FTIR evidence that the PsbP extrinsic protein induces protein conformational changes around the oxygen-evolving Mn cluster in photosystem II

Biochemistry

Volumn 48, Issue 27, 2009, Pages 6318-6325

  Tomita, Megumi ^a   Ifuku, Kentaro ^b   Sato, Fumihiko ^b   Noguchi, Takumi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE I; AMIDE I BANDS; BINDING PROPERTIES; COFACTORS; CONFORMATIONAL CHANGE; FTIR; HIGHER PLANTS; IMIDAZOLE GROUP; LIGAND STRUCTURE; MN CLUSTERS; MOLECULAR MECHANISM; N-TERMINAL; PHOTOSYSTEM II; PROTEIN CONFORMATION; RETENTION ABILITY; STRUCTURAL COUPLING;

AMIDES; BINDING ENERGY; CALCIUM; CALCIUM CHLORIDE; CARBOXYLATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; MANGANESE; OXYGEN; PLANTS (BOTANY); PROTEINS; RESTORATION; SODIUM CHLORIDE; WASHING;

MANGANESE COMPOUNDS;

AMIDE; CALCIUM; CARBON 13; CARBOXYLIC ACID; CHLORIDE; IMIDAZOLE; LIGAND; MANGANESE; OXYGEN; PROTEIN PSBO; PROTEIN PSBP; PROTEIN PSBQ; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; HIGHER PLANT; INFRARED SPECTROSCOPY; NONHUMAN; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SPINACH;

MANGANESE; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PROTEIN CONFORMATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EMBRYOPHYTA; SPINACIA OLERACEA;

EID: 67650080532     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9006308     Document Type: Article

References (68)

1. Debus, R. J. (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1102, 269-352.
2. Hillier, W., and Messinger, J. (2005) Mechanism of photosynthetic oxygen production. In Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 567-608, Springer, Dordrecht, The Netherlands.
3. McEvoy, J. P., and Brudvig, G. W. (2006) Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483.
4. Renger, G. (2007) Oxidative photosynthetic water splitting: Energetics, kinetics and mechanism. Photosynth. Res. 92, 407-425.
5. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
6. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040-1044.
7. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16, 334-342.
8. Yano, J., Kern, J., Sauer, K., Latimer, M. J., Pushkar, Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A., and Yachandra, V. K. (2006) Where water is oxidized to dioxygen: Structure of the photosynthetic Mn4Ca cluster. Science 314, 821-825.
9. Murray, J. W., Maghlaoui, K., Kargul, J., Ishida, N., Lai, T.-L., Rutherford, A. W., Sugiura, M., Boussac, A., and Barber, J. (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of Photosystem II. Energy Environ. Sci. 1, 161-166.
10. Yano, J., Kern, J., Irrgang, K. D., Latimer, M. J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J., Zouni, A., and Yachandra, V. K. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II:Acase study for metalloprotein crystallography. Proc. Natl. Acad. Sci. U.S.A. 102, 12047-12052.
11. Grabolle, M., Haumann, M., Muller, C., Liebisch, P., and Dau, H. (2006) Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K. J. Biol. Chem. 281, 4580-4588.
12. Seidler, A. (1996) The extrinsic polypeptides of Photosystem II. Biochim. Biophys. Acta 1277, 35-60.
13. Bricker, T. M., and Burnap, R. L. (2005) The extrinsic proteins of photosystem II. In Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 95-120, Springer, Dordrecht, The Netherlands.
14. Roose, J. L., Wegener, K. M., and Pakrasi, H. B. (2007) The extrinsic proteins of photosystem II. Photosynth. Res. 92, 369-387.
15. Enami, I., Okumura, A., Nagao, R., Suzuki, T., Iwai, M., and Shen, J.-R. (2008) Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth. Res. 98, 349-363.
16. Ifuku, K., Ishihara, S., Shimamoto, R., Ido, K., and Sato, F. (2008) Structure, function, and evolution of the PsbP protein family in higher plants. Photosynth. Res. 98, 427-437.
17. Miyao, M., Murata, N., Lavorel, J., Maisonpeteri, B., Boussac, A., and Etienne, A. L. (1987) Effect of the 33 kDa protein on the S-state transitions in photosynthetic oxygen evolution. Biochim. Biophys. Acta 890, 151-159.
18. Nield, J., and Barber, J. (2006) Refinement of the structural model for the Photosystem II supercomplex of higher plants. Biochim. Biophys. Acta 1757, 353-361.
19. Miyao, M., and Murata, N. (1983) Partial reconstitution of the photosynthetic oxygen evolution system by rebinding of the 33-kDa polypeptide. FEBS Lett. 164, 375-378.
20. Miyao, M., and Murata, N. (1983) Partial disintegration and reconstitution of the photosynthetic oxygen evolution system. Binding of 24 kDa and 18 kDa polypeptides. Biochim. Biophys. Acta 725, 87-93.
21. 2+. Biochemistry 34, 9021-9027.
22. 2 evolving complex of photosystem II. Biochemistry 37, 8595-8604.
23. Ghanotakis, D. F., Babcock, G. T., and Yocum, C. F. (1984) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations. FEBS Lett. 167, 127-130.
24. Miyao, M., and Murata, N. (1984) Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution. FEBS Lett. 168, 118-120.
25. 2+. Biochemistry 27, 3476-3483.
26. Ghanotakis, D. F., Topper, J. N., and Yocum, C. F. (1984) Structural organization of the oxidizing side of photosystem II. Exogenous reductants reduce and destroy the Mn-complex in photosystems II membranes depleted of the 17 and 23 kDa polypeptides. Biochim. Biophys. Acta 767, 524-531.
27. Ifuku, K., Yamamoto, Y., Ono, T., Ishihara, S., and Sato, F. (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol. 139, 1175-1184.
28. Yi, X. P., Hargett, S. R., Liu, H. J., Frankel, L. K., and Bricker, T. M. (2007) The PsbP protein is required for photosystem II complex assembly/stability and photoautotrophy in Arabidopsis thaliana. J. Biol. Chem. 282, 24833-24841.
29. Yi, X. P., Hargett, S. R., Frankel, L. K., and Bricker, T. M. (2006) The PsbQ protein is required in Arabidopsis for photosystem II assembly/stability and photoautotrophy under low light conditions. J. Biol. Chem. 281, 26260-26267.
30. Chu, H.-A., Hillier, W., Law, N. A., and Babcock, G. T. (2001) Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim. Biophys. Acta 1503, 69-82.
31. Noguchi, T., and Berthomieu, C. (2005) Molecular analysis by vibrational spectroscopy. In Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 367-387, Springer, Dordrecht, The Netherlands.
32. Noguchi, T. (2007) Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. Photosynth. Res. 91, 59-69.
33. Noguchi, T. (2008) Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord. Chem. Rev. 252, 336-346.
34. Debus, R. J. (2008) Protein ligation of the photosynthetic oxygenevolving center. Coord. Chem. Rev. 252, 244-258.
35. Noguchi, T. (2008) FTIR detection of water reactions in the oxygenevolving center of photosystem II. Philos. Trans. R. Soc. London, Ser. B 363, 1189-1195.
36. 2+ retention in photosystem II. Plant Cell Physiol. 43, 1244-1249.
37. Ifuku, K., Nakatsu, T., Shimamoto, R., Yamamoto, Y., Ishihara, S., Kato, H., and Sato, F. (2005) Structure and function of the PsbP protein of Photosystem II from higher plants. Photosynth. Res. 84, 251-255.
38. Berthold, D. A., Babcock, G. T., and Yocum, C. F. (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties. FEBS Lett. 134, 231-234.
39. Ono, T., and Inoue, Y. (1986) Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in photosystem II particles. Biochim. Biophys. Acta 850, 380-389.
40. Åkerlund, H.-E., Jansson, C., and Andersson, B. (1982) Reconstitution of photosynthetic water splitting in inside-out thylakoid vesicles and identification of a participating polypeptide. Biochim. Biophys. Acta 681, 1-10.
41. 2-evolving PS II particles by divalent salt-washing. FEBS Lett. 164, 255-260.
42. Ifuku, K., and Sato, F. (2001) Importance of the N-terminal sequence of the extrinsic 23 kDa polypeptide in Photosystem II in ion retention in oxygen evolution. Biochim. Biophys. Acta 1546, 196-204.
43. 2+ in the photosynthetic oxygen-evolving center by means of Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1228, 189-200.
44. Noguchi, T., and Inoue, Y. (1995) Identification of Fourier-transform infrared signals from the non-heme iron in photosystem II. J. Biochem. 118, 9-12.
45. 13C isotope labeling. Biochemistry 42, 6035-6042.
46. 2 transition: An isotope-edited FTIR study. Biochemistry 43, 3152-3166.
47. Yamanari, T., Kimura, Y., Mizusawa, N., Ishii, A., and Ono, T. (2004) Mid- to low-frequency Fourier transform infrared spectra of S-state cycle for photosynthetic water oxidation in Synechocystis sp PCC 6803. Biochemistry 43, 7479-7490.
48. Noguchi, T., Inoue, Y., and Tang, X.-S. (1999) Structure of a histidine ligand in the photosynthetic oxygen-evolving complex as studied by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 38, 10187-10195.
49. 2+ depletion as revealed by FTIR difference spectroscopy. Biochim. Biophys. Acta 1767, 535-540.
50. Hasegawa, K., Kimura, Y., and Ono, T. (2002) Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy. Biochemistry 41, 13839-13850.
51. 1 FTIR spectrum in oxygen-evolving complex of photosystem II. Biochemistry 40, 14061-14068.
52. 2+ depletion and metal cation substitution in the photosynthetic oxygen-evolving complex. Biochemistry 41, 5844-5853.
53. Byler, D. M., and Susi, H. (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25, 469-487.
54. Surewicz, W. K., and Mantsch, H. H. (1988) New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta 952, 115-130.
55. Ifuku, K., Nakatsu, T., Kato, H., and Sato, F. (2004) Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum. EMBO Rep. 5, 362-367.
56. Zhang, H., Ishikawa, Y., Yamamoto, Y., and Carpentier, R. (1998) Secondary structure and thermal stability of the extrinsic 23 kDa protein of photosystem II studied by Fourier transform infrared spectroscopy. FEBS Lett. 426, 347-351.
57. B of photosystem II determined by time-resolved Fourier transform infrared spectroscopy. Biochemistry 37, 5511-5517.
58. 1-state manganese cluster. Biochemistry 37, 5039-5045.
59. Tohri, A., Dohmae, N., Suzuki, T., Ohta, H., Inoue, Y., and Enami, I. (2004) Identification of domains on the extrinsic 23 kDa protein possibly involved in electrostatic interaction with the extrinsic 33 kDa protein in spinach photosystem II. Eur. J. Biochem. 271, 962-971.
60. Calderone, V., Trabucco, M., Vujicic, A., Battistutta, R., Giacometti, G. M., Andreucci, F., Barbato, R., and Zanotti, G. (2003) Crystal structure of the PsbQ protein of photosystem II from higher plants. EMBO Rep. 4, 900-905.
61. Hutchison, R. S., Steenhuis, J. J., Yocum, C. F., Razeghifard, M. R., and Barry, B. A. (1999) Deprotonation of the 33-kDa, extrinsic, manganese-stabilizing subunit accompanies photooxidation of manganese in photosystem II. J. Biol. Chem. 274, 31987-31995.
62. 2 transition in the oxygen-evolving manganese cluster in photosystem II by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 31, 5953-5956.
63. Chu, H.-A., Gardner, M. T., O'Brien, J. P., and Babcock, G. T. (1999) Low-frequency Fourier transform infrared spectroscopy of the oxygen-evolving and quinone acceptor complexes in photosystem II. Biochemistry 38, 4533-4541.
64. Remy, A., Niklas, J., Kuhl, H., Kellers, P., Schott, T., Rögner, M., and Gerwert, K. (2004) FTIR spectroscopy shows structural similarities between photosystems II from cyanobacteria and spinach. Eur. J. Biochem. 271, 563-567.
65. A reduction in photosystem II. Biochemistry 35, 15447-15460.
66. -• in cyanidetreated, high pH-treated and iron-depleted photosystem II membrane fragments. Biochemistry 38, 4846-4852.
67. Halverson, K. M., and Barry, B. A. (2003) Evidence for spontaneous structural changes in a dark-adapted state of photosystem II. Biophys. J. 85, 2581-2588.
68. 2 state. Photosynth. Res. 63, 47-57.