In our earlier works, we have identified rate-limiting steps in the dark-to-light transition of PSII. By measuring chlorophyll a fluorescence transients elicited by single-turnover saturating flashes (STSFs) we have shown that in diuron-treated samples an STSF generates only F1 (< Fm) fluorescence level, and to produce the maximum (Fm) level, additional excitations are required, which, however, can only be effective if sufficiently long Δτ waiting times are allowed between the excitations. Biological variations in the half-rise time (Δτ 1/2) of the fluorescence increment suggest that it may be sensitive to the physicochemical environment of PSII. Here, we investigated the influence of the lipidic environment on Δτ 1/2 of PSII core complexes of Thermosynechococcus vulcanus. We found that while non-native lipids had no noticeable effects, thylakoid membrane lipids considerably shortened the Δτ 1/2, from ~ 1 ms to ~ 0.2 ms. The importance of the presence of native lipids was confirmed by obtaining similarly short Δτ 1/2 values in the whole T. vulcanus cells and isolated pea thylakoid membranes. Minor, lipid-dependent reorganizations were also observed by steady-state and time-resolved spectroscopic measurements. These data show that the processes beyond the dark-to-light transition of PSII depend significantly on the lipid matrix of the reaction center.

Faculty of Science University of Ostrava Ostrava Czech Republic

Institute of Plant Biology Biological Research Centre Szeged Hungary

Photosynthesis Research Center Key Laboratory of Photobiology Institute of Botany Chinese Academy of Sciences Beijing China

Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology Okayama University Okayama Japan

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Akhtar P., Dorogi M., Pawlak K. et al.: Pigment interactions in light-harvesting complex II in different molecular environments. – J. Biol. Chem. 290: 4877-4886, 2015. https://www.sciencedirect.com/science/article/pii/S0021925819468968?via%3Dihub PubMed PMC

Akhtar P., Lingvay M., Kiss T. et al.: Excitation energy transfer between Light-harvesting complex II and Photosystem I in reconstituted membranes. – BBA-Bioenergetics 1857: 462-472, 2016. https://www.sciencedirect.com/science/article/pii/S0005272816300184?via%3Dihub PubMed

Alfonso M., Montoya G., Cases R. et al.: Core antenna complexes, Cp43 and Cp47, of higher plant photosystem II. Spectral properties, pigment stoichiometry, and amino acid composition. – Biochemistry-US 33: 10494-10500, 1994. https://pubs.acs.org/doi/abs/10.1021/bi00200a034 PubMed DOI

Andrizhiyevskaya E.G., Chojnicka A., Bautista J.A. et al.: Origin of the F685 and F695 fluorescence in Photosystem II. – Photosynth. Res. 84: 173-180, 2005. https://link.springer.com/article/10.1007/s11120-005-0478-7 PubMed DOI

Brettel K., Schlodder E., Witt H.T.: Nanosecond reduction kinetics of photooxidized chlorophyll-aII (P-680) in single flashes as a probe for the electron pathway, H+-release and charge accumulation in the O2-evolving complex. – BBA-Bioenergetics 766: 403-415, 1984. https://www.sciencedirect.com/science/article/pii/0005272884902561?via%3Dihub

Cardona T., Sedoud A., Cox N., Rutherford A.W.: Charge separation in Photosystem II: A comparative and evolutionary overview. – BBA-Bioenergetics 1817: 26-43, 2012. https://www.sciencedirect.com/science/article/pii/S0005272811001782?via%3Dihub PubMed

Chylla R.A., Garab G., Whitmarsh J.: Evidence for slow turnover in a fraction of Photosystem II complexes in thylakoid membranes. – BBA-Bioenergetics 894: 562-571, 1987. https://www.sciencedirect.com/science/article/pii/0005272887901368?via%3Dihub

Delosme R.: [Study of the induction of fluorescence in green algae and chloroplasts at the onset of an intense illumination.] – BBA-Bioenergetics 143: 108-128, 1967. [In French] https://www.sciencedirect.com/science/article/pii/0005272867901156?via%3Dihub PubMed

Dimroth P., Kaim G., Matthey U.: Crucial role of the membrane potential for ATP synthesis by F1Fo ATP synthases. – J. Exp. Biol. 203: 51-59, 2000. https://journals.biologists.com/jeb/article/203/1/51/8299/Crucial-role-of-the-membrane-potential-for-ATP PubMed

Dlouhý O., Kurasová I., Karlický V. et al.: Modulation of non-bilayer lipid phases and the structure and functions of thylakoid membranes: effects on the water-soluble enzyme violaxanthin de-epoxidase. – Sci. Rep.-UK 10: 11959, 2020. https://www.nature.com/articles/s41598-020-68854-x PubMed PMC

Duchêne S., Siegenthaler P.-A.: Do glycerolipids display lateral heterogeneity in the thylakoid membrane? – Lipids 35: 739-744, 2000. https://aocs.onlinelibrary.wiley.com/doi/abs/10.1007/s11745-000-0580-4 PubMed DOI

Duncan A.L., Robinson A.J., Walker J.E.: Cardiolipin binds selectively but transiently to conserved lysine residues in the rotor of metazoan ATP synthases. – P. Natl. Acad. Sci. USA 113: 8687-8692, 2016. https://www.pnas.org/doi/full/10.1073/pnas.1608396113 PubMed DOI PMC

France L.L., Geacintov N.E., Breton J., Valkunas L.: The dependence of the degrees of sigmoidicities of fluorescence induction curves in spinach chloroplasts on the duration of actinic pulses in pump-probe experiments. – BBA-Bioenergetics 1101: 105-119, 1992. https://www.sciencedirect.com/science/article/pii/016748389290474R?via%3Dihub

Garab G., van Amerongen H.: Linear dichroism and circular dichroism in photosynthesis research. – Photosynth. Res. 101: 135-146, 2009. https://link.springer.com/article/10.1007/s11120-009-9424-4 PubMed DOI PMC

Gombos Z., Várkonyi Z., Hagio M. et al.: Phosphatidylglycerol requirement for the function of electron acceptor plastoquinone QB in the photosystem II reaction center. – Biochemistry-US 41: 3796-3802, 2002. PubMed

Goss R., Latowski D.: Lipid dependence of xanthophyll cycling in higher plants and algae. – Front. Plant Sci. 11: 455, 2020. https://www.frontiersin.org/articles/10.3389/fpls.2020.00455/full PubMed DOI PMC

Haferkamp S., Haase W., Pascal A.A. et al.: Efficient light harvesting by photosytem II requires an optimized protein packing density in grana thylakoids. – J. Biol. Chem. 285: 17020-17028, 2010. https://www.sciencedirect.com/science/article/pii/S0021925819356273?via%3Dihub PubMed PMC

Hansson O., Wydrzynski T.: Current perceptions of Photo- system II. – Photosynth. Res. 23: 131-162, 1990. https://link.springer.com/article/10.1007/BF00035006 PubMed DOI

Heinemeyer J., Eubel H., Wehmhöner D. et al.: Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. – Phytochemistry 65: 1683-1692, 2004. https://www.sciencedirect.com/science/article/pii/S0031942204001840?via%3Dihub PubMed

Hinz U.G.: Isolation of the photosystem II reaction center complex from barley. Characterization by circular dichroism spectroscopy and amino acid sequencing. – Carlsberg Res. Commun. 50: 285-298, 1985. https://link.springer.com/article/10.1007/BF02907152 DOI

Horton P., Ruban A.: Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. – J. Exp. Bot. 56: 365-373, 2005. https://academic.oup.com/jxb/article/56/411/365/429873 PubMed

Jarvis P., Dörmann P., Peto C.A. et al.: Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. – P. Natl. Acad. Sci. USA 97: 8175-8179, 2000. https://www.pnas.org/doi/full/10.1073/pnas.100132197 PubMed DOI PMC

Joliot P., Joliot A.: Comparative study of the fluorescence yield and of the C550 absorption change at room temperature. – BBA-Bioenergetics 546: 93-105, 1979. https://www.sciencedirect.com/science/article/pii/0005272879901737?via%3Dihub PubMed

Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. – Photosynth. Res. 122: 121-158, 2014. https://link.springer.com/article/10.1007/s11120-014-0024-6 PubMed DOI PMC

Kansy M., Wilhelm C., Goss R.: Influence of thylakoid membrane lipids on the structure and function of the plant photosystem II core complex. – Planta 240: 781-796, 2014. https://link.springer.com/article/10.1007/s00425-014-2130-2 PubMed DOI

Kawakami K., Shen J.R.: Purification of fully active and crystallizable photosystem II from thermophilic cyanobacteria. – Method. Enzymol. 613: 1-16, 2018. https://www.sciencedirect.com/science/article/abs/pii/S0076687918304166?via%3Dihub PubMed

Koike H., Inoue Y.: Preparation of oxygen-evolving photosystem II particles from a thermophilic blue-green alga. – In: Inoue Y., Crofts A.R., Govindjee et al. (ed.): The Oxygen Evolving System of Photosynthesis. Pp. 257-263. Academic Press, Tokyo: 1983. https://www.sciencedirect.com/science/article/pii/B9780123723604500341?via%3Dihub

Krumova S.B., Laptenok S.P., Kovács L. et al.: Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. – Photosynth. Res. 105: 229-242, 2010. https://link.springer.com/article/10.1007/s11120-010-9581-5 PubMed DOI PMC

Kruse O., Hankamer B., Konczak C. et al.: Phosphatidylglycerol is involved in the dimerization of photosystem II. – J. Biol. Chem. 275: 6509-6514, 2000. https://www.sciencedirect.com/science/article/pii/S0021925818305131?via%3Dihub PubMed

Laisk A., Oja V.: Variable fluorescence of closed photochemical reaction centers. – Photosynth. Res. 143: 335-346, 2020. https://link.springer.com/article/10.1007/s11120-020-00712-3 PubMed DOI

Latowski D., Åkerlund H.E., Strzalka K.: Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. – Biochemistry-US 43: 4417-4420, 2004. https://pubs.acs.org/doi/10.1021/bi049652g PubMed DOI

Lavergne J., Matthews C., Ginet N.: Electron and proton transfer on the acceptor side of the reaction center in chromatophores of Rhodobacter capsulatus: Evidence for direct protonation of the semiquinone state of QB. – Biochemistry-US 38: 4542-4552, 1999. PubMed

Lavergne J., Trissl H.W.: 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, 1995. https://www.sciencedirect.com/science/article/pii/S0006349595804297?via%3Dihub PubMed PMC

Lazár D., Pospíšil P.: Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3',4'-dichlorophenyl)-1,1-dimethylurea-treated barley leaves at room and high temperatures. – Eur. Biophys. J. 28: 468-477, 1999. https://link.springer.com/article/10.1007/s002490050229 PubMed DOI

Lee A.G.: Membrane lipids: It's only a phase. – Curr. Biol. 10: R377-R380, 2000. https://www.sciencedirect.com/science/article/pii/S0960982200004772?via%3Dihub PubMed

Leng J., Sakurai I., Wada H., Shen J.-R.: Effects of phospholipase and lipase treatments on photosystem II core dimer from a thermophilic cyanobacterium. – Photosynth. Res. 98: 469-478, 2008. https://link.springer.com/article/10.1007/s11120-008-9335-9 PubMed DOI

Magyar M., Sipka G., Kovács L. et al.: Rate-limiting steps in the dark-to-light transition of Photosystem II – revealed by chlorophyll-a fluorescence induction. – Sci. Rep.-UK 8: 2755, 2018. https://www.nature.com/articles/s41598-018-21195-2 PubMed PMC

Miloslavina Y., Szczepaniak M., Müller M.G. et al.: Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. – Biochemistry-US 45: 2436-2442, 2006. https://pubs.acs.org/doi/10.1021/bi052248c PubMed DOI

Minoda A., Sonoike K., Okada K. et al.: Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. – FEBS Lett. 553: 109-112, 2003. https://febs.onlinelibrary.wiley.com/doi/abs/10.1016/S0014-5793%2803%2900981-5 PubMed DOI

Moise N., Moya I.: 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. – BBA-Bioenergetics 1657: 33-46, 2004. https://www.sciencedirect.com/science/article/pii/S0005272804000799?via%3Dihub PubMed

Nelson N., Ben-Shem A.: The complex architecture of oxygenic photosynthesis. – Nat. Rev. Mol. Cell Biol. 5: 971-982, 2004. https://www.nature.com/articles/nrm1525 PubMed

Neubauer C., Schreiber U.: 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. Naturforsch. C 42: 1246-1254, 1987. https://www.degruyter.com/document/doi/10.1515/znc-1987-11-1217/html DOI

Nuijs A.M., van Gorkom H.J., Plijter J.J., Duysens L.N.M.: Primary-charge separation and excitation of chlorophyll a in photosystem II particles from spinach as studied by picosecond absorbance-difference spectroscopy. – BBA-Bioenergetics 848: 167-175, 1986. https://www.sciencedirect.com/science/article/pii/0005272886900381?via%3Dihub

Oja V., Laisk A.: Time- and reduction-dependent rise of photosystem II fluorescence during microseconds-long inductions in leaves. – Photosynth. Res. 145: 209-225, 2020. https://link.springer.com/article/10.1007/s11120-020-00783-2 PubMed DOI

Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 818. Springer, Dordrecht: 2004. https://link.springer.com/book/10.1007/978-1-4020-3218-9 DOI

Papageorgiou G.C., Govindjee: Photosystem II fluorescence: Slow changes – Scaling from the past. – J. Photoch. Photobio. B 104: 258-270, 2011. https://www.sciencedirect.com/science/article/abs/pii/S1011134411000844?via%3Dihub PubMed

Prášil O., Kolber Z.S., Falkowski P.G.: Control of the maximal chlorophyll fluorescence yield by the QB binding site. – Photosynthetica 56: 150-162, 2018. https://ps.ueb.cas.cz/artkey/phs-201801-0013_control-of-the-maximal-chlorophyll-fluorescence-yield-by-the-qb-binding-site.php

Reifarth F., Christen G., Seeliger A.G. et al.: Modification of the water oxidizing complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol. – Biochemistry-US 36: 11769-11776, 1997. https://pubs.acs.org/doi/10.1021/bi9709654 PubMed DOI

Rutherford A.W.: Photosystem II, the water-splitting enzyme. – Trends Biochem. Sci. 14: 227-232, 1989. https://www.sciencedirect.com/science/article/abs/pii/0968000489900327?via%3Dihub PubMed

Sakurai I., Mizusawa N., Wada H. et al.: Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. – Plant Physiol. 145: 1361-1370, 2007. https://academic.oup.com/plphys/article/145/4/1361/6107243 PubMed PMC

Sakurai I., Shen J.R., Leng J. et al.: Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. – J. Biochem. 140: 201-209, 2006. https://academic.oup.com/jb/article-abstract/140/2/201/806078?redirectedFrom=fulltext PubMed

Schansker G., Tóth S.Z., Holzwarth A.R., Garab G.: Chlorophyll a fluorescence: Beyond the limits of the QA model. – Photosynth. Res. 120: 43-58, 2014. https://link.springer.com/article/10.1007/s11120-013-9806-5 PubMed DOI

Schansker G., Tóth S.Z., Kovács L. et al.: 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: 1032-1043, 2011. https://www.sciencedirect.com/science/article/pii/S000527281100140X?via%3Dihub PubMed

Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. – In: Schulze E.-D., Caldwell M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 49-70. Springer, Berlin-Heidelberg: 1995. https://link.springer.com/chapter/10.1007%2F978-3-642-79354-7_3

Sebban P., Wraight C.A.: Heterogeneity of the P+Q–A recombination kinetics in reaction centers from Rhodopseudomonas viridis: the effects of pH and temperature. – BBA-Bioenergetics 974: 54-65, 1989. https://www.sciencedirect.com/science/article/abs/pii/S0005272889801653?via%3Dihub

Shen J.R., Inoue Y.: Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. – Biochemistry-US 32: 1825-1832, 1993. https://pubs.acs.org/doi/abs/10.1021/bi00058a017 PubMed DOI

Shen J.R., Kamiya N.: Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. – Biochemistry-US 39: 14739-14744, 2000. https://pubs.acs.org/doi/10.1021/bi001402m PubMed DOI

Shen J.R., Kawakami K., Koike H.: Purification and crystallization of oxygen-evolving photosystem II core complex from thermophilic cyanobacteria. – In: Carpentier R. (ed.): Photosynthesis Research Protocols. Methods in Molecular Biology (Methods and Protocols). Vol. 684. Pp. 41-51. Humana Press, Totowa: 2011. https://link.springer.com/protocol/10.1007/978-1-60761-925-3_5 PubMed DOI

Shibata Y., Nishi S., Kawakami K. et al.: Photosystem II does not possess a simple excitation energy funnel: time-resolved fluorescence spectroscopy meets theory. – J. Am. Chem. Soc. 135: 6903-6914, 2013. https://pubs.acs.org/doi/10.1021/ja312586p PubMed DOI PMC

Shlyk-Kerner O., Samish I., Kaftan D. et al.: Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature. – Nature 442: 827-830, 2006. https://www.nature.com/articles/nature04947 PubMed

Siefermann D., Yamamoto H.Y.: Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts IV. The effects of electron-transport conditions on violaxanthin availability. – BBA-Bioenergetics 387: 149-158, 1975. https://www.sciencedirect.com/science/article/abs/pii/0005272875900596?via%3Dihub PubMed

Sipka G., Magyar M., Mezzetti A. et al.: Light-adapted charge-separated state of photosystem II: Structural and functional dynamics of the closed reaction center. – Plant Cell 33: 1286-1302, 2021. https://academic.oup.com/plcell/article-abstract/33/4/1286/6119330?redirectedFrom=fulltext PubMed PMC

Sipka G., Müller P., Brettel K. et al.: 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, 2019. https://onlinelibrary.wiley.com/doi/10.1111/ppl.12945 PubMed DOI

Sirohiwal A., Neese F., Pantazis D.A.: Chlorophyll excitation energies and structural stability of the CP47 antenna of photosystem II: a case study in the first-principles simulation of light-harvesting complexes. – Chem. Sci. 12: 4463-4476, 2021. https://pubs.rsc.org/en/content/articlelanding/2021/SC/D0SC06616H PubMed PMC

Stirbet A.: Excitonic connectivity between photosystem II units: what is it, and how to measure it? – Photosynth. Res. 116: 189-214, 2013. https://link.springer.com/article/10.1007/s11120-013-9863-9 PubMed DOI

Strasser R.J., Srivastava A., Govindjee: Polyphasic chlorophyll-a fluorescence transient in plants and cyanobacteria. – Photochem. Photobiol. 61: 32-42, 1995. https://onlinelibrary.wiley.com/doi/10.1111/j.1751-1097.1995.tb09240.x DOI

Szczepaniak M., Sander J., Nowaczyk M. et al.: Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction center. – Biophys. J. 96: 621-631, 2009. https://www.cell.com/biophysj/fulltext/S0006-3495(08)00044-1 PubMed PMC

Tang D.M., Jankowiak R., Seibert M., Small G.J.: Effects of detergent on the excited-state structure and relaxation dynamics of the photosystem II reaction center: A high-resolution hole burning study. – Photosynth. Res. 27: 19-29, 1991. https://link.springer.com/article/10.1007/BF00029973 PubMed DOI

Tiede D.M., Vázquez J., Córdova J., Marone P.A.: Time-resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. – Biochemistry-US 35: 10763-10775, 1996. https://pubs.acs.org/doi/10.1021/bi9605907 PubMed DOI

Tóth S.Z., Schansker G., Strasser R.J.: A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. – Photosynth Res 93: 193-203, 2007. https://link.springer.com/article/10.1007/s11120-007-9179-8 PubMed DOI

Umena Y., Kawakami K., Shen J.R. et al.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. – Nature 473: 55-60, 2011. https://www.nature.com/articles/nature09913 PubMed

Valkunas L., Geacintov N.E., France L., Breton J.: The dependence of the shapes of fluorescence induction curves in chloroplasts on the duration of illumination pulses. – Biophys. J. 59: 397-408, 1991. https://www.cell.com/biophysj/pdf/S0006-3495(91)82233-0.pdf PubMed PMC

van der Weij-de Wit C.D., Dekker J.P., van Grondelle R., van Stokkum I.H.M.: Charge separation is virtually irreversible in photosystem II core complexes with oxidized primary quinone acceptor. – J. Phys. Chem. A 115: 3947-3956, 2011. 10.1021/jp1083746 PubMed DOI

Vredenberg W.J.: 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, 2008. https://link.springer.com/article/10.1007/s11120-007-9287-5 PubMed DOI

Vredenberg W.: A simple routine for quantitative analysis of light and dark kinetics of photochemical and non-photochemical quenching of chlorophyll fluorescence in intact leaves. – Photosynth. Res. 124: 87-106, 2015. https://link.springer.com/article/10.1007/s11120-015-0097-x PubMed DOI PMC

Vredenberg W., Prasil O.: On the polyphasic quenching kinetics of chlorophyll a fluorescence in algae after light pulses of variable length. – Photosynth. Res. 117: 321-337, 2013. https://link.springer.com/article/10.1007/s11120-013-9917-z PubMed DOI

Yamamoto H.Y., Higashi R.M.: Violaxanthin de-epoxidase: Lipid composition and substrate specificity. – Arch. Biochem. Biophys. 190: 514-522, 1978. https://www.sciencedirect.com/science/article/abs/pii/0003986178903053?via%3Dihub PubMed