fork DC, Satoh Ka (1983) State I-State II transitions in the thermophilic blue-green alga (cyanobacterium) Synechococcus lividus. Photochem Photobiol 37:421–427
Franck F, Juneau P, Popovic R (2002) Resolution of Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 162:239–246
Franck UF, Hoffmann N, Arenz H, Schreiber U (1969) Chlorophylfluoreszenz als Indikator der photochemischen Primärprozesse der Photosynthese. Berichte Bunsengesel Physik Chemie 73:871–879
Fromme P, Jordan P, Krauss N (2001) Structure of Photosystem I. Biochim Biophys Acta 1507:5–31
Fujita Y, Murakami A, Aizawa K, Ohki K (1994) Short-term and long-term adaptation of the photosynthetic aparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The molecular biology of cyanobacteria, Advances in photosynthesis vol 1. Kluwer AcademicPublishers, Dordrecht, The Netherlands, pp 677–692
Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99:197–207
Gilmore AM, Itoh SS, Govindjee (2000) Global spectral-kinetic analysis of room temperature chlorophyll a fluorescence from light-harvesting antenna mutants of barley. Phil Trans R Soc London 355:1369–1382
Gitelson AA, Buschmann C, Lichtenthaler HK (1999) The chlorophyll fluorescence ratio F735/F700 as an accurate measure of the chlorophyll content in plants. Remote Sens Environ 69:296–302
Golan T, Li XP, Müller-Moulé P, Niyogi KK (2004) Using mutants to understand light stress acclimation in plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 525–554
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160
Govindjee (2004) Chlorophyll fluorescence. A bit of basics and history. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 1–42
Govindjee, Papageorgiou G (1971) Chlorophyll fluorescence and photosynthesis: fluorescence transients. In: Giese AC (ed) Photophysiology vol 6. Academic Press, New York, pp 1–46
Govindjee , Satoh Ka (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, New York, pp 497–537
Govindjee, Seufferfeld MJ (2002) Non-photochemical quenching of chlorophyll a fluorescence: early history and characterization of two xanthophyll cycle mutants of Chlamydomonas reinhardtii. Funct Plant Biol 29:1141–1155
Govindjee, Spilotro P (2002) An Arabidopsis thaliana mutant, altered in the γ-subunit of ATP synthase, has a different pattern of intensity-dependent changes in nonphotochemical quenching and kinetics of the P-to-S fluorescence decay. Funct Plant Biol 29:425–434
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 1706:239–249
Haworth P, Karukstis KK, Sauer K (1983) Picosecond fluorescence kinetics in spinach chloroplasts at room temperature effects of phosphorylation. Biochim Biophys Acta 725:261–271
Hirano M, Satoh K, Katoh S (1980) Plastoquinone as a common link between photosynthesis and respiration in a blue green alga. Photosyn Res 1:149–162
Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–435
Holub O, Seufferheld MJ, Gohlke C, Govindjee, Heiss GJ, Clegg, RM (2007) Fluorescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient. J Microscopy 1–31
Holzwarth AR (1993) Is it time to throw away your apparatus for chlorophyll fluorescence induction? Biophys J 64:1280–1281
Holzwarth AR, Wendler J, Haehnel W (1985) Time-resolved picosecond fluorescence spectra of the antenna chlorophylls in Chlorella vulgaris. Resolution of Photosystem I fluorescence. Biochim Biophys Acta 807:155–167
Holzwarth AR, Müller M, Reus M, Nowaczyk M, Sander J, Rögner M (2006) Kinetics and mechanism of electron transfer in intact Photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103:6895–6900
Hoober JK, Argyroudi-Akoyunoglou JH (2004) Assembly of light-harvesting complexes of Photosystem II and the role of chlorophyll b. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 679–712
Horton P (1983a) Relations between electron transport and carbon dioxide assimilation; simultaneous measurement of chlorophyll fluorescence, transthylakoid pH gradient and O2 evolution in isolated chloroplasts. Proc R Soc London B 217:405–416
Horton P (1983b) Effects of changes in the capacity for photosynthetic electron transfer and photophosphorylation on the kinetics of fluorescence induction in isolated chloroplasts. Biochim Biophys Acta 724:404–410
Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Reduction of non-photochemical quenching. Biochim Biophys Acta 932:107–115
Hsu BD (1992) A theoretical study on the fluorescence induction curve of spinach thylakoids in the absence of DCMU. Biochim Biophys Acta 1140:30–36
Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M, Itoh S (1998) A Photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Nat Acad Sci USA 95:13319–13323
Hu Q, Marquardt J, Iwasaki I, Miyashita H, Kurano N, Moerschel E, Miyachi S (1999) Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochim Biophys Acta 1412:250–261
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 concentrations. Planta 100:550–558
Joliot P (1965a) Cinétiques des réactions liées a l’émission d’oxygène photosynthétique. Biochim Biophys Acta 102:116–134
Joliot P (1965b) Études simultanées des cinétiques de fluorescence et d’ l’émission d’oxygène photosynthétique. Biochim Biophys Acta 102:135–148
Joliot P, Joliot A (1964) Études cinétique de la réaction photochimique liberant l’oxygène au cours de la photosynthése. CR Acad Sci Paris 258:4622–4625
Joliot P, Joliot A (2003) Excitation transfer between photosynthetic units; the 1964 experiment. Photosynth Res 76:241–245
Joshi MK, Mohanty P (1995) Probing photosynthetic performance by chlorophyll a fluorescence: analysis and interpretation of fluorescence parameters. J Sci Ind Res 54:155–174
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, The Netherlands, pp 637–661
Karukstis KK, Sauer K(1983) Fluorescence decay kinetics of chlorophyll in photosynthetic membranes. J Cellular Biochem 23:131–158
Kautsky H, Hirsch A (1931) Neue versuche zur kohlensäureassimilation. Naturwissensch 48:964
Kautsky H, Appel W, Amann H (1960) Chlorophyllfluoreszenz und kohlensäureassimilation. III. Die Fluoreszenzkurve und die photochemie der pflanze. Biochem Z 332:227–292
Klimov VV, Klevanik AA, Shuvalov VA, Krasnovsky AA (1977) Reduction of pheorphytin in the primary light reaction of photosystem II. FEBS Lett 82:183–196
Klimov VV, Shuvalov VA, Heber U (1985) Photoreduction of pheophytin as a result of electron donation from the water-splitting system to Photosystem-ll reaction centers. Biochim Biophys Acta 809:345–350
Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60:151–163
Kramer DM, Avenson TJ, Kanazawa A, Cruz JA, Ivanov B, Edwards GR (2004) In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 251–278
Krause GH (1974) Changes in chlorophyll fluorescence in relation to light-dependent cation transfer across thylakoid membranes. Biochim Biophys Acta 333:301–313
Krause GH, Jahns P (2004) Nonphotochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 463–495
Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynth Res 5:139–157
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42:313–349
Krause GH, Vernotte C, Briantais J-M (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae, resolution into two components. Biochim Biophys Acta 679:116–124
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 68:2474–2492
Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28
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 Theo Biol 220:469–503
Lazar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30
Lichtenthaler HK (1992) The Kautsky effect: 60 years of chlorophyll fluorescence induction kinetics. Photosynthetica 27:45–55
Lichtenthaler HK, Babani F (2004) Light adaptation and scenescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 713–736
McAlister ED, Myers J (1940) The time course of photosynthesis and fluorescence observed simultaneously. Smithsonian Miscellaneous Collections 99:1–37
Malkin S (1966) Fluorescence induction studies in isolated chloroplasts II. Kinetic analysis of the fluorescence intensity dependence on time. Biochim Biophys Acta 126:433–442
Malkin S (1971) Fluorescence induction studies in isolated chloroplasts III. On the electron-transfer equilibria in the pool of electron acceptors of Photosystem II. Biochim Biophys Acta 234:415–427
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 126:413–432
Malkin S, Wong D, Govindjee, Merkelo H (1980) Parallel measurements on fluorescence lifetime and intensity from leaves during fluorescence induction. Photobiochem Photobiophys 1:83–89
Marquardt J, Senger H, Miyashita H, Miyachi S, Moerchel E (1997) Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 410:428–432
Mauzerall D (1972) Light-induced fluorescence changes in Chlorella, and the primary photoreactions for the production of O2. Proc Nat Acad Sci USA 69:1358–1362
Melis A, Homann PH (1976) Kinetic analysis of the fluorescence in 3-(3,4-dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts. Photochem Photobiol 21:431–437
Mimuro M, Akimoto S,Yamazaki I, Miyashita H, Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412:37–46
Mimuro M, Akimoto S, Gotoh T, Yokono M, Akiyamad M, Tsuchiyaa, Miyashita H, Kobayashi M, Yamazakic I (2004) Identification of the primary electron donor in PS II of the Chl d-dominated cyanobacterium Acaryochloris marina. FEBS Lett 536:95–98
Mohanty P, Govindjee (1973) Light-induced changes in the fluorescence yield of Chl 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 14:611–629
Mohanty P, Govindjee (1974) The slow decline and subsequent rise of chlorophyll fluorescence transients in intact algal cells. Plant Biochem J 1:78–106
Mohanty P, Papageorgiou GC, Govindjee (1971) Fluorescence induction in the red alga Porphyridium cruentum. Photochem Photobiol 14:667–682
Moise N, Moya I (2004a) Correlation between lifetime heterogeneity and kinetics heterogeneity during chlorophyll fluorescence induction in leaves: 1. Mono-frequency phase and modulation analysis reveals a conformational change of a PSII pigment complex during the IP thermal phase. Biochim Biophys Acta 1657:33–46
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
Morin P (1964) Études des cinetiques de fluorescence de la chlorophylle in vivo dans les premières instants qui suivent le debut de illumination. J Chim Phys 61:674–680
Munday JCM Jr, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21
Murata N (1970) Control of excitation transfer in photosynthesis. IV.- Kinetics of chlorophyll a fluorescence in Porphyra yezoensis. Biochim Biophys Acta 205:379–389
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion . Plant Cell 10:1121–1134
Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382
Paillotin G (1976) Movement of excitations in the photosynthetic domains of Photosystem II. J Theor Biol 58:337–352
Paillotin G, Geacintov NE, Breton J (1983) A master equation theory of fluorescence induction, photochemical yield, and singlet-triplet exciton quenching in photosynthetic systems. Biophys J 44:65–77
Papageorgiou GC (1975) Chlorophyll fluorescence: an intrinsic probe of photosynthesis. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 319–372
Papageorgiou GC, Alygizaki-Zorba A (1997) A sensitive method for the estimation of the cytoplasmic osmolality of cyanobacterial cells using chlorophyll a fluorescence. Biochim Biophys Acta 1335:1–4
Papageorgiou GC, Govindjee (1968a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo I. Anacystis nidulans. Biophys J 8:1299–1315
Papageorgiou GC, Govindjee (1968b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II. Chlorella pyrenoidosa. Biophys J 8:1316–1328
Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Dordrecht, The Netherlands
Papageorgiou GC, Stamatakis K (2004) Water and solute transport in cyanobacteria as probed by chlorophyll fluorescence. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 663–678
Papageorgiou GC, Alygizaki-Zorba A, Ladas N, Murata N (1998) A method to probe the cytoplasmic osmolality and water and solute fluxes across the cell membrane of cyanobacteria with chlorophyll a fluorescence: experiments with Synechococcus sp. PCC 7942 Physiol Plant 103:215–224
Peterson R, Sivak M, Walker DA (1988) Carbon dioxide-induced oscillations in fluorescence and photosynthesis. Role of thylakoid membrane energization in regulation of Photosystem II activity. Plant Physiol 88:1125–1130
Peterson RB, Oja V, Laisk A (2001) Chlorophyll fluorescence at 680 and 730 nm and leaf photosynthesis. Photosynth Res 56:185–195
Pfündel E (1998) Estimating the contribution of Photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195
Quick WP, Horton P (1984a) Studies on the induction of chlorophyll fluorescence in barley protoplasts. I. Factors affecting the observation of oscillations in the yield of chlorophyll fluorescence and the rate of oxygen evolution. Proc R Soc London B 220:361–370
Quick WP, Horton P (1984b) Studies on the induction of chlorophyll fluorescence in barley protoplasts. II. Resolution of fluorescence quenching by redox state and the transthylakoid pH gradient. Proc R Soc London B 220:361–370
Rajagopal S, Egorova EA, Bukhov NG, Carpentier R (2003) Quenching of excited states of chlorophyll molecules in submembrane fractions of Photosystem I by exogenous quinones. Biochim Biophys Acta 1606:147–152
Rabinowitch E (1956) Photosynthesis and related processes vol. II, Part 2. Interscience Publishers Inc., New York
Reifarth F, Renger G (1998) Indirect evidence for structural changes coupled with QB-. formation in Photosystem II FEBS Lett 428:123–126
Samson G, Prasil O, Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 37:163–182
Schansker G, Toth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of Photosystem I in the chlorophyll a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261
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
Scheller HV, Jensen PE, Haldrup A, Lunde C, Knoetzel J (2001) Role of subunits in eukaryotic Photosystem I. Biochim Biophys Acta 1507:41–60
Schelvis JPM, van Noort PI, Aartsma HJ, van Gorkom HJ (1994) Energy transfer, charge separation and pigment arrangement in the reaction center of Photosystem II. Biochim Biophys Acta 1184:242–250
Scherer S (1990) Do photosynthetic and respiratory electron transport chains share redox components? Trends Biochem Sci 15:458–462
Schiller H, Senger H, Miyashita H, Miyachi S, Dau H (1997) Light-harvesting in Acaryochloris marina - spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system. FEBS Lett 410:433–436
Schlodder E, Cetin M, Byrdin M, Terekhova IV, Karapetyan NV (2005) P700+- and 3P700-induced quenching of fluorescence at 760 nm in trimeric Photosystem I complexes from the cyanobacteriun Arthrospira platensis. Biochim Biophys Acta 1706:53–67
Schoedel R, Irrgang K-D, Voigt J, Gernot Renger G (1998) Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys J 75:3143–3153
Schreiber U (2004) Pulse-amplitude-modulation (PAM) and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 279–319
Schreiber U, Vidaver W (1974) Chlorophyll fluorescence induction in anaerobic Scenedesmus obliquus. Biochim Biophys Acta, 368:97–112
Schreiber U, Vidaver W (1976) The I-D fluorescence transient an indicator of rapid energy distribution changes in photosynthesis. Biochim Biophys Acta 440:205–214
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62
Shinkarev V (2004) Photosystem II: oxygen evolution and chlorophyll a fluorescence induced by multiple flashes. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 197–229
Shinkarev V, 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 90:7466–7469
Sivak MN, Walker DA (1987) Oscillations and other symptoms of limitation of in vivo photosynthesis by inadequate phosphate supply to the chloroplast. Plant Physiol Biochem 25:635–648
Sivak MN, Prinsley RT, Walker DA (1983) Some effects of changes in gas phase on the steady state chlorophyll a fluorescence exhibited by illuminated leaves. Proc R Soc Lond B 217:393–404
Sivak MN, Heber U, Walker DA (1985a) Chlorophyll a fluorescence and light-scattering kinetics displayed by leaves during induction of photosynthesis. Planta 163:419–423
Sivak MN, Dietz K.-J, Heber U, Walker DA (1985b) The relationship between light-scattering and chlorophyll a fluorescence during oscillations in photosynthetic carbon assimilation. Arch Biochem Biophys 237:513–519
Sonneveld A, Rademaker H, Duysens LNM (1979) Chlorophyll fluorescence as a monitor of nanosecond reduction of the photo-oxidation of the primary donor P-680+ of Photostem II. Biochim Biophys Acta 548:536–551
Srivastava A, Strasser RJ, Govindjee (1995) Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutant of Chlamydomonas reinhardtii. Photosynth Res 43:131–141
Stamatakis K, Papageorgiou GC (2001) The osmolality of the cell suspension regulates phycobilisome-to-Photosystem I excitation transfers in cyanobacteria. Biochim Biophys Acta 1506:172–181
Stamatakis K, Tsimilli-Michael M, Papageorgiou GC (2007) Fluorescence induction in the phycobilisome-containing cyanobacterium Synechococcus sp PCC 7942 Analysis of the slow fluorescence transient. Biochim Biophys Acta 1767:766–772
Steffen R, Eckert HJ, 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
Strasser RJ, Stirbet AD (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 Simulat 56:451–461
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescent transient in plants and cyanobacteria. Photochem Photobiol 61:32–42
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, UK, pp 443–480
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 321–362
Stirbet AD, Govindjee, Strasser BJ, Strasser RJ (1998) Chlorophyll fluorescence induction in higher plants: modeling and numerical simulation. J Theor Biol 193:131–151
Thomas JB, Voskuil W, Olsman H, De Boois HM (1962) Fluorescence-induction phenomena in isolated chloroplasts. Biochim Biophys Acta 59:224–226
Toth 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 1708:275–282
Trissl HW (1994) Response to Falkowski et al. Biophys J 66:925–926
Trissl HW, Gao Y, Wulf K (1993) Theoretical fluorescence induction curves derived from coupled differential equations describing the primary photochemistry of Photosystem II by an exciton/radical pair equilibrium. Biophys J 64:984–998
Vernotte C, Etienne AL, Briantais J-M (1979) Quenching of the Photosystem II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545:519–527
Vredenberg WJ (1970) Chlorophyll a fluorescence induction and changes in the electrical potential of the cellular membranes of green plant cells. Biochim Biophys Acta 223:230–239
Vredenberg WJ (2000) A three-state model for energy trapping and chlorophyll fluorescence in Photosystem II incorporating radical pair recombination. Biophys J 79:25–38
Vredenberg WJ (2004) System analysis and photoelectrochemical control of chlorophyll fluorescence in terms of trapping models of photosystem II: a challenging view. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration vol 19. Springer, Dordrecht, The Netherlands, pp 133–172
Vredenberg W, Durchan M, Prasil O (2007) On the chlorophyll a fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains. Photosynth Res. doi:10.1007/s11120-007-9150-08
Vredenberg WJ, Kasalicky V, Durchan M, Prasil O (2006) The chlorophyll a fluorescence induction pattern in chloroplasts upon repetitive single turnover excitations: accumulation and function of QB-nonreducing centers. Biochim Biophys Acta 1757:173–181
Walker DA (1981) Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation. Planta 143:273–278
Walker DA, Sivak MN (1986) Photosynthesis and phosphate: a cellular affair. Trends Biochem Sci 11:176–179
Walker DA, Sivak MN, Prinsley R, Cheesbrough JK (1983a) Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol 73:542–549
Walker DA, Horton P, Sivak MN, Quick WP (1983b) Antiparallel relationships between O2 evolution and slow fluorescence induction kinetics. Photobiochem Photobiophys 5:35–39
Warburg O (1920) Über die Geschwindigkeit der photochemischen kohlensäurezersetzung in lebenden zellen. Biochem Z 103:188–217
Williams WP, Allen JF (1987) State 1/state 2 changes in higher plants and algae. Photosynth Res 13:19–45
Williams WP, Salamon Z (1976) Enhancement studies of algae and isolated chloroplasts. Part I. Variabiliy of photosynthetic enhancement in Chlorella pyrenoidosa. Biochim. Biophys Acta 430:282–289
Wraight C, Crofts AR (1970) Energy-dependent quenching of chlorophyll a fluorescence in isolated chloroplasts. Eur J Biochem 17:319–327
Zhu XG, Govindjee, Baker NR, de Sturler E, Ort DR, Long SP (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with Photosystem II. Planta 223:114–133
Acknowledgments
We thank Prof. Shigeru Itoh, Nagoya University, Japan, for a generous gift of Acaryochloris marina culture; also, Emeritus Prof. Govindjee, University of Illinois, USA, and Hon. Prof. Prasanna Mohanty, Regional Plant Resource Center, Bhubaneswar. India for reading the manuscript and providing critical comments.
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Papageorgiou, G.C., Tsimilli-Michael, M. & Stamatakis, K. The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94, 275–290 (2007). https://doi.org/10.1007/s11120-007-9193-x
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DOI: https://doi.org/10.1007/s11120-007-9193-x