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Primary charge separation in Photosystem II

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Abstract

In this Minireview, we discuss a number of issues on the primary photosynthetic reactions of the green plant Photosystem II. We discuss the origin of the 683 and 679 nm absorption bands of the PS II RC complex and suggest that these forms may reflect the single-site spectrum with dominant contributions from the zero-phonon line and a pronounced ∼80 cm−1 phonon side band, respectively. The couplings between the six central RC chlorins are probably very similar and, therefore, a `multimer' model arises in which there is no `special pair' and in which for each realization of the disorder the excitation may be dynamically localized on basically any combination of neighbouring chlorins. The key features of our model for the primary reactions in PS II include ultrafast (<500 fs) energy transfer processes within the multimer, `slow' (∼20 ps) energy transfer processes from peripheral RC chlorophylls to the RC multimer, ultrafast charge separation (<500 fs) with a low yield starting from the singlet-excited `accessory' chlorophyll of the active branch, cation transfer from this `accessory' chlorophyll to a `special pair' chlorophyll and/or charge separation starting from this `special pair' chlorophyll (∼8 ps), and slow relaxation (∼50 ps) of the radical pair by conformational changes of the protein. The charge separation in the PS II RC can probably not be described as a simple trap-limited or diffusion-limited process, while for the PS II core and larger complexes the transfer of the excitation energy to the PS II RC may be rate limiting.

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References

  • Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66

    Article  PubMed  CAS  Google Scholar 

  • Bassi R, Sandonà D and Croce R (1997) Novel aspects of chlorophyll a/b proteins. Physiol Plant 100: 769–779

    Article  CAS  Google Scholar 

  • Beekman LMP, Van Mourik F, Jones MR, Visser HM, Hunter CN and Van Grondelle R (1994) Trapping kinetics in mutants of the photosynthetic purple bacterium Rhodobacter sphaeroides: Influence of the charge separation rate and consequences for the rate-limiting step in the light-harvesting process. Biochemistry 33: 3143–3147

    Article  PubMed  CAS  Google Scholar 

  • Blomberg MRA, Siegbahn PER and Babcock GT (1998) Modeling electron transfer in biochemistry: A quantum chemical study of charge separation in Rhodobacter sphaeroides and Photosystem II. J Am Chem Soc 120: 8812–8824

    Article  CAS  Google Scholar 

  • Boekema EJ, Van Roon H, Calkoen F, Bassi R and Dekker JP (1999a) Multiple types of association of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Biochemistry 38: 2233–2239

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, Van Roon H, Van Breemen JFL and Dekker JP (1999b) Supramolecular organization of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Eur J Biochem 266: 444–452

    Article  PubMed  CAS  Google Scholar 

  • Bosch MK, Proskuryakov II, Gast P and Hoff AJ (1995) Relative orientation of the optical transition dipole and triplet axes of the Photosystem II primary donor. A magnetophoto-selection study. J Phys Chem 99: 15310–15316

    Article  CAS  Google Scholar 

  • Braun P, Greenberg BM and Scherz A (1990) D1-D2-cytochrome b-559 complex from the aquatic plant Spirodela oligorrhiza: Correlation between complex integrity, spectroscopic properties, photochemical activity and pigment composition. Biochemistry 29: 10376–10387

    Article  PubMed  CAS  Google Scholar 

  • Chang H-C, Jankowiak R, Yocum CF, Picorel R, Alfonso M, Seibert M and Small GJ (1994a) Excition level structure and dynamics in the CP47 antenna complex of Photosystem II. J Phys Chem 98: 7717–7724

    Article  CAS  Google Scholar 

  • Chang H-C, Jankowiak R, Reddy NRS, Yocum CF, Picorel R, Seibert M and Small GJ (1994b) On the question of the chlorophyll a content of the Photosystem II reaction center. J Phys Chem 98: 7725–7735

    Article  CAS  Google Scholar 

  • Dekker JP, Van Roon H and Boekema EJ (1999) Heptameric association of light-harvesting complex II trimers in partially solubilized Photosystem II membranes. FEBS Letters 449: 211–214

    Article  PubMed  CAS  Google Scholar 

  • Den Hartog FTH, Vacha F, Lock AJ, Barber J, Dekker JP and Völker S (1998a) Comparison of the excited-state dynamics of five-and six-chlorophyll Photosystem II reaction center complexes. J Phys Chem B 102: 9174–9180

    Article  CAS  Google Scholar 

  • Diner BA and Babcock GT (1996) Structure, dynamics, and energy conversion efficiency in Photosystem II. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis. The Light Reactions, pp 213–247. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Donovan B, Walker LA II, Kaplan D, Bouvier M, Yocum CF and Sension RJ (1997) Structure and function in the isolated reaction center complex of Photosystem II. 1. Ultrafast fluorescence measurements of PS II. J Phys Chem B 101: 5232–5238

    Article  CAS  Google Scholar 

  • Durrant JR, Hastings G, Joseph DM, Barber J, Porter G and Klug DR (1992) Subpicosecond equilibration of excitation energy in isolated Photosystem II reaction centers. Proc Natl Acad Sci USA 89: 11632–11636

    Article  PubMed  CAS  Google Scholar 

  • Durrant JR, Klug DR, Kwa SLS, Van Grondelle R, Porter G and Dekker JP (1995) A multimer model for P680, the primary electron donor of Photosystem II. Proc Natl Acad Sci USA 92: 4798–4802

    Article  PubMed  CAS  Google Scholar 

  • Eijckelhoff C, Van Roon H, Groot M-L, Van Grondelle R and Dekker JP (1996) Purification and spectroscopic characterization of Photosystem II reaction center complexes isolated with or without Triton X-100. Biochemistry 35: 12864–12872

    Article  PubMed  CAS  Google Scholar 

  • Eijckelhoff C, Vacha F, Van Grondelle R, Dekker JP and Barber J (1997a) Spectroscopic characterization of a 5 Chl a Photosystem II reaction center complex. Biochim Biophys Acta 1318: 266–274

    Article  CAS  Google Scholar 

  • Eijckelhoff C, Dekker JP and Boekema EJ (1997b) Characterization by electron microscopy of dimeric Photosystem II core complexes from spinach with and without CP43. Biochim Biophys Acta 1321: 10–20

    Article  CAS  Google Scholar 

  • Fleming GR, Martin JL and Breton J (1988) Rates of primary electron transfer in photosynthetic reaction centers and their mechanistic implications. Nature 333: 190–192

    Article  CAS  Google Scholar 

  • Friesner RA and Won Y (1989) Spectroscopy and electron transfer dynamics of the bacterial photosynthetic reaction center. Biochim Biophys Acta 977: 99–122

    PubMed  CAS  Google Scholar 

  • Greenfield SR, Seibert M, Govindjee and Wasielewski MR (1997) Direct measurement of the effective rate constant for primary charge separation in isolated Photosystem II reaction centers. J Phys Chem B 101: 2251–2255

    Article  CAS  Google Scholar 

  • Greenfield SR, Seibert M and Wasielewski MR (1999) Time-resolved absorption changes of the pheophytin Qx band in isolated Photosystem II reaction centers at 7 K: Energy transfer and charge separation. J Phys Chem B 103: 8364–8374

    Article  CAS  Google Scholar 

  • Groot M-L, Peterman EJG, Van Kan PJM, Van Stokkum IHM, Dekker JP and Van Grondelle R (1994) Temperature dependent triplet and fluorescence quantum yields of the Photosystem II reaction center described in a thermodynamic model. Biophys J 67: 318–330

    PubMed  CAS  Google Scholar 

  • Groot M-L, Dekker JP, Van Grondelle R, Den Hartog FTH and Völker S (1996) Energy transfer and trapping in isolated Photosystem II reaction centers of green plants at low temperature. A study by spectral hole-burning. J Phys Chem 100: 11488–11495

    Article  CAS  Google Scholar 

  • Groot M-L, Van Mourik F, Eijckelhoff C, Van Stokkum IHM, Dekker JP and Van Grondelle R (1997) Charge separation in the reaction center of Photosystem II studied as function of temperature. Proc Natl Acad Sci USA 94: 4389–4394

    Article  PubMed  CAS  Google Scholar 

  • Groot M-L, Frese RN, de Weerd FL, Bromek K, Pettersson Å, Peterman EJG, Van Stokkum IHM, Van Grondelle R and Dekker JP (1999) Spectroscopic properties of the CP43 core antenna protein of Photosystem II. Biophys J 77: 3328–3340

    Article  PubMed  CAS  Google Scholar 

  • Gudowska-Nowak E, Newton MD and Fajer J (1990) Conformational and environmental effects on bacteriochlorophyll optical spectra: Correlations of calculated spectra with structural results. J Phys Chem 94: 5795–5801

    Article  CAS  Google Scholar 

  • Hankamer B, Barber J and Boekema EJ (1997) Structure and membrane organization of Photosystem II from green plants. Ann Rev Plant Phys Plant Mol Biol 48: 641–672

    Article  CAS  Google Scholar 

  • Hankamer B, Morris EP and Barber J (1999) Revealing the structure of the oxygen-evolving core dimer of Photosystem II by cryoelectron crystallography. Nature Struct Biol 6: 560–564

    Article  PubMed  CAS  Google Scholar 

  • Harrer R, Bassi R, Testi MG and Schäfer C (1998) Nearestneighbour analysis of a Photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction centre and antenna proteins. Eur J Biochem 255: 196–205

    Article  PubMed  CAS  Google Scholar 

  • Hillmann B, Brettel K, Van Mieghem F, Kamlowski A, Rutherford AW and Schlodder E (1995) Charge recombination reactions in Photosystem II. 2. Transient absorbance difference spectra and their temperature dependence. Biochemistry 34: 4814–4827

    Article  PubMed  CAS  Google Scholar 

  • Hoff AJ (1988) Bacterial reaction centers are intrinsically heterogeneous. In: Breton J and Verméglio A (eds) The Photosynthetic Bacterial Reaction Center, Structure and Dynamics, pp. 89–97. Plenum Press, New York

    Google Scholar 

  • Jankowiak R, Rãtsep M, Picorel R, Seibert M and Small GJ (1999) Excited states of the 5-chlorophyll Photosystem II reaction center. J Phys Chem B 103: 9759–9769

    Article  CAS  Google Scholar 

  • Jennings RC, Bassi R, Garlaschi FM, Dainese P and Zucchelli G (1993) Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of Photosystem II antenna. Biochemistry 32: 3203–3210

    Article  PubMed  CAS  Google Scholar 

  • Kamlowski A, Frankemüller L, Van der Est A, Stehlik D and Holzwarth AR (1996) Evidence for delocalization of the triplet state 3P680 in the D1D2cytb559-complex of Photosystem II. Ber Bunsenges Phys Chem 100: 2045–2051

    CAS  Google Scholar 

  • Klug DR, Durrant JR and Barber J (1998) The entanglement of excitation energy transfer and electron transfer in the reaction centre of Photosystem II. Phil Trans R Soc 356: 449–464

    Article  CAS  Google Scholar 

  • Konermann L and Holzwarth AR (1996) Analysis of the absorption spectrum of Photosystem II reaction centers: Temperature dependence, pigment assignment and inhomogeneous broadening. Biochemistry 35: 829–842

    Article  PubMed  CAS  Google Scholar 

  • Konermann L, Gatzen G and Holzwarth AR (1997a) Primary processes and structure of the Photosystem II reaction center. 5. Modeling of the fluorescence kinetics of the D1-D2-cyt-b559 complex at 77 K. J Phys Chem B 101: 2933–2944

    Article  CAS  Google Scholar 

  • Konermann L, Yruela I and Holzwarth AR (1997b) Pigment assignment in the absorption spectrum of the Photosystem II reaction center by site-selected fluorescence spectroscopy. Biochemistry 36: 7498–7502

    Article  PubMed  CAS  Google Scholar 

  • Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621

    Article  PubMed  Google Scholar 

  • Kwa SLS (1993) Plant solar cells under illumination. A spectroscopic investigation of Photosystem II. Doctoral Thesis, Vrije Universiteit Amsterdam

  • Kwa SLS, Eijckelhoff C, Van Grondelle R and Dekker JP (1994) Site-selection spectroscopy of the reaction center complex of Photosystem II. I. Triplet-minus-singlet absorption difference: A search for a second excition band of P-680. J Phys Chem 98: 7702–7711

    Article  CAS  Google Scholar 

  • Leegwater JA, Durrant JR and Klug DR (1997) Exciton equilibration induced by phonons: Theory and application to PS II reaction centers. J Phys Chem B 101: 7205–7210

    Article  CAS  Google Scholar 

  • Louwe RJW, Vrieze J, Hoff AJ and Aartsma TJ (1997) Towards an integral interpretation of the optical steady-state spectra of the FMO-complex of Prosthecochloris aestuarii. 2. Exciton simulations. J Phys Chem B 101: 11280–11287

    Article  CAS  Google Scholar 

  • Merry SAP, Kumazaki S, Tachibana Y, Joseph DM, Porter G, Yoshihara K, Barber J, Durrant JR and Klug DR (1996) Subpicosecond equilibration of excitation energy in isolated Photosystem II reaction center revisited: Time-dependent anisotropy. J Phys Chem 100: 10469–10478

    Article  CAS  Google Scholar 

  • Merry SAP, Nixon PJ, Barter LMC, Schilstra M, Porter G, Barber J, Durrant JR and Klug DR (1998) Modulation of quantum yield of primary radical pair formation in Photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37: 17439–17447

    Article  PubMed  CAS  Google Scholar 

  • Mulkidjanian AY (1999) Photosystem II of green plants: On the possible role of retarded protonic relaxation in water oxidation. Biochim Biophys Acta 1410: 1–6

    Article  PubMed  CAS  Google Scholar 

  • Müller MG, Hucke M, Reus M and Holzwarth AR (1996) Primary processes and structure of the Photosystem II reaction center. 4. Low-intensity femtosecond transient absorption spectra of D1-D2-cyt-b559 reaction centers. J Phys Chem 100: 9527–9536

    Article  Google Scholar 

  • Noguchi T, Inoue Y and Satoh K (1993) FTIR studies on the triplet state of P680 in the Photosystem II reaction center: Triplet equilibrium within a chlorophyll dimer. Biochemistry 32: 7186–7195

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Tomo T and Inoue Y (1998) Fourier transform infrared study of the cation radical of P680 in the Photosystem II reaction center: Evidence for charge delocalization on the chlorophyll dimer. Biochemistry 37: 13614–13625

    Article  PubMed  CAS  Google Scholar 

  • Nuijs AM, Van Gorkom HJ, Plijter JJ and Duysens LNM (1986) Primary charge separation and excitation of chlorophyll a in Photosystem II particles from spinach as studied by picosecond absorbance difference spectroscopy. Biochim Biophys Acta 848: 167–175

    Article  CAS  Google Scholar 

  • Peterman EJG, Van Amerongen H, Van Grondelle R and Dekker JP (1998) The nature of the excited state of the reaction center of Photosystem II of green plants. A high-resolution fluorescence spectroscopy study. Proc Natl Acad Sci USA 95: 6128–6133

    Article  PubMed  CAS  Google Scholar 

  • Rech T, Durrant JR, Joseph MD, Barber J, Porter G and Klug DR (1994) Does slow energy transfer limit the observed time constant for radial pair formation in photosystem II reaction centers? Biochemistry 33: 14768–14774

    Article  PubMed  CAS  Google Scholar 

  • Rhee K-H, Morris EP, Barber J and Kühlbrandt W (1998) Three-dimensional structure of the plant Photosystem II reaction centre at 8 Å resolution. Nature 396: 283–286

    Article  PubMed  CAS  Google Scholar 

  • Roelofs TA, Kwa SLS, Van Grondelle R, Dekker JP and Holzwarth AR (1993) Primary processes and structure of the Photosystem II reaction center. II. Low temperature picosecond fluorescence kinetics of a D1-D2-Cytochrome b-559 reaction center complex isolated by short Triton-exposure. Biochim Biophys Acta 1143: 147–157

    Article  CAS  Google Scholar 

  • Satoh K (1996) Introduction to the Photosystem II reaction center — isolation and biochemical and biophysical characterization. In Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 193–211. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Schatz GH, Brock H and Holzwarth AR (1988) A kinetic and energetic model for the primary processes in Photosystem II. Biophys J 54: 397–405

    CAS  Google Scholar 

  • Schelvis JPM, Van Noort PI, Aartsma TJ and Van Gorkom IIJ (1994) Energy transfer, charge separation and pigment arrangement in the reaction center of Photosystem II. Biochim Biophys Acta 1184: 242–250

    Article  CAS  Google Scholar 

  • Schilstra MJ, Nield J, Dörner W, Hankamer B, Carradus M, Barter LMC, Barber J and Klug DR (1999) Similarity between electron donor side reactions in the solubilized Photosystem II-LHC II supercomplex and Photosystem II-containing membranes. Photosynth Res 60: 191–198

    Article  CAS  Google Scholar 

  • Seibert M (1993) Biochemical, biophysical, and structural characterization of the isolated Photosystem II reaction center complex. In: Deisenhofer J and Norris JR (eds) The Photosynthetic Reaction Center, Vol I, pp 319–356. Academic Press, New York

    Google Scholar 

  • Shkuropatov AY, Khatypov RA, Volshchukova TS, Shkuropatova VA, Owens TG and Shuvalov VA (1997) Spectral and photochemical properties of borohydride-treated D1–D2-cytochrome b-559 complex of Photosystem II. FEBS Lett 420: 171–174

    Article  PubMed  CAS  Google Scholar 

  • Tetenkin VL, Gulyaev BA, Seibert M and Rubin AB (1989) Spectral properties of stabilized D1/D2/cytochrome b-559 Photosystem II reaction center complex. FEBS Lett 250: 459–463

    Article  CAS  Google Scholar 

  • Vacha F, Joseph DM, Durrant JR, Telfer A, Klug DR, Porter G and Barber J (1995) Photochemistry and spectroscopy of a five-chlorophyll reaction center of Photosystem II isolated by using a Cu affinity column. Proc Natl Acad Sci USA 92: 2929–2933

    Article  PubMed  CAS  Google Scholar 

  • Valkunas L, Liuolia V, Dekker JP and Van Grondelle R (1995) Description of energy migration and trapping in Photosystem I. The application of a model with two scaling parameters. Photosynth Res 43: 149–154

    Article  CAS  Google Scholar 

  • Van Amerongen H, Valkunas L and Van Grondelle R (2000) Photosynthetic Excitons. World Scientific, Singapore

    Google Scholar 

  • Van Brederode ME and Van Grondelle R (1999) New and unexpected pathways for ultrafast electron transfer in photosynthetic reaction centers. FEBS Lett 455: 1–7

    Article  PubMed  CAS  Google Scholar 

  • Van Brederode ME, Jones MR, Van Mourik F, Van Stokkum IHM and Van Grondelle R (1997) A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacter sphaeroides not involving the excited special pair. Biochemistry 36: 6855–6861

    Article  PubMed  CAS  Google Scholar 

  • Van Brederode ME, Van Mourik F, Van Stokkum IHM, Jones MR and Van Grondelle R (1999) Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 96: 2054–2059

    Article  PubMed  CAS  Google Scholar 

  • Van der Vos R, Van Leeuwen PJ, Braun P and Hoff AJ (1992) Analysis of the optical absorbance spectra of D1–D2-cytochrome b-559 complexes by absorbance-detected magnetic resonance, Structural properties of P680. Biochim. Biophys. Acta 1140: 184–198

    Article  CAS  Google Scholar 

  • Van Gorkom (1985) Electron transfer in Photosystem II. Photosynth Res 6: 97–112

    Article  CAS  Google Scholar 

  • Van Grondelle (1985) Excitation energy transfer, trapping and annihilation in photosynthetic systems. Biochim Biophys Acta 811: 147–195

    Google Scholar 

  • Van Grondelle R, Dekker JP, Gillbro T and Sundström V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187: 1–65

    Article  Google Scholar 

  • Van Kan PJM, Otte SCM, Kleinherenbrink FAM, Nieveen MC, Aartsma TJ and Van Gorkom HJ (1990) Time-resolved spectroscopy at 10 K of the Photosystem II reaction center; deconvolution of the red absorption band. Biochim Biophys Acta 1020: 146–152

    Article  CAS  Google Scholar 

  • Van Mieghem FJE, Satoh K and Rutherford AW (1991) A chlorophyll tilted 30° relative to the membrane in the Photosystem II reaction centre. Biochim Biophys Acta 1058: 379–385

    CAS  Google Scholar 

  • Van Mieghem FJE, Searle GFW, Rutherford AW and Schaafsma TJ (1992) The influence of the double reduction of QA on the fluorescence decay kinetics of Photosystem II. Biochim Biophys Acta 1100: 198–206

    Article  CAS  Google Scholar 

  • Vass I, Gatzen G and Holzwarth AR (1993) Picosecond time-resolved fluorescence studies on photoinhibition and double reduction of QA in Photosystem II. Biochim Biophys Acta 1183: 388–396

    Article  CAS  Google Scholar 

  • Yruela I, Tomas R, Alfonso M and Picorel R (1999) Effect of the pH on the absorption spectrum of the isolated D1–D2-cytochrome b559 complex of Photosystem II. J Photochem Photobiol B 50: 129–136

    Article  CAS  Google Scholar 

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  1. Faculty of Sciences, Division of Physics and Astronomy, Vrije Universiteit, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands

    Jan P. Dekker

  2. Faculty of Sciences, Division of Physics and Astronomy, Vrije Universiteit, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands

    Rienk Van Grondelle

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Dekker, J.P., Van Grondelle, R. Primary charge separation in Photosystem II. Photosynthesis Research 63, 195–208 (2000). https://doi.org/10.1023/A:1006468024245

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