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Oxygen evolution and chlorophyll fluorescence from multiple turnover light pulses: charge recombination in photosystem II in sunflower leaves

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Abstract

Oxygen evolution and Chl fluorescence induction were measured during multiple turnover light pulses (MTP) of 630-nm wavelength, intensities from 250 to 8,000 μmol quanta m−2 s−1 and duration from 0.3 to 200 ms in sunflower leaves at 22 °C. The ambient O2 concentration was 10–30 ppm and MTP were applied after pre-illumination under far-red light (FRL), which oxidized plastoquinone (PQ) and randomized S-states because of the partial excitation of PSII. Electron (e ) flow was calculated as 4·O2 evolution. Illumination with MTP of increasing length resulted in increasing O2 evolution per pulse, which was differentiated against pulse length to find the time course of O2 evolution rate with sub-millisecond resolution. Comparison of the quantum yields, Y IIO = e /hν from O2 evolution and Y IIF = (F m − F)/F m from Chl fluorescence, detected significant losses not accompanied by fluorescence emission. These quantum losses are discussed to be caused by charge recombination between Q A and oxidized TyrZ at a rate of about 1,000 s−1, either directly or via the donor side equilibrium complex QA → P +D1  ↔ TyrZox, or because of cycling facilitated by Cyt b 559. Predicted from the suggested mechanism, charge recombination is enhanced by damage to the water-oxidizing complex and by restricted PSII acceptor side oxidation. The rate of PSII charge recombination/cycling is fast enough for being important in photoprotection.

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Abbreviations

A/D:

Analog-to-digital converter

ETR:

Electron transport rate

F 0, F, F m :

Fluorescence yields: minimum, steady-state and maximum

FRL:

Far-red light

LED:

Light-emitting diode

MTP:

Multiple turnover pulse

PAD, PFD:

Photon flux density, absorbed and incident

PD1 :

PSII donor pigment

PQ(H2):

Plastoquinone (reduced)

PSII:

Photosystem II

QA, QB :

PSII acceptor side electron carriers

RC:

Reaction center

STF:

Single turnover flash

TyrZ:

PSII donor side electron carrier, tyrosine

WOC:

Water-oxidizing complex

References

  • Allen JF (2003) State transition: a question of balance. Science 299:1530–1532

    Article  PubMed  CAS  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origin. Planta 170:489–504

    Article  Google Scholar 

  • Buser CA, Thompson LK, Diner BA, Brudvig GW (1990) Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry 29:8977–8985

    Article  PubMed  CAS  Google Scholar 

  • Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b559 in oxygen-evolving photosystem II. Biochemistry 31:11449–11459

    Article  PubMed  CAS  Google Scholar 

  • Butler WL, Kitajima WL (1975) Fluorescence quenching in photosystem 2 of chloroplasts. Biochim Biophys Acta 376:116–125

    Article  PubMed  CAS  Google Scholar 

  • 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 429:49–52

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Nguyen AP, Debus RJ (1995) Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34:5839–5858

    Article  PubMed  CAS  Google Scholar 

  • Crofts AR, Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • De Wijn R, van Gorkom HJ (2002) The rate of charge recombination in photosystem II. Biochim Biophys Acta 1553:302–308

    Article  PubMed  Google Scholar 

  • De Wijn R, Schrama T, van Gorkom HJ (2001) Secondary stabilization reactions and proton-coupled electron transport in photosystem II investigated by electroluminescence and fluorescence spectroscopy. Biochemistry 40:5821–5834

    Article  PubMed  Google Scholar 

  • Diner BA, Force DA, Randall DW, Britt RD (1998) Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine YZ in Mn-depleted core complexes of photosystem II. Biochemistry 37:17931–17943

    Article  PubMed  CAS  Google Scholar 

  • Eckert H-J, Renger G, Witt HT (1984) Reduction kinetics of the photo-oxidized chlorophyll a +II in the nanosecond range: measurements of the absorption changes at 688 nm under repetitive flash excitation. FEBS Lett 167:316–320

    Article  CAS  Google Scholar 

  • Ehleringer J, Björkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants. Plant Physiol 59:86–90

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer J, Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiol 73:555–559

    Article  PubMed  CAS  Google Scholar 

  • Eichelmann H, Laisk A (2000) Cooperation of photosystems II and I in leaves as analysed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800 nm. Plant Cell Physiol 41:138–147

    Article  PubMed  CAS  Google Scholar 

  • Eichelmann H, Oja V, Peterson RB, Laisk A (2011) The rate of nitrite reduction in leaves as indicated by O2 and CO2 exchange during photosynthesis. J Exp Bot 62:2205–2215

    Article  PubMed  CAS  Google Scholar 

  • Feyziyev Y, van Rotterdam BJ, Bernat G, Styring S (2003) Electron transfer from cytochrome b559 and tyrosineD to the S2 and S3 states of the water oxidizing complex in photosystem II. Chem Phys 294:415–431

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kaminskaya O, Shuvalov VA, Renger G (2007) Evidence for a novel quinone-binding site in the photosystem II (PS II) complex that regulates the redox potential of cytochrome b559. Biochemistry 46:1091–1105

    Article  PubMed  CAS  Google Scholar 

  • Kopecky J, Azarkovich M, Pfündel EE, Shuvalov VA, Heber U (2005) Thermal dissipation of light energy is regulated differently and by different mechanisms in lichens and higher plants. Plant Biol 7:1–13

    Article  Google Scholar 

  • Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Laisk A, Eichelmann H, Oja V, Rasulov B, Rämma H (2006) Photosystem II cycle and alternative electron flow in leaves. Plant Cell Physiol 47:972–983

    Article  PubMed  CAS  Google Scholar 

  • 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 48:1575–1588

    Article  PubMed  CAS  Google Scholar 

  • Laisk A, Talts E, Oja V, Eichelmann H, Peterson R (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95

    Article  PubMed  CAS  Google Scholar 

  • Long SP, Postl WF, Bolhar-Nordenkampf HR (1993) Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic grou**s. Planta 189:226–234

    Article  CAS  Google Scholar 

  • Miyake C, Yokota A (2001) Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiol 42:508–515

    Article  PubMed  CAS  Google Scholar 

  • Moser CC, Page CC, Dutton PL (2005) Tunneling in PSII. Photochem Photobiol Sci 4:933–939

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Berg A, Berkowicz SM, Kaplan A, Keren N (2011) Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiol Plantarum 142:79–86

    Article  CAS  Google Scholar 

  • Oja V, Laisk A (2000) Oxygen yield from single turnover flashes in leaves: non-photochemical excitation quenching and the number of active PSII. Biochim Biophys Acta 1460:291–301

    Article  PubMed  CAS  Google Scholar 

  • Oja V, Eichelmann H, Anijalg A, Rämma H, Laisk A (2010) Equilibrium or disequilibrium? A dual-wavelength investigation of photosystem I donors. Photosynth Res 103:153–166

    Article  PubMed  CAS  Google Scholar 

  • Oja V, Eichelmann H, Laisk A (2011) Oxygen evolution from single- and multiple-turnover light pulses: temporal kinetics of electron transport through PSII in sunflower leaves. Photosynth Res 110:99–109

    Article  PubMed  CAS  Google Scholar 

  • Pettai H, Oja V, Freiberg A, Laisk A (2005) Photosynthetic activity of far-red light in green plants. Biochim Biophys Acta 1708:311–321

    Article  PubMed  CAS  Google Scholar 

  • 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 1184:178–192

    Article  CAS  Google Scholar 

  • Reifarth F, Christen G, Seelinger AG, Dörmann P, Benning C, Renger G (1997) Modification of the water oxidizing complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol. Biochemistry 36:11769–11776

    Article  PubMed  CAS  Google Scholar 

  • Reinman S, Mathis P, Conjeaud H, Stewart A (1981) Kinetics of reduction of the primary donor of photosystem II. Influence of pH in various preparations. Biochim Biophys Acta 635:429–433

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2010) The light reactions of photosynthesis. Current Sci 98:1305–1319

    CAS  Google Scholar 

  • Renger G, Eckert H-J, Buchwald HE (1978) On the detection of a new rapid-recovery kinetics of photo-oxidized chlorophyll-a II in isolated chloroplasts under repetitive flash illumination. FEBS Lett 90:10–14

    Article  CAS  Google Scholar 

  • Robinson H, 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

    Article  CAS  Google Scholar 

  • Seaton GGR, Walker DA (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc R Soc Lond B 242:29–35

    Article  Google Scholar 

  • Sharp RE, Matthews MA, Boyer JS (1984) Kok effect and the quantum yield of photosynthesis. Light partially inhibits dark respiration. Plant Physiol 75:95–101

    Article  PubMed  CAS  Google Scholar 

  • Strasser R, Tsimili-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. A signature of photosynthesis. Springer, Dordrecht, The Netherlands, pp 321–362

    Google Scholar 

  • Thompson LK, Brudvig GW (1988) Cytochrome b-559 may function to protect photosystem II from photoinhibition. Biochemistry 27:6653–6658

    Article  PubMed  CAS  Google Scholar 

  • Vredenberg VJ (2008) 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 91:58–65

    Article  CAS  Google Scholar 

  • Whitmarsh J, Pakrasi HB (1996) Form and function of cytochrome b-559. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer, The Netherlands

    Google Scholar 

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Laisk, A., Oja, V. & Eichelmann, H. Oxygen evolution and chlorophyll fluorescence from multiple turnover light pulses: charge recombination in photosystem II in sunflower leaves. Photosynth Res 113, 145–155 (2012). https://doi.org/10.1007/s11120-012-9751-8

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