Revisiting the QA model of chlorophyll-a fluorescence induction: new perspectives to monitor the photochemical activity and structural dynamics of photosystem II
Jazyk angličtina Země Nizozemsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
41128974
PubMed Central
PMC12549761
DOI
10.1007/s11120-025-01178-x
PII: 10.1007/s11120-025-01178-x
Knihovny.cz E-zdroje
- Klíčová slova
- F v/F m, Chlorophyll-a fluorescence, Conformational transitions, Dielectric relaxation, Photosystem II, QA model,
- MeSH
- chlorofyl a MeSH
- chlorofyl * metabolismus chemie MeSH
- fluorescence MeSH
- fotosyntéza MeSH
- fotosystém II (proteinový komplex) * metabolismus chemie MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- chlorofyl a MeSH
- chlorofyl * MeSH
- fotosystém II (proteinový komplex) * MeSH
The technique of chlorophyll-a fluorescence induction (ChlF) is widely used in plant biology. The 'mainstream', so-called QA model of ChlF, posits that the reaction centers (RCs) of Photosystem-II (PSII) exist in two states, quenched (Fo) or open (PSIIO), and unquenched (Fm) or closed (PSIIC), containing the primary quinone acceptor, QA, in oxidized and reduced state, respectively; and that the quantum yield of PSII photochemistry of a dark-adapted sample is Y(II) = Fv/Fm, where Fv=Fm-Fo. The widespread application of ChlF, with user-friendly instruments, and the use of the QA model, have substantially contributed to our understanding of the operation of the photosynthetic machineries under different environmental conditions. However, recent experimental data - multiple light-induced fluorescence increments in PSIIC; the complex, pH and temperature dependent kinetic and spectral features of key ChlF parameters; twith enhanced stabilization of the charges - cannot be reconciled with the QA model. These features are explained by subtle conformational transitions driven by stationary and transient electric fields and associated dielectric relaxation processes. This interpretation, while invites further studies, places the hitherto unknown structural and functional plasticity of the RC matrix in the context of its physiological significance.
Department of Physics Faculty of Science University of Ostrava Ostrava Czech Republic
Institute of Plant Biology HUN REN Biological Research Centre Szeged Hungary
Zobrazit více v PubMed
Abgaryan GA, Christophorov LN, Goushcha AO, Holzwarth AR, Kharkyanen VN, Knox PP, Lukashev EA (1998) Effects of mutual influence of photoinduced electron transitions and slow structural rearrangements in bacterial photosynthetic reaction centers. J Biol Phys 24(1):1–17. 10.1023/A:1005039023702 PubMed PMC
Allen JP, Chamberlain KD, Williams JC (2022) Identification of amino acid residues in a proton release pathway near the bacteriochlorophyll dimer in reaction centers from rhodobacter sphaeroides. Photosynth Res. 10.1007/s11120-022-00968-x PubMed
Ananyev G, Dismukes GC (2005) How fast can photosystem II split water? Kinetic performance at high and low frequencies. Photosynth Res 84:355–365. 10.1007/s11120-004-7081-1 PubMed
Andréasson U, Andréasson LE (2003) Characterization of a semi-stable, charge-separated state in reaction centers from rhodobacter sphaeroides. Photosynth Res 75(3):223–233. 10.1023/A:1023944605460 PubMed
Barabash YM, Berezetskaya NM, Christophorov LN, Goushcha AO, Kharkyanen VN (2002) Effects of structural memory in protein reactions. J Chem Phys 116(10):4339–4352. 10.1063/1.1447906
Blankenship RE (2021) Molecular Mechanisms of Photosynthesis, 3rd Edition. UK: Wiley-Blackwell, Chichester
Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29(1):345–378. 10.1146/annurev.pp.29.060178.002021
Croce R, van Amerongen H (2011) Light-harvesting and structural organization of photosystem II: from individual complexes to thylakoid membrane. J Photochem Photobiology B Biology 104(1–2):142–153. 10.1016/j.jphotobiol.2011.02.015
Cseh Z, Rajagopal S, Tsonev T, Busheva M, Papp E, Garab G (2000) Thermooptic effect in Chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochem 39(49):15250–15257. 10.1021/bi001600d PubMed
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
Delosme R, Joliot P (2002) Period four oscillations in chlorophyll a fluorescence. Photosynth Res 73:165–168. 10.1023/A:1020430610627 PubMed
Demeter S, Rozsa Z, Vass I, Sallai A (1985) Thermoluminescence study of charge recombination in photosystem II at low temperatures. I. Characterization of the Zv and A thermoluminescence bands. Biochim Biophys Acta 809:369–378. 10.1016/0005-2728(85)90187-2
Deshmukh SS, Tang K, Kalman L (2011a) Lipid binding to the carotenoid binding site in photosynthetic reaction centers. J Am Chem Soc 133(40):16309–16316. 10.1021/ja207750z PubMed
Deshmukh SS, Williams JC, Allen JP, Kalman L (2011b) Light-induced conformational changes in photosynthetic reaction centers: dielectric relaxation in the vicinity of the dimer. Biochem 50(3):340–348. 10.1021/bi101496c PubMed
Ducruet J-M, Vass I (2009) Thermoluminescence: experimental. Photosynth Res 101:195–204. 10.1007/s11120-009-9436-0 PubMed
Duysens LMN, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. Studies on microalgae and photosynthetic bacteria. Japanese Society of Plant Physiologists, University of Tokyo, Tokyo, pp 353–372
Garab G (2024) Revisiting the nonregulatory, constitutive nonphotochemical quenching of the absorbed light energy in oxygenic photosynthetic organisms. Photosynthetica 62:204–208. 10.32615/ps.2024.022 PubMed PMC
Garab G, Magyar M, Sipka G, Lambrev PH (2023) New foundations for the physical mechanism of variable chlorophyll a fluorescence. Quantum efficiency versus the light-adapted state of photosystem II. J Exp Bot 74:5458–5471. 10.1093/jxb/erad252 PubMed
Garab G, Böde K, Dlouhý O, Násztor Z, Karlický V, Dér A, Špunda V (2025) Lipid polymorphism of plant thylakoid membranes. The dynamic exchange model – facts and hypotheses. Physiol Plant 177:e70230. 10.1111/ppl.70230 PubMed PMC
Garbers A, Reifarth F, Kurreck J, Renger G, Parak F (1998) Correlation between protein flexibility and electron transfer from Q(A)/(-·) to Q(B) in PSII membrane fragments from spinach. Biochemistry 37:11399–11404. 10.1021/bi980296+ PubMed
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. BBA 990(1):87–92. 10.1016/S0304-4165(89)80016-9
Genty B, Harbinson J, Cailly AL, Rizza F (1996) Fate of excitation at PS II in leaves: the nonphotochemical side — The Third BBSRC Robert Hill Symposium on Photosynthesis, Abstract No. P28: pp. University of Sheffield, Department of Molecular Biology and Biotechnology, Western Bank, Sheffield, UK
Goushcha AO, Manzo AJ, Scott GW, Christophorov LN, Knox PP, Barabash YM, Kapoustina MT, Berezetska NM, Kharkyanen VN (2003) Self-regulation phenomena applied to bacterial reaction centers: 2. Nonequilibrium adiabatic potential: dark and light conformations revisited. Biophys J 84(2 Pt 1):1146–1160. 10.1016/S0006-3495(03)74930-3 PubMed PMC
Govindjee G (1995) Sixty-three years since kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160
Gulbinas V, Karpicz R, Garab G, Valkunas L (2006) Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochem 45(31):9559–9565. 10.1021/bi060048a PubMed
Hussein R, Graça A, Forsman J, Aydin AU, Hall M, Gaetcke J, Chernev P, Wendler P, Dobbek H, Messinger J, Zouni A, Schröder WP (2024) Cryo–electron microscopy reveals hydrogen positions and water networks in photosystem II. Science 384:1349–1355. 10.1126/science.adn6541 PubMed
Jennings RC, Bassi R, Garlaschi FM, Dainese P, Zucchelli G (1993) Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna. Biochemistry 32:3203–3210 PubMed
Joliot A, Joliot P (1964) Étude cinétique de La réaction photochimique libérant l’oxygéne Au cours de La photosynthése. CR Acad Sci Paris 258:4622–4625 (in French) PubMed
Joliot P, Joliot A (1979) Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. BBA - Bioenergetics 546(1):93–105. 10.1016/0005-2728(79)90173-7 PubMed
Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli DB, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serodio J, Suresh K, Szulc W, Tambussi E, Yanniccari, Zivcak M (2014) Frequently asked questions about
Kautsky H, Hirsch A (1931) Neue versuche Zur kohlensaureassimilation. Naturwissenschaften 19:964. 10.1007/BF01516164
Kirmaier C, Holten D, Parson WW (1985) Temperature and detection-wavelength dependence of the picosecond electron-transfer kinetics measured in
Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and promary photochemistry in chloroplasts by dibromothymoquinone. BBA Bioenergetics 376:105–116. 10.1016/0005-2728(75)90209-1 PubMed
Klughammer C, Schreiber U (2008) Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1: 27–35
Klughammer C, Schlosser F, Schreiber U (2024) Flash-kinetics as a complementary analytical tool in PAM fluorimetry. Photosynth Res 161:151–176. 10.1007/s11120-024-01101-w PubMed PMC
Kono M, Miyata K, Matsuzawa S, Noguchi T, Oguchi R, Suzuki Y, Terashima I (2022) Mixed population hypothesis of the active and inactive PSII complexes opens a new door for photoinhibition and fluorescence studies: an ecophysiological perspective. Funct Plant Biol 49: 917–925. 10.1071/FP21355
Krieger A, Rutherford AW, Johnson GN (1995) On the determination of redox midpoint potential of the primary Quinone electron-acceptor, Q(a), in Photosystem-II. Biochim Biophys Acta-Bioenergetics 1229:193–201. 10.1016/0005-2728(95)00002-z
Laisk A, Oja V (2020) Variable fluorescence of closed photochemical reaction centers. Photosynth Res 143:335–346. 10.1007/s11120-020-00712-3 PubMed
Lakowicz JR (2006) Principles of Fluorescence Spectroscopy. 3rd Edition Springer
Lambreva MD, Zobnina V, Antal TK, Peeva VN, Giardi MT, Bertalan I, Johanningmeier U, Virtanen O, Ray M, Mulo P, Polticelli F, Tyystjärvi E, Rea G (2025) Redesign of the
Lazar D, Pospisil P (1999) Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3’,4’-dichlorophenyl)-1,1-dimethylure barley leaves at room and high temperatures. Eur Biophys J Biophy 28(6):468–477. 10.1007/s002490050229
Lukashev EP, Knox PP, Krasilnikov PM, Seifullina NK, Rubin AB (2014) Mechanisms of anomalous temperature dependence of the recombination of the photoseparated charges between bacteriochlorophyll and primary Quinone in Rb. sphaeroides: the role of RC hydrogen bonds. Dokl Biochem Biophys 459(1):199–203. 10.1134/S1607672914060052 PubMed
Magyar M, Sipka G, Kovács L, Ughy B, Zhu Q, Han G, Špunda V, Lambrev PH, Shen JR, Garab G (2018) Rate-limiting steps in the dark-to-light transition of photosystem II - revealed by chlorophyll-a fluorescence induction. Sci Rep 8(1):2755. 10.1038/s41598-018-21195-2 PubMed PMC
Magyar M, Akhtar P, Sipka G, Han W, Li X, Han G, Shen JR, Lambrev PH, Garab G (2022) Dependence of the rate-limiting steps in the dark-to-light transition of photosystem II on the lipidic environment of the reaction center. Photosynthetica 60(1):147–156. 10.32615/ps.2022.016 PubMed PMC
Magyar M, Sipka G, Han WH, Li XY, Han GY, Shen J-R, Lambrev PH, Garab G (2023) Characterization of the rate-limiting steps in the dark-to-light transitions of closed photosystem II: temperature dependence and invariance of waiting times during multiple light reactions. Int J Mol Sci 24:94. 10.3390/ijms24010094
Magyar M, Akhtar P, Sipka G, Domonkos I, Han W, Li X et al (2024) Effects of lipids on the rate-limiting steps in the dark-to-light transition of photosystem II core complex of PubMed PMC
Magyar M, Sipka G, Domonkos I, Chen X, Wang X, Han G, Shen J-R, Lambrev PH, Garab G (2025) The role of protonation processes in the gradual formation of the light-adapted charge-separated state of photosystem II. Front Photobiology 3:1623224. 10.3389/fphbi.2025.1623224
Malferrari M, Mezzetti A, Francia F, Venturoli G (2013) Effects of dehydration on light-induced conformational changes in bacterial photosynthetic reaction centers probed by optical and differential FTIR spectroscopy. Biochim Biophys Acta Bioenerg 1827:328–339. 10.1016/j.bbabio.2012.10.009
Mattila H, Mishra S, Tyystjärvi T, Tyystjärvi E (2023) Singlet oxygen production by photosystem II is caused by misses of the oxygen evolving complex. New Phytol 237: 113–125. 10.1111/nph.18514
Morin P (1964) Études des cinétiques de fluorescence de La chlorophylle in vivo, Dans Les premiers instants Qui suivent Le début de l’illumination. J Chim Phys 61:674–680
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and Understanding some new applications. J Exp Bot 64:3983–3998. 10.1093/jxb/ert208 PubMed
Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous Illumination.1. Saturation characteristics and partial control by the Photosystem-Ii acceptor side. Z Naturforsch C 42(11–12):1246–1254. 10.1515/znc-1987-11-1217
Nguyen HL, Do TN, Zhong K, Akhtar P, Jansen TLC, Knoester J, Caffarri S, Lambrev PH, Tan H-S (2024) Inter- subunit energy transfer processes in a minimal plant photosystem II supercomplex. Sci Adv 10:eadh0911. 10.1126/sciadv.adh0911 PubMed PMC
Oja V, Laisk A (2020) Time- and reduction-dependent rise of photosystem II fluorescence during microseconds-long inductions in leaves. Photosynth Res 145:209–225. 10.1007/s11120-020-00783-2 PubMed
Ostroumov EE, Khan YR, Scholes GD, Govindjee (2014) Photophysics of photosynthetic Pigment-Protein complexes. In: Demmig-Adams et al (eds) non-photochemical quenching and energy dissipation in Plants, algae and cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer
Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Netherlands. 10.1007/978-1-4020-3218-9
Remelli W, Santabarbara S (2018) Excitation and emission wavelength dependence of fluorescence spectra in whole cells of the Cyanobacterium
Renger G, Gleiter HM, Haag E, Reifarth F (1993) Photosystem II: thermodynamics and kinetics of electron transport from Q
Romero E, Novoderezhkin VI, van Grondelle R (2017) Quantum design of photosynthesis for bio-inspired solar-energy conversion. Nature 543(7645):355–365. 10.1038/nature22012 PubMed
Ruan M, Xu Y, Liao G, Wang Z, Chen H, Weng Y (2025) Investigation of transient temperature rising of Light-Harvesting complex II by nonradiative heat dissipation at the protein level. J Phys Chem Lett 2025(16 1):308–316. 10.1021/acs.jpclett.4c03056
Ruban AV, Saccon F (2022) Chlorophyll a de-excitation pathways in the LHCII antenna. J Chem Phys 156(7):070902. 10.1063/5.0073825 PubMed
Santabarbara S, Villafiorita Monteleone F, Remelli W, Rizzo F, Menin B, Casazza AP (2019) Comparative excitation–emission dependence of the PubMed
Schansker G, Tóth SZ, Kovács L, Holzwarth AR, Garab G (2011) Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise. BBA - Bioenergetics 1807(9):1032–1043. 10.1016/j.bbabio.2011.05.022 PubMed
Schansker G, Tóth SZ, Holzwart AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynth Res 120(1):43–58. 10.1007/s11120-013-9806-5 PubMed
Schlodder E, Cetin M, Lendzian F (2015) Temperature dependence of the oxidation kinetics of TyrZ and TyrD in oxygen-evolving photosystem II complexes throughout the range from 320 K to 5 K. Biochim Biophys Acta-Bioenergetics 1847(10):1283–1296. 10.1016/j.bbabio.2015.07.005
Schreiber U, Krieger A (1996) Hypothesis: two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett 397:131–135. 10.1016/S0014-5793(96)01176-3 PubMed
Schreiber U, Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the photosystem II donor side and possible ways of interpretation. Z Naturforsch 42c:1255–1264
Shen JR (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48. 10.1146/annurevarplant-050312-120129 PubMed
Shevela D, Kern JF, Govindjee G, Messinger J (2023) Solar energy conversion by photosystem II: principles and structures. Photosynth Res 156:279–307. 10.1007/s11120-022-00991-y PubMed PMC
Shibata Y, Nishi S, Kawakami K, Shen JR, Renger T (2013) Photosystem II does not possess a simple excitation energy funnel: time-resolved fluorescence spectroscopy Meets theory. JACS 135(18):6903–6914. 10.1021/ja312586p
Siegbahn PE (2013) Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O-O bond formation and O2 release. Biochim Biophys Acta 1827:1003–1019. 10.1016/j.bbabio.2012.10.006 PubMed
Sipka G, Kis M, Maróti P (2018) Characterization of mercury(II)-induced Inhibition of photochemistry in the reaction center of photosynthetic bacteria. Photosynth Res 136(3):379–392. 10.1007/s11120-017-0474-8 PubMed
Sipka G, Müller P, Brettel K, Magyar M, Kovács L, Zhu QJ, Xiao YA, Han GY, Lambrev PH, Shen JR, 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 PubMed
Sipka G, Magyar M, Mezzetti A, Akhtar P, Zhu QJ, Xiao YA, Han GY, Santabarbara S, Shen JR, Lambrev PH, Garab G (2021) Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. Plant Cell 33(4):1286–1302. 10.1093/plcell/koab008 PubMed PMC
Sipka G, Nagy L, Magyar M, Akhtar P, Shen JR, Holzwarth AR, Lambrev PH, Garab G (2022) Light-induced reversible reorganizations in closed type II reaction centre complexes: physiological roles and physical mechanisms. Open Biology 12:220297. 10.1098/rsob.220297 PubMed PMC
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. 10.1007/s11120-012-9754-5 PubMed
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Advances in Photosynthesis and Respiration, vol 19. Springer, Dordrecht, pp 463–495
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(2):621–631. 10.1016/j.bpj.2008.09.036) PubMed PMC
Treves H, Raanan H, Kedem I, Murik O, Keren N, Zer H, Berkowicz SM, Giordano M, Norici A, Shotland Y, Ohad I, Kaplan A (2016) The mechanisms whereby the green Alga chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. New Phytol 210(4):1229–1243. 10.1111/nph.13870 PubMed
Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205. 10.1016/j.tplants.2009.01.009 PubMed
Vavilin DV, Ermakova-Gerdes SY, Keilty AT, Vermaas WF (1999) Tryptophan at position 181 of the D2 protein of photosystem II confers quenching of variable fluorescence of chlorophyll: implications for the mechanism of energy-dependent quenching. Biochem 38(44):14690–14696. 10.1021/bi9915622 PubMed
Vredenberg W (2011) Kinetic analyses and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. BioSystems 103(2):138–151. 10.1016/j.biosystems.2010.10.016 PubMed
Wientjes E, van Amerongen H, Croce R (2013) Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J Phys Chem B 117:11200–11208 PubMed
Yang S-J, Arsenault EA, Orcutt K, Iwai M, Yoneda Y, Fleming GR (2022) From antenna to reaction center: pathways of ultrafast energy and charge transfer in photosystem II. Proc Natl Acad Sci USA 119:e2208033119 PubMed PMC
Zaharieva I, Dau H (2019) Energetics and kinetics of S-state transitions monitored by delayed chlorophyll fluorescence. Front Plant Sci 10:386. 10.3389/fpls.2019.00386 PubMed PMC
Zuo G (2025) Non-photochemical quenching (NPQ) in photoprotection: insights into NPQ levels required to avoid photoinactivation and photoinhibition. New Phytol 246:1967–1974. 10.1111/nph.70121 PubMed