, Volume 56, Issue 1, pp 178–184 | Cite as

PsbP-induced protein conformational changes around Cl ions in the water oxidizing center of photosystem II

  • J. Kondo
  • T. Noguchi


PsbP is an extrinsic protein of PSII having a function of Ca2+ and Cl retention in the water-oxidizing center (WOC). In order to understand the mechanism how PsbP regulates the Cl binding in WOC, we examined the effect of PsbP depletion on the protein structures around the Cl sites using Fourier transform infrared (FTIR) spectroscopy. Light-induced FTIR difference spectra upon the S1→S2 transition were obtained using Cl-bound and NO3-substituted PSII membranes in the presence and absence of PsbP. A clear difference in the amide I band changes by PsbP depletion was observed between Cl-bound and NO3-substituted PSII samples, indicating that PsbP binding perturbed the protein conformations around the Clion(s) in WOC. It is suggested that PsbP stabilizes the Cl binding by regulating the dissociation constant of Cl and/or an energy barrier of Cl dissociation through protein conformational changes around the Cl ion(s).

Additional key words

Mn4CaO5 cluster oxygen evolution photosynthesis 





Fourier transform infrared


2-(N-morpholino) ethanesulfonic acid


phenazine methosulfate


water-oxidizing center


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  1. Ashizawa R., Noguchi T.: Effects of hydrogen bonding interactions on the redox potential and molecular vibrations of plastoquinone as studied by density functional theory calculations.–Phys. Chem. Chem. Phys. 16: 11864–11876, 2014.CrossRefPubMedGoogle Scholar
  2. Berthomieu C., Nabedryk E., Mäntele W. et al.: Characterization by FTIR spectroscopy of the photoreduction of the primary quinone acceptor QA in photosystem II.–FEBS Lett. 269: 363–367, 1990.CrossRefPubMedGoogle Scholar
  3. Bricker T.M., Roose J.L., Fagerlund R.D. et al.: The extrinsic proteins of Photosystem II.–Biochim. Biophys. Acta 1817: 121–142, 2012.CrossRefPubMedGoogle Scholar
  4. Bricker T.M., Roose J.L., Zhang P. et al.: The PsbP family of proteins.–Photosynth. Res. 116: 235–250, 2013.CrossRefPubMedGoogle Scholar
  5. Chu H.-A.: Fourier transform infrared difference spectroscopy for studying the molecular mechanism of photosynthetic water oxidation.–Front. Plant Sci. 4: 146, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Debus R.J.: FTIR studies of metal ligands, networks of hydrogen bonds, and water molecules near the active site Mn4CaO5 cluster in Photosystem II.–BBA-Bioenergetics 1847: 19–34, 2015.CrossRefPubMedGoogle Scholar
  7. Enami I., Okumura A., Nagao R. et al.: Structures and functions of the extrinsic proteins of photosystem II from different species.–Photosynth. Res. 98: 349–363, 2008.CrossRefPubMedGoogle Scholar
  8. Fagerlund R.D., Eaton-Rye J.J.: The lipoproteins of cyanobacterial photosystem II.–J. Photoch. Photobio. B 104: 191–203, 2011.CrossRefGoogle Scholar
  9. Grundmeier A., Dau H.: Structural models of the manganese complex of photosystem II and mechanistic implications.–Biochim. Biophys. Acta 1817: 88–105, 2012.CrossRefPubMedGoogle Scholar
  10. Hasegawa K,. Kimura Y., Ono T.: Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy.–Biochemistry 41: 13839–13850, 2002.CrossRefPubMedGoogle Scholar
  11. Hasegawa K., Kimura Y., Ono T.: Oxidation of the Mn cluster induces structural changes of NO3− functionally bound to the Cl− site in the oxygen-evolving complex of photosystem II.–Biophys. J. 86: 1042–1050, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ido K., Kakiuchi S., Uno C. et al.: The conserved His-144 in the PsbP protein is important for the interaction between the PsbP N-terminus and the Cyt b559 subunit of photosystem II.–J. Biol. Chem. 287: 26377–26387, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ifuku K., Ishihara S., Shimamoto R. et al.: Structure, function, and evolution of the PsbP protein family in higher plants.–Photosynth. Res. 98: 427–437, 2008.CrossRefPubMedGoogle Scholar
  14. Ifuku K., Ido K., Sato F.: Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex.–J. Photoch. Photobio. B 104: 158–164, 2011.CrossRefGoogle Scholar
  15. Ifuku K., Noguchi T.: Structural coupling of extrinsic proteins with the oxygen-evolving center in photosystem II.–Front. Plant Sci. 7: 84, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Joliot P., Barbieri G., Chabaud R.: Model of the System II photochemical centers.–Photochem. Photobiol. 10: 309–329, 1969.CrossRefGoogle Scholar
  17. Kakiuchi S., Uno C., Ido K. et al.: The PsbQ protein stabilizes the functional binding of the PsbP protein to photosystem II in higher plants.–Biochim. Biophys. Acta 1817: 1346–1351, 2012.CrossRefPubMedGoogle Scholar
  18. Kok B., Forbush B., McGloin M.: Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism.–Photochem. Photobiol. 11: 457–475, 1970.CrossRefPubMedGoogle Scholar
  19. Messinger J., Noguchi T., Yano J.: Photosynthetic O2 evolution. Chapter 7.–In: Wydrzynski T., Hillier W. (ed.): Molecular Solar Fuels. Pp. 163–207. Royal Society of Chemistry, Cambridge 2012.Google Scholar
  20. Miyao M., Fujimura Y., Murata N.: Partial degradation of the extrinsic 23-kDa protein of the Photosystem II complex of spinach.–BBA-Bioenergetics 936: 465–474, 1988.CrossRefGoogle Scholar
  21. Nagao R., Tomo T., Noguchi T.: Effects of extrinsic proteins on the protein conformation of the oxygen-evolving center in cyanobacterial photosystem II as revealed by Fourier transform infrared spectroscopy.–Biochemistry 54: 2022–2031, 2015.CrossRefPubMedGoogle Scholar
  22. Nakamura S., Noguchi T.: Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the wateroxidizing Mn4CaO5 cluster in photosystem II.–P. Natl. Acad. Sci. USA 113: 12727–12732, 2016.CrossRefGoogle Scholar
  23. Nishimura T., Nagao R., Noguchi T. et al.: The N-terminal sequence of the extrinsic PsbP protein modulates the redox potential of Cyt b559 in photosystem II.–Sci. Rep. 6: 21490, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nishimura T., Uno C., Ido K. et al.: Identification of the basic amino acid residues on the PsbP protein involved in the electrostatic interaction with photosystem II.–Biochim. Biophys. Acta 1837: 1447–1453, 2014.CrossRefPubMedGoogle Scholar
  25. Noguchi T.: Fourier transform infrared difference and timeresolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation.–BBABioenergetics 1847: 35–45, 2015.CrossRefGoogle Scholar
  26. Noguchi T., Berthomieu C.: Molecular analysis by vibrational spectroscopy.–In: Wydrzynski T., Satoh K. (ed.): Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Pp. 367–387. Springer, Dordrecht 2005.Google Scholar
  27. Noguchi T., Ono T., Inoue Y.: Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygenevolving center by means of Fourier transform infrared spectroscopy.–BBA-Bioenergetics 1228: 189–200, 1995.CrossRefGoogle Scholar
  28. Noguchi T., Sugiura M.: Flash-induced Fourier transform infrared detection of the structural changes during the S-state cycle of the oxygen-evolving complex in photosystem II.–Biochemistry 40: 1497–1502, 2001.CrossRefPubMedGoogle Scholar
  29. Noguchi T., Sugiura M.: Analysis of flash-induced FTIR difference spectra of the S-state cycle in the photosynthetic water-oxidizing complex by uniform 15N and 13C isotope labeling.–Biochemistry 42: 6035–6042, 2003.CrossRefPubMedGoogle Scholar
  30. Ono T., Inoue Y.: Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in photosystem II particles.–BBA-Bioenergetics 850: 380–389, 1986.CrossRefGoogle Scholar
  31. Petrouleas V., Crofts A.R.: The quinone iron acceptor complex.–In: Wydrzynski T., Satoh K. (ed.): Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Pp. 177–206. Springer, Dordrecht 2005.Google Scholar
  32. Roose J.L., Frankel L.K., Mummadisetti M.P. et al.: The extrinsic proteins of photosystem II: update.–Planta 243: 889–908, 2016.CrossRefPubMedGoogle Scholar
  33. Seidler A.: The extrinsic polypeptides of Photosystem II.–Biochim. Biophys. Acta 1277: 35–60, 1996.CrossRefPubMedGoogle Scholar
  34. Shen J.-R.: The structure of photosystem II and the mechanism of water oxidation in photosynthesis.–Annu. Rev. Plant Biol. 66: 23–48, 2015.CrossRefPubMedGoogle Scholar
  35. Sinclair J.: The influence of anions on oxygen evolution by isolated spinach chloroplasts.–Biochim. Biophys. Acta 764: 247–252, 1984.CrossRefGoogle Scholar
  36. Suga M., Akita F., Hirata K. et al.: Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.–Nature 517: 99–103, 2015.CrossRefPubMedGoogle Scholar
  37. Suzuki H., Sugiura M., Noguchi T.: 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, 2012.CrossRefPubMedGoogle Scholar
  38. Suzuki H., Yu J., Kobayashi T. et al.: 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, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tomita M., Ifuku K., Sato F. et al: FTIR evidence that the PsbP extrinsic protein induces protein conformational changes around the oxygen-evolving Mn cluster in photosystem II.–Biochemistry 48: 6318–6325, 2009.CrossRefPubMedGoogle Scholar
  40. Uno C., Nagao R., Suzuki H. et al.: Structural coupling of extrinsic proteins with the oxygen-evolving center in red algal photosystem II as revealed by light-induced FTIR difference spectroscopy.–Biochemistry 52: 5705–5707, 2013.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. Vinyard D.J., Ananyev G.M., Dismukes G.C.: Photosystem II: The reaction center of oxygenic photosynthesis.–Annu. Rev. Biochem. 82: 577–606, 2013.CrossRefPubMedGoogle Scholar
  43. Wei X.P., Su X.D., Cao P. et al.: Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution.–Nature 534: 69–74, 2016.CrossRefPubMedGoogle Scholar
  44. Wincencjusz H., Yocum C.F., van Gorkom H.J.: Activating anions that replace Cl− in the O2-evolving complex of photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states.–Biochemistry 38: 3719–3725, 1999.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Division of Material Science, Graduate School of ScienceNagoya UniversityFuro-cho, Chikusa-ku, NagoyaJapan

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