Rate-limiting steps in the dark-to-light transition of Photosystem II - revealed by chlorophyll-a fluorescence induction
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29426901
PubMed Central
PMC5807364
DOI
10.1038/s41598-018-21195-2
PII: 10.1038/s41598-018-21195-2
Knihovny.cz E-zdroje
- MeSH
- chlorofyl a metabolismus MeSH
- fluorescence * MeSH
- fotosyntéza MeSH
- fotosystém II - proteinový komplex antagonisté a inhibitory metabolismus MeSH
- Spinacia oleracea metabolismus MeSH
- Synechococcus metabolismus MeSH
- Synechocystis metabolismus MeSH
- teplota MeSH
- tylakoidy metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chlorofyl a MeSH
- fotosystém II - proteinový komplex MeSH
Photosystem II (PSII) catalyses the photoinduced oxygen evolution and, by producing reducing equivalents drives, in concert with PSI, the conversion of carbon dioxide to sugars. Our knowledge about the architecture of the reaction centre (RC) complex and the mechanisms of charge separation and stabilisation is well advanced. However, our understanding of the processes associated with the functioning of RC is incomplete: the photochemical activity of PSII is routinely monitored by chlorophyll-a fluorescence induction but the presently available data are not free of controversy. In this work, we examined the nature of gradual fluorescence rise of PSII elicited by trains of single-turnover saturating flashes (STSFs) in the presence of a PSII inhibitor, permitting only one stable charge separation. We show that a substantial part of the fluorescence rise originates from light-induced processes that occur after the stabilisation of charge separation, induced by the first STSF; the temperature-dependent relaxation characteristics suggest the involvement of conformational changes in the additional rise. In experiments using double flashes with variable waiting times (∆τ) between them, we found that no rise could be induced with zero or short ∆τ, the value of which depended on the temperature - revealing a previously unknown rate-limiting step in PSII.
Global Change Research Institute Czech Academy of Sciences Bělidla 986 4a 603 00 Brno Czech Republic
Zobrazit více v PubMed
Umena Y, Kawakami K, Shen JR, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature. 2011;473:55–U65. doi: 10.1038/nature09913. PubMed DOI
Cardona T, Sedoud A, Cox N, Rutherford AW. Charge separation in photosystem II: A comparative and evolutionary overview. Biochim Biophys Acta-Bioenergetics. 2012;1817:26–43. doi: 10.1016/j.bbabio.2011.07.012. PubMed DOI
Vinyard DJ, Ananyev GM, Dismukes GC. Photosystem II: The reaction center of oxygenic photosynthesis. Annu Rev Biochem. 2013;82:577–606. doi: 10.1146/annurev-biochem-070511-100425. PubMed DOI
Romero E, Novoderezhkin VI, van Grondelle R. Quantum design of photosynthesis for bio-inspired solar-energy conversion. Nature. 2017;543:355–365. doi: 10.1038/nature22012. PubMed DOI
Suga M, et al. Light-induced structural changes and the site of O = O bond formation in PSII caught by XFEL. Nature. 2017;543:131–135. doi: 10.1038/nature21400. PubMed DOI
Genty B, Briantais JM, Baker NR. The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta. 1989;990:87–92. doi: 10.1016/S0304-4165(89)80016-9. 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. Biochim Biophys Acta-Bioenergetics. 2004;1657:33–46. doi: 10.1016/j.bbabio.2004.04.001. PubMed DOI
Schansker G, Toth SZ, Kovacs L, Holzwarth AR, Garab G. 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-Bioenergetics. 2011;1807:1032–1043. doi: 10.1016/j.bbabio.2011.05.022. PubMed DOI
Duysens, L. M. N. & Sweers, H. E. In Studies on Microalgae and Photosynthetic Bacteria 353–372 (Japanese Society of Plant Physiologists, University of Tokyo Press, 1963).
Stirbet AG. Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res. 2012;113:15–61. doi: 10.1007/s11120-012-9754-5. PubMed DOI
Joliot P, Joliot A. Comparative-study of the fluorescence yield and of the C550 absorption change at room-temperature. Biochim Biophys Acta. 1979;546:93–105. doi: 10.1016/0005-2728(79)90173-7. 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. 2015;124:87–106. doi: 10.1007/s11120-015-0097-x. PubMed DOI PMC
Delosme R. Study of the induction of fluorescence in green algae and chloroplasts at the onset of an intense illumination. Biochim Biophys Acta. 1967;143:108–128. doi: 10.1016/0005-2728(67)90115-6. PubMed DOI
Papageorgiou, G. C. & Govindjee. Chlorophyll a Fluorescence: A Signature of Photosynthesis. (Springer, 2004).
Strasser, R. J., Tsimilli-Michael, M. & Srivastava, A. Analysis of the chlorophyll a fluorescence transient in Chlorophyll a Fluorescence: A Signature of Photosynthesis (eds G.C. Papageorgiou & Govindjee) 463–495 (Springer, 2004).
Kalaji HM, et al. Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res. 2014;122:121–158. doi: 10.1007/s11120-014-0024-6. PubMed DOI PMC
Stirbet A, Riznichenko GY, Rubin AB. & Govindjee. Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry. Biokhimiia. 2014;79:291–323. doi: 10.1134/S0006297914040014. PubMed DOI
Joliot P, Joliot A. A photosystem II electron-acceptor which is not a plastoquinone. Febs Lett. 1981;134:155–158. doi: 10.1016/0014-5793(81)80590-X. DOI
Valkunas L, Geacintov NE, France L, Breton J. The dependence of the shapes of fluorescence induction curves in chloroplasts on the duration of illumination pulses. Biophys J. 1991;59:397–408. doi: 10.1016/S0006-3495(91)82233-0. PubMed DOI PMC
France LL, Geacintov NE, 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. Biochim Biophys Acta. 1992;1101:105–119. doi: 10.1016/0167-4838(92)90474-R. DOI
Joliot, A. & Joliot, P. Étude cinétique de la réaction photochimique libérant l’oxygéne au cours de la photosynthése. CR Acad Sci Paris258, 4622–4625 (in French) (1964). PubMed
Stirbet A. Excitonic connectivity between photosystem II units: what is it, and how to measure it? Photosynth Res. 2013;116:189–214. doi: 10.1007/s11120-013-9863-9. PubMed DOI
Vredenberg WJ. 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. 2008;96:83–97. doi: 10.1007/s11120-007-9287-5. PubMed DOI
Govindjee KH, Inoue Y. Thermo-luminescence and oxygen evolution from a thermophilic blue-green-alga obtained after single-turnover light-flashes. Photochem Photobiol. 1985;42:579–585. doi: 10.1111/j.1751-1097.1985.tb01613.x. DOI
Ajlani G, Vernotte C. Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol. 1998;37:577–580. doi: 10.1023/A:1005924730298. PubMed DOI
Caffarri S, Tibiletti T, Jennings RC, Santabarbara S. A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sc. 2014;15:296–331. doi: 10.2174/1389203715666140327102218. PubMed DOI PMC
Shevela D, Eaton-Rye JJ, Shen JR. & Govindjee. Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta. 2012;1817:1134–1151. doi: 10.1016/j.bbabio.2012.04.003. PubMed DOI
Muh F, Zouni A. The nonheme iron in photosystem II. Photosynth Res. 2013;116:295–314. doi: 10.1007/s11120-013-9926-y. PubMed DOI
Brettel K, Setif P, Mathis P. Flash-induced absorption changes in photosystem-I at low-temperature - evidence that the electron acceptor-A1 is vitamin-K1. Febs Lett. 1986;203:220–224. doi: 10.1016/0014-5793(86)80746-3. DOI
Ikegami I, Katoh S. Studies on chlorophyll fluorescence in chloroplasts II. Effect of ferricyanide on the induction of fluorescence in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylure. Plant Cell Physiol. 1973;14:829–836.
Guskov A, et al. Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009;16:334–342. doi: 10.1038/nsmb.1559. PubMed DOI
Muh F, Glockner C, Hellmich J, Zouni A. Light-induced quinone reduction in photosystem II. Biochim Biophys Acta-Bioenergetics. 2012;1817:44–65. doi: 10.1016/j.bbabio.2011.05.021. PubMed DOI
Lazar D, Ilik P, Kruk J, Strzalka K, Naus J. A theoretical study on effect of the initial redox state of cytochrome b(559) on maximal chlorophyll fluorescence level (F-M) implications for photoinhibition of photosystem II. J Theor Biol. 2005;233:287–300. doi: 10.1016/j.jtbi.2004.10.015. PubMed DOI
Samson G, Bruce D. Origins of the low yield of chlorophyll a fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta-Bioenergetics. 1996;1276:147–153. doi: 10.1016/0005-2728(96)00072-2. DOI
Barabas K, Garab G. 2 Populations of the high-potential form of cytochrome-B-559 in chloroplasts treated with 2-(3-Chloro-4-Trifluoromethyl)Anilino-3,5-Dinitrothiophene (Ant 2p) Febs Lett. 1989;248:62–66. doi: 10.1016/0014-5793(89)80432-6. DOI
Vredenberg W. Kinetic analyses and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. Biosystems. 2011;103:138–151. doi: 10.1016/j.biosystems.2010.10.016. PubMed DOI
Chylla RA, Garab G, Whitmarsh J. Evidence for slow turnover in a fraction of photosystem II complexes in thylakoid membranes. Biochim Biophys Acta. 1987;894:562–571. doi: 10.1016/0005-2728(87)90136-8. DOI
Schlodder E, Cetin M, Lendzian F. Temperature dependence of the oxidation kinetics of Tyr(Z) and Tyr(D) in oxygen-evolving photosystem II complexes throughout the range from 320 K to 5 K. Biochim Biophys Acta-Bioenergetics. 2015;1847:1283–1296. doi: 10.1016/j.bbabio.2015.07.005. PubMed DOI
Shinkarev VPG. Insight into the relationship of chlorophyll a fluorescence yield to the concentration of its natural quenchers in oxygenic photosynthesis. Proceedings of the National Academy of Sciences of the United States of America. 1993;90:7466–7469. doi: 10.1073/pnas.90.16.7466. PubMed DOI PMC
Schreiber, U. Assessment of maximal fluorescence yield: donor-side dependent quenching and QB quenching. In Plant spectrophotometry: applications and basic research (eds O van Kooten & JFH Snel) 23–47 (Rozenberg Publishers, 2002).
Lelkes PI, Miller IR. Perturbations of membrane structure by optical probes: I. Location and structural sensitivity of merocyanine 540 bound to phospholipid membranes. The Journal of membrane biology. 1980;52:1–15. doi: 10.1007/BF01869001. PubMed DOI
Connolly JS, Samuel EB, Janzen AF. Effects of solvent on the fluorescence properties of bacteriochlorophyll a. Photochem Photobiol. 1982;36:565–574. doi: 10.1111/j.1751-1097.1982.tb04417.x. DOI
Ilioaia C, Johnson MP, Horton P, Ruban AV. Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J Biol Chem. 2008;283:29505–29512. doi: 10.1074/jbc.M802438200. PubMed DOI PMC
Akhtar P, et al. Pigment Interactions in light-harvesting complex II in different molecular environments. J Biol Chem. 2015;290:4877–4886. doi: 10.1074/jbc.M114.607770. PubMed DOI PMC
Antal TK, Osipov V, Matorin DN, Rubin AB. Membrane potential is involved in regulation of photosynthetic reactions in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B: Biology. 2011;102:169–173. doi: 10.1016/j.jphotobiol.2010.11.005. PubMed DOI
Zimanyi L, Garab G. Configuration of the electric-field and distribution of ions in energy transducing biological-membranes - model-calculations in a vesicle containing discrete charges. J Theor Biol. 1989;138:59–76. doi: 10.1016/S0022-5193(89)80178-X. DOI
Malferrari M, Mezzetti A, Francia F, Venturoli G. Effects of dehydration on light-induced conformational changes in bacterial photosynthetic reaction centers probed by optical and differential FTIR spectroscopy. Biochim Biophys Acta-Bioenergetics. 2013;1827:328–339. doi: 10.1016/j.bbabio.2012.10.009. PubMed DOI
Panagopoulou A, Kyritsis A, Shinyashiki N, Pissis P. Protein and water dynamics in bovine serum albumin-water mixtures over wide ranges of composition. J Phys Chem B. 2012;116:4593–4602. doi: 10.1021/jp2105727. PubMed DOI
Bhaduri S, et al. Pathways of Transmembrane Electron Transfer in Cytochrome bc Complexes: Dielectric Heterogeneity and Interheme Coulombic Interactions. J Phys Chem B. 2017;121:975–983. doi: 10.1021/acs.jpcb.6b11709. PubMed DOI
Garab G. Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta-Bioenergetics. 2014;1837:481–494. doi: 10.1016/j.bbabio.2013.12.003. PubMed DOI
Goushcha AO, Kharkyanen VN, Scott GW, Holzwarth AR. Self-regulation phenomena in bacterial reaction centers. I. General theory. Biophys J. 2000;79:1237–1252. doi: 10.1016/S0006-3495(00)76378-8. PubMed DOI PMC
Garbers A, Reifarth F, Kurreck J, Renger G, Parak F. Correlation between protein flexibility and electron transfer from QA−* to QB in PSII membrane fragments from spinach. Biochemistry. 1998;37:11399–11404. doi: 10.1021/bi980296+. PubMed DOI
Shlyk-Kerner O, et al. Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature. Nature. 2006;442:827–830. doi: 10.1038/nature04947. PubMed DOI
Pieper J, Renger G. Protein dynamics investigated by neutron scattering. Photosynth Res. 2009;102:281–293. doi: 10.1007/s11120-009-9480-9. PubMed DOI
Shen JR, Inoue Y. Binding and functional-properties of two new extrinsic components, cytochrome c-550 and a 12-kDa Protein, in cyanobacterial photosystem II. Biochemistry. 1993;32:1825–1832. doi: 10.1021/bi00058a017. PubMed DOI
Shen JR, Kamiya N. Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry. 2000;39:14739–14744. doi: 10.1021/bi001402m. PubMed DOI
Insights on the regulation of photosynthesis in pea leaves exposed to oscillating light
Light quality, oxygenic photosynthesis and more
Photosynthesis dynamics and regulation sensed in the frequency domain
Photosynthesis: basics, history and modelling
Effects of selenate and red Se-nanoparticles on the photosynthetic apparatus of Nicotiana tabacum