Skip to main content

Molecular Mechanism of Asymmetric Electron Transfer on the Electron Donor Side of Photosystem II

  • Chapter
  • First Online:
Photosynthesis: Molecular Approaches to Solar Energy Conversion

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 47))

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allen JP, Williams JC (1998) Photosynthetic reaction centers. FEBS Lett 438:5–9

    Article  CAS  PubMed  Google Scholar 

  • Ananyev GA, Sakiyan I, Diner BA, Dismukes GC (2002) A functional role for tyrosine-D in assembly of the inorganic core of the water oxidase complex of photosystem II and the kinetics of water oxidation. Biochemistry 41:974–980

    Article  CAS  PubMed  Google Scholar 

  • Berthomieu C, Hienerwadel R, Boussac A, Breton J, Diner BA (1998) Hydrogen bonding of redox-active tyrosine Z of photosystem II probed by FTIR difference spectroscopy. Biochemistry 37:10547–10554

    Article  CAS  PubMed  Google Scholar 

  • Boussac A, Etienne AL (1984) Midpoint potential of signal II (slow) in Tris-washed photosystem-II particles. Biochim Biophys Acta 766:576–581

    Article  CAS  Google Scholar 

  • Buser CA, Thompson LK, Diner BA, Brudvig GW (1990) Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry 29:8977–8985

    Article  CAS  PubMed  Google Scholar 

  • Diner B, Britt RD (2005) The redox-active tyrosine YZ and YD. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 207–233

    Google Scholar 

  • Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580

    Article  CAS  PubMed  Google Scholar 

  • Diner BA, Schlodder E, Nixon PJ, Coleman WJ, Rappaport F, Lavergne J, Vermaas WFJ, Chisholm DA (2001) Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry 40:9265–9281

    Article  CAS  PubMed  Google Scholar 

  • Dixon WT, Murphy D (1976) Determination of acidity constants of some phenol radical cations by means of electron spin resonance. J Chem Soc Faraday Trans 2 72:1221–1230

    Article  CAS  Google Scholar 

  • Faller P, Debus RJ, Brettel K, Sugiura M, Rutherford AW, Boussac A (2001) Rapid formation of the stable tyrosyl radical in photosystem II. Proc Natl Acad Sci U S A 98:14368–14373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammes-Schiffer S (2009) Theory of proton-coupled electron transfer in energy conversion processes. Acc Chem Res 42:1881–1889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haumann M, Liebisch P, Müller C, Barra M, Grabolle M, Dau H (2005) Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019–1021

    Article  CAS  PubMed  Google Scholar 

  • Hienerwadel R, Boussac A, Breton J, Berthomieu C (1996) Fourier transform infrared difference study of tyrosineD oxidation and plastoquinone QA reduction in photosystem II. Biochemistry 35:15447–15460

    Article  CAS  PubMed  Google Scholar 

  • Ivancich A, Artz K, Williams JC, Allen JP, Mattioli TA (1998) Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor. Biochemistry 37:11812–11820

    Article  CAS  PubMed  Google Scholar 

  • Joliot P, Barbieri G, Chabaud R (1969) A new model of photochemical centers in system II. Photochem Photobiol 10:309–329

    Article  CAS  Google Scholar 

  • Kato Y, Sugiura M, Oda A, Watanabe T (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc Natl Acad Sci U S A 106:17365–17370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitajima Y, Noguchi T (2006) Photooxidation pathway of chlorophyll Z in photosystem II as studied by Fourier transform infrared spectroscopy. Biochemistry 45:1938–1945

    Article  CAS  PubMed  Google Scholar 

  • Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution: 1. A linear four step mechanism. Photochem Photobiol 11:457–475

    Article  CAS  PubMed  Google Scholar 

  • Krawczyk S (1989) The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a. Biochim Biophys Acta 976:140–149

    Article  CAS  Google Scholar 

  • Kühn P, Eckert H, Eichler HJ, Renger G (2004) Analysis of the P680+• reduction pattern and its temperature dependence in oxygen-evolving PSII core complexes from a thermophilic cyanobacteria and higher plants. Phys Chem Chem Phys 6:4838–4843

    Article  Google Scholar 

  • Magnuson A, Rova M, Mamedov F, Fredriksson PO, Styring S (1999) The role of cytochrome b559 and tyrosineD in protection against photoinhibition during in vivo photoactivation of photosystem II. Biochim Biophys Acta 1411:180–191

    Article  CAS  PubMed  Google Scholar 

  • Messinger J, Renger G (1994) Analyses of pH-induced modifications of the period four oscillation of flash-induced oxygen evolution reveal distinct structural changes of the photosystem II donor side at characteristic pH values. Biochemistry 33:10896–10905

    Article  CAS  PubMed  Google Scholar 

  • Metz JG, Nixon PJ, Rögner M, Brudvig GW, Diner BA (1989) Directed alteration of the D1 polypeptide of photosystem II: evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron-donor, P680. Biochemistry 28:6960–6969

    Article  CAS  PubMed  Google Scholar 

  • Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65

    Article  PubMed  CAS  Google Scholar 

  • Nabedryk E, Leonhard M, Mäntele W, Breton J (1990) Fourier-transform infrared difference spectroscopy shows no evidence for an enolization of chlorophyll a upon cation formation either in vitro or during P700 photooxidation. Biochemistry 29:3242–3247

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yamaguchi M, Nakamura S, Ueoka-Nakanishi H, Noguchi T (2017) Genetically introduced hydrogen bond interactions reveal an asymmetric charge distribution on the radical cation of the special-pair chlorophyll P680. J Biol Chem 292:7474–7486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura S, Noguchi T (2015) Infrared detection of a proton released from tyrosine YD to the bulk upon its photo-oxidation in photosystem II. Biochemistry 54:5045–5053

    Article  CAS  PubMed  Google Scholar 

  • Nakamura S, Nagao R, Takahashi R, Noguchi T (2014) Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II: relevance to the proton transfer mechanism of water oxidation. Biochemistry 53:3131–3144

    Article  CAS  PubMed  Google Scholar 

  • Narzi D, Bovi D, De Gaetano P, Guidoni L (2016) Dynamics of the special pair of chlorophylls of photosystem II. J Am Chem Soc 138:257–264

    Article  CAS  PubMed  Google Scholar 

  • Noguchi T, Tomo T, 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  CAS  PubMed  Google Scholar 

  • Okubo T, Tomo T, Sugiura M, Noguchi T (2007) Perturbation of the structure of P680 and the charge distribution on its radical cation in isolated reaction center complexes of photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 46:4390–4397

    Article  CAS  PubMed  Google Scholar 

  • Petrouleas V, Crofts AR (2005) The iron-quinone acceptor complex. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 177–206

    Google Scholar 

  • Pokhrel R, Service RJ, Debus RJ, Brudvig GW (2013) Mutation of lysine 317 in the D2 subunit of photosystem II alters chloride binding and proton transport. Biochemistry 52:4758–4773

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41:8518–8527

    Article  CAS  PubMed  Google Scholar 

  • Raszewski G, Saenger W, Renger T (2005) Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J 88:986–998

    Article  CAS  PubMed  Google Scholar 

  • Raszewski G, Diner BA, Schlodder E, Renger T (2008) Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys J 95:105–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renger G (2012) Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms. Biochim Biophys Acta 1817:1164–1176

    Article  CAS  PubMed  Google Scholar 

  • Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 139–175

    Google Scholar 

  • Renger T, Schlodder E (2011) Optical properties, excitation energy and primary charge transfer in photosystem II: theory meets experiment. J Photochem Photobiol B 104:126–141

    Article  CAS  PubMed  Google Scholar 

  • Rhile IJ, Markle TF, Nagao H, DiPasquale AG, Lam OP, Lockwood MA, Rotter K, Mayer JM (2006) Concerted proton-electron transfer in the oxidation of hydrogen-bonded phenols. J Am Chem Soc 128:6075–6088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivalta I, Amin M, Luber S, Vassiliev S, Pokhrel R, Umena Y, Kawakami K, Shen JR, Kamiya N, Bruce D, Brudvig GW, Gunner MR, Batista VS (2011) Structural-functional role of chloride in photosystem II. Biochemistry 50:6312–6315

    Article  CAS  PubMed  Google Scholar 

  • Rutherford AW, Boussac A, Faller P (2004) The stable tyrosyl radical in Photosystem II: why D? Biochim Biophys Acta 1655:222–230

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Ishida T, Sugiura M, Kawakami K, Umena Y, Kamiya N, Shen JR, Ishikita H (2011) Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center. J Am Chem Soc 133:14379–14388

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Rutherford AW, Ishikita H (2013) Mechanism of tyrosine D oxidation in photosystem II. Proc Natl Acad Sci U S A 110:7690–7695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Sugiura M, Noguchi T (2018) Mechanism of proton-coupled electron transfer in the S0-to-S1 transition of photosynthetic water oxidation as revealed by time-resolved infrared spectroscopy. J Phys Chem B 122:9460–9470

    Article  CAS  PubMed  Google Scholar 

  • Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817:66–75

    Article  CAS  PubMed  Google Scholar 

  • Styring S, Rutherford AW (1987) In the oxygen-evolving complex of photosystem II the S0 state is oxidized to the S1 state by D+ (signal IIslow). Biochemistry 26:2401–2405

    Article  CAS  Google Scholar 

  • Styring S, Sjöholm J, Mamedov F (2012) Two tyrosines that changed the world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim Biophys Acta 1817:76–87

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Sugiura M, Noguchi T (2009) Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy. J Am Chem Soc 131:7849–7857

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Sugiura M, Noguchi T (2012) Determination of the miss probabilities of individual S-state transitions during photosynthetic water oxidation by monitoring electron flow in photosystem II using FTIR spectroscopy. Biochemistry 51:6776–6785

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Yu J, Kobayashi T, Nakanishi H, Nixon PJ, Noguchi T (2013) Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by Fourier transform infrared analysis. Biochemistry 52:4748–4757

    Article  CAS  PubMed  Google Scholar 

  • Takahashi R, Noguchi T (2007) Criteria for determining the hydrogen-bond structures of a tyrosine side chain by Fourier transform infrared spectroscopy: density functional theory analyses of model hydrogen-bonded complexes of p-cresol. J Phys Chem B 111:13833–13844

    Article  CAS  PubMed  Google Scholar 

  • Takahashi R, Hasegawa K, Noguchi T (2008) Effect of charge distribution over a chlorophyll dimer on the redox potential of P680 in photosystein II as studied by density functional theory calculations. Biochemistry 47:6289–6291

    Article  CAS  PubMed  Google Scholar 

  • Tracewell CA, Cua A, Stewart DH, Bocian DF, Brudvig GW (2001) Characterization of carotenoid and chlorophyll photooxidation in photosystem II. Biochemistry 40:193–203

    Article  CAS  PubMed  Google Scholar 

  • Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Ã…. Nature 473:55–60

    Article  CAS  PubMed  Google Scholar 

  • Vass I, Styring S (1991) pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30:830–839

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Gosztola D, Ruffle SV, Hemann C, Seibert M, Wasielewski MR, Hille R, Gustafson TL, Sayre RT (2002) Functional asymmetry of photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 99:4091–4096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takumi Noguchi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Noguchi, T. (2021). Molecular Mechanism of Asymmetric Electron Transfer on the Electron Donor Side of Photosystem II. In: Shen, JR., Satoh, K., Allakhverdiev, S.I. (eds) Photosynthesis: Molecular Approaches to Solar Energy Conversion. Advances in Photosynthesis and Respiration, vol 47. Springer, Cham. https://doi.org/10.1007/978-3-030-67407-6_12

Download citation

Publish with us

Policies and ethics