Abstract
Chlorophyll fluorescence induction during 0.4 to 200 ms multiple-turnover pulses (MTP) was measured in parallel with O2 evolution induced by the MTP light. Additionally, a saturating single-turnover flash (STF) was applied at the end of each MTP and the total MTP +STF O2 evolution was measured. Quantum yield of O2 evolution during the MTP transients was calculated and related to the number of open PSII centers, found from the STF O2 evolution. Proportionality between the number of open PSII and their running photochemical activity showed the quantum yield of open PSII remained constant independent of the closure of adjacent centers. During the induction, total fluorescence was partitioned between Fo of all the open centers and Fc of all the closed centers. The fluorescence yield of a closed center was 0.55 of the final Fm while less than a half of the centers were closed, but later increased, approaching Fm to the end of the induction. In the framework of the antenna/radical pair equilibrium model, the collective rise of the fluorescence of centers closed earlier during the induction is explained by an electric field, facilitating return of excitation energy from the Pheo− P680+ radical pair to the antenna.
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Abbreviations
- Chl:
-
Chlorophyll
- ETR:
-
Electron transport rate
- FI:
-
Fluorescence induction
- F max :
-
Fluorescence yield from the antenna
- Fm,:
-
Maximum fluorescence yield at the end of a saturation pulse
- F f :
-
Fluorescence yield after a single-turnover flash
- F c :
-
Running fluorescence yield of a closed center
- FR:
-
Far-red light
- LHCII:
-
Light-harvesting complex II
- MTP:
-
Multiple-turnover pulse
- PFD, PAD:
-
Photon flux density, incident and absorbed
- Pheo:
-
Pheophytin
- PQ:
-
Plastoquinone
- PSI, PSII:
-
Photosystem I and photosystem II
- P680:
-
Six-Chl complex in reaction center
- QA :
-
Primary quinone acceptor of PSII
- QB :
-
Secondary quinone acceptor of PSII
- RP:
-
Radical pair
- STF:
-
Single-turnover flash
- ∆E :
-
Voltage difference
References
Akhtar P, Zhang C, Do TN, Garab G, Lambrev PH, Tan H-S (2017) Two-dimensional spectroscopy of chlorophyll a excited-state equilibration in light-harvesting complex II. J Phys Chem Lett 8:257–263
Belgio E, Johnson MP, Jurić S, Ruban AV (2012) Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime—both the maximum and the nonphotochemically quenched. Biophys J 102:2761–2771
Bulychev AA, Vredenberg WJ (1999) Light-triggered electrical events in the thylakoid membrane of plant chloroplasts. Physiol Plant 105:577–584
Chukhutsina VU, Holzwarth AR, Croce R (2019) Time-resolved fluorescence measurements on leaves: principles and recent developments. Photosynth Res 140:355–369
Croce R, Dorra D, Holzwarth AR, Jennings RC (2000) Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochemistry 39:6341–6348
Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (DY) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into DY and DpH by ionic strength. Biochemistry 40:1226–1237
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 1102:91–106
Delosme R (1967) Étude de l'induction de fluorescence des algues vertes et des chloroplastes an début d'une illumination intense. Biochim Biophys Acta 143:108–128
Ehleringer J, Björkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants. Dependence on temperature, CO2 and O2 concentration. Plant Physiol 59:86–90
Farooq S, Chmeliov J, Wientjes E, Koehorst R, Bader A, Valkunas L, Trinkunas G, van Amerongen H (1918) Dynamic feedback of the photosystem II reaction centre on photoprotection in plants. Nature Plants 4:225–231
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
Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507:80–99
Gruber JM, Chmeliov J, Krüger TPJ, Valkunas L, van Grondelle R (2015) Singlet–triplet annihilation in single LHCII complexes. Phys Chem Chem Phys 17:19844–19853
Holzwarth AR, Müller MG, Niklas J, Lubitz W (2006) Ultrafast transient absorption studies on Photosystem I reaction centers from Chlamydomonas reinhardtii. 2: Mutations near the P700 reaction center chlorophylls provide new Insight into the nature of the primary electron donor. Biophys J 90:552–565
Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting. Chem Phys Lett 483:262–267
Joliot A, Joliot P (1964) Étude cinétique de la réaction photochimique libérant l'oxygène au cours de la photosynthése. C R Acad Sci Paris 258:4622–4625
Joliot P, Joliot A (1977) Evidence for a double hit process in photosystem II based on fluorescence studies. Biochim Biophys Acta 462:559–574
Joliot P, Joliot A (1981) Double photoreactions induced by laser flash as measured by oxygen emission. Biochim Biophys Acta 638:132–140
Junge W, Witt T (1968) On the ion transport system of photosynthesis. Investigations on a molecular level. Z Naturforsch 23b:244–254
Keuper HJK, Sauer K (1989) Effect of photosystem II reaction center closure on nanosecond fluorescence relaxation kinetics. Photosynth Res 20:85–103
Klughammer K, Siebke K, Schreiber U (2013) Continuous ECS-indicated recording of the proton-motive charge flux in leaves. Photosynth Res 117:471–487
Koblížek 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 induction study. Photosynth Res 68:141–152
Laisk A, Oja V (2013) Thermal phase and excitonic connectivity in fluorescence induction. Photosynth Res 117:431–448. https://doi.org/10.1007/s11120-013-9915-1
Laisk A, Oja V (2018) Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction. Photosynth Res 136:63–82. https://doi.org/10.1007/s11120-017-0439-y
Laisk A, Oja V, Rasulov B, Rämma H, Eichelmann H, Kasparova I, Pettai H, Padu E, Vapaavuori E (2002) A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves. Plant Cell Env 25:923–943
Laisk A, Eichelmann H, Oja V (2012) Oxygen evolution and chlorophyll fluorescence from multiple turnover light pulses: charge recombination in photosystem II in sunflower leaves. Photosynth Res 113:145–155
Laisk A, Oja V, Eichelmann H, Dall’Osto L, (2014) Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in State 1. Biochim Biophys Acta 1837:315–325
Laisk A, Eichelmann H, Oja V (2015) Oxidation of plastohydroquinone by photosystem II and by dioxygen in leaves. Biochim Biophys Acta 1847:565–575
Lambrev PH, Miloslavina Y, Jahns P, Holzwarth AR (2012) On the relationship between non-photochemical quenching and photoprotection of Photosystem II. Biochim Biophys Acta 1817:760–769
Leibl W, Breton J, Deprez J, Trissl H-W (1989) Photoelectric study on the kinetics of trapping and charge stabilization in oriented PS II membranes. Photosynth Res 22:257–275
Lyu H, Lazár D (2017a) Modeling the light-induced electric potential difference (ΔΨ), the pH difference (ΔpH) and the proton motive force across the thylakoid membrane in C3 leaves. J Theor Biol 413:11–23
Lyu H, Lazár D (2017b) Modeling the light-induced electric potential difference ΔΨ across the thylakoid membrane based on the transition state rate theory. Biochim Biophys Acta 1858:239–248
Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: I. Saturation characteristics and partial control by the photosystem II acceptor side. Z Naturforschung 42c:123–131
Oja V, Eichelmann H, Anijalg A, Rämma H, Laisk A (2010) Equilibrium or disequilibrium? A dual-wavelength investigation of photosystem I donors. Photosynth Res. https://doi.org/10.1007/s11120-010-9534-z
Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light harvesting. Nature 436:134–137. https://doi.org/10.1038/nature03795
Peterson RB, Oja V, Eichelmann H, Bichele I, Dall'Osto L, Laisk A (2014) Fluorescence F0 of photosystems II and I in developing C3 and C4 leaves, and implications on regulation of excitation balance. Photosynth Res 122:41–56
Pospíšil P, Dau H (2002) Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll f luorescence transients. Biochim Biophys Acta 1554:94–100
Prášil O, Kolber ZS, Falkowski PG (2018) Control of the maximal chlorophyll fluorescence yield by the QB binding site. Photosynthetica 56:150–162
Samson G, Bruce D (1996) Origin of the low yield of chlorophyll fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta 1276:147–153
Schansker G, To'th S, Kova'cs 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 1807:1032–1043
Schatz G, 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 84:8414–8418
Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405
Schreiber U (2002) Assessment of maximal fluorescence yield. Donor-side dependent quenching and QB-quenching. In: Kooten O, Snel J (eds) Plant Spectrophotometry: Applications and Basic research. Rozenberg, Amsterdam, pp 23–47
Schreiber U, Krieger A (1996) Two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett 397:131–135
Schreiber U, Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continous illumination: II. Partial control by the photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c:132–141
Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293
Sipka G, Müller P, Brettel K, Magyar M, Kovács L, Zhu Q, Xiao Y, Han G, Lambrev PH, Shen J-R, Garab G (2019) Redox transients of P680 associated with the incremental chlorophyll-a fluorescence yield rises elicited by a series of saturating flashes in diuron-treated photosystem II core complex of Thermosynechococcus vulcanus. Physiol Plantarum 166:22–32
Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61
Szczepaniak M, Sugiura M, Holzwarth AR (2008) The role of TyrD in the eelctron transfer kinetics in photosystem II. Biochim Biophys Acta 1777:1510–1517
Szczepaniak M, Sander J, Nowaczyk M, Müller MG, Rögner M, Holzwarth AR (2009) Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction center. Biophys J 96:621–631
Vredenberg WJ (2008) Analysis of initial chlorophyll fluorescence induction kinetics in chloroplasts in terms of rate constants of donor side quenching release and electron trapping in photosystem II. Photosynth Res 96:83–97
Vredenberg W, Durchan M, Prášil O (2009) Photochemical and photoelectrochemical quenching of chlorophyll fluorescence in photosystem II. Biochim Biophys Acta 1787:1468–1478
Acknowledgement
We appreciate constructive discussions with Alfred Holzwarth, facilitating formulation of conclusions.
Funding
The project was financed by University of Tartu (Basic funding), Institute of Technology, and by Estonian Academy of Science (A.L.).
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Laisk, A., Oja, V. Variable fluorescence of closed photochemical reaction centers. Photosynth Res 143, 335–346 (2020). https://doi.org/10.1007/s11120-020-00712-3
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DOI: https://doi.org/10.1007/s11120-020-00712-3