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Electron Paramagnetic Resonance Distance Measurements in Photosystems

  • K. V. Lakshmi
  • Gary W. Brudvig
Chapter
Part of the Biological Magnetic Resonance book series (BIMR, volume 19)

Abstract

EPR distance measurements have been extensively employed to characterize the structure and function of the photosynthetic reaction centers from plants, bacteria and algae. Such measurements have also been pivotal in establishing the feasibility of EPR distance measurements in biological systems. In this chapter, we present an overview of distance measurements in the purple non-sulfur bacterial, Photosystem II and Photosystem I reaction centers. The distance measurement techniques described involve both line shape analyses and spin-lattice relaxation measurements by cw and pulsed methods. Also described are EPR studies of oriented membranes and single crystals that facilitate the measurement of interspin distances and relative orientations of redox cofactors.

Keywords

Electron Paramagnetic Resonance Spectrum Electron Paramagnetic Resonance Signal Dipolar Coupling Mosaic Spread Interspin Distance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abragam, A., 1961, The Principles of Nuclear Magnetism, Clarendon Press, Oxford.Google Scholar
  2. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H. and Rees, D. C., 1987, “Structure of the reaction center from Rhodobacter-Sphaeroides R-26–The cofactors.1” Proc. Natl. Acad. Sci. USA 84, 5730–5734.PubMedCentralPubMedCrossRefGoogle Scholar
  3. Astashkin, A. V., Hara, H. and Kawamori, A., 1998, “The pulsed electron-electron doubte resonance and ‘2+1’ electron spin echo study of the oriented oxygen-evolving and Mn-depleted preparations of photosystem II” J. Chem. Phys. 108, 3805–3812.CrossRefGoogle Scholar
  4. Astashkin, A. V., Kodera, Y. and Kawamori, A., 1994, “Distance between tyrosines Z+ and D+ in plant photosystem-II as determined by pulsed EPR” Biochim. Biophys. Acta 1187, 89–93.CrossRefGoogle Scholar
  5. Beck, W. F., Iimes, J. B., Lynch, J. B. and Brudvig, G. W., 1991, “Electron spin-lattice relaxation and spectral diffusion measurements on tyrosine radicals in proteins” J. Magn. Reson. 91, 12–29.Google Scholar
  6. Beinert, H. and Orme-Johnson, W. H., 1967, in “Magnetic Resonance in Biological Systems” (Ehrenberg, A., Malmström, B. G., and Vänngârd, T., Eds.), Pergamon Press, Oxford, pp 221–247.CrossRefGoogle Scholar
  7. Berry, M. C., Bratt, P. J. and Evans, M. C. W., 1997, “Relaxation properties of the photosystem I electron transfer components: Indications of the relative positions of the electron transfer cofactors in photosystem I” Biochim. Biophys. Acta 1319, 163–176.CrossRefGoogle Scholar
  8. Bloembergen, N., 1949, “On the interaction of nuclear spins in a crystalline lattice” Physica 15, 386–426.CrossRefGoogle Scholar
  9. Blum, H., Bowyer, J. R., Cusanovich, M. A., Waring, A. J. and Ohnishi, T., 1983, “Spin-lattice relaxation rates of iron-sulfur proteins and heure proteins affected by dysprosium complexes and temperature” Biochim. Biophys. Acta 748, 418–428.CrossRefGoogle Scholar
  10. Blum, H., Cusanovich, M. A., Sweeney, W. V. and Ohnishi, T., 1981, “Magnetic interactions between dysprosium complexes and soluble iron-sulfur proteins” J. Biol. Chem. 256, 2199–2206.PubMedGoogle Scholar
  11. Blum, H., Leigh, J. S. and Ohnishi, T., 1980, “Effect of dysprosium on the spin-lattice relaxation time of cytochrome c and cytochrome a” Biochim. Biophys. Acta 626, 31–40.PubMedCrossRefGoogle Scholar
  12. Bonvoisin, J., Blondin, G., Girerd, J.-J. and Zimmerman, J.-L., 1992, “Theoretical study of the multiline EPR signal from the S2 state of the oxygen evolving complex of photosystem II” Biophys. J. 61, 1076–1086.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Boussac, A. and Rutherford, A. W., 1988, “Nature of the inhibition of the oxygen-evolving enzyme of photosystem II induced by NaC1 washing and reversed by the addition of Cat+ or Sr2+” Biochemistry 27, 3476–3483.CrossRefGoogle Scholar
  14. Brudvig, G. W., Blair, D. F. and Chan, S. I., 1984, “Electron spin relaxation of CuA and cytochrome a in cytochrome c oxidase comparison to heme, copper, and sulfur radical complexes” J. Biol. Chem. 259, 11001–11009.PubMedGoogle Scholar
  15. Butler, W. F., Calvo, R., Fredkin, D. R., Isaacson, R. A., Okamura, M. Y. and Feher, G., 1984, “The electronic-structure of Fez+ in reaction-centers from RhodopseudomonasSphaeroides.3. Electron-paramagnetic resonance measurements of the reduced acceptor complex” Biophys. J. 45, 947–973.PubMedCentralPubMedCrossRefGoogle Scholar
  16. Butler, W. F., Johnston, D. C., Shore, H. B., Fredkin, D. R., Okamura, M. Y. and Feher, G., 1980, “The electronic structure of Fez+ in reaction centers from Rhodopseudomonas Sphaeroides I. Static magnetization measurements” Biophys. J 32, 967–992.PubMedCentralPubMedCrossRefGoogle Scholar
  17. Castner, T. G., 1959, “Saturation of the paramagnetic resonance of a V center” Phys. Rev. 115, 1506–1515.CrossRefGoogle Scholar
  18. Coffman, R. E. and Buettner, G. R., 1979, “Limit function for long-range ferromagnetic and anti-ferromagnetic superexchange” J. Phys. Chem. 83, 2387–2392.CrossRefGoogle Scholar
  19. Case, G. D. and Leigh, J. S., 1976, “Intramitochondrial positions of cytochrome heme groups determined by dipolar interactions with paramagnetic cations” Biochem. J. 160, 769–783.PubMedCentralPubMedGoogle Scholar
  20. Case, G. D., Ohnishi, T. and Leigh, J. S., 1976, “Intramitochondrial positions of ubiquinone and iron-sulfur centers determined by dipolar interactions with paramagnetic ions” Biochem. J. 160, 785–795.PubMedCentralPubMedGoogle Scholar
  21. Dalton, L. R., Kwiram, A. L. and Cowen, J. A., 1972a, “Electron spin-lattice and cross relaxation in irradiated malonic acid” Chem. Phys. Lett. 14, 77–81.CrossRefGoogle Scholar
  22. Dalton, L. R., Kwiram, A. L. and Cowen, J. A., 1972b, ‘Electron spin-lattice relaxation in molecular crystals-S = 1/2“ Chem. Phys. Lett. 17, 495–499.CrossRefGoogle Scholar
  23. Debus, R. J., 1992, “The manganese and calcium-ions of photosynthetic oxygen evolution” Biochim. Biophys. Acta 1102, 269–352.PubMedCrossRefGoogle Scholar
  24. Deisenhofer, J., Epp, O., Miki, K., Huber, R. and Michel, H., 1984, “X-ray structure analysis of a membrane protein complex–Electron density map at 3 A resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas Viridis” J. Mol. Biol. 180, 385–398.PubMedCrossRefGoogle Scholar
  25. Deisenhofer, J., Epp, O., Miki, K., Huber, R. and Michel, H., 1985, “Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas Viridis at 3 A resolution” Nature 318, 618–624.PubMedCrossRefGoogle Scholar
  26. Deligiannakis, Y., Hanley, J. and Rutherford, A. W., 1998, “Spin-lattice relaxation of the phyllosemiquinone radical of photosystem I” Biochemistry 37, 3329–3336.PubMedCrossRefGoogle Scholar
  27. Deligiannakis, Y. and Rutherford, A. W., 1996, “Spin-lattice relaxation of the pheophytin, pheo, radical of photosystem II” Biochemistry 35, 11239–11246.PubMedCrossRefGoogle Scholar
  28. Dismukes, G. C., Frank, H. A., Friesner, R. and Sauer, K., 1984, “Electronic interactions between iron and bound semiquinones in bacterial photosynthesis–Electron paramagnetic resonance spectroscopy of oriented cells of Rhodopseudomonas-Viridis” Biochim. Biophys. Acta 764, 253–271.CrossRefGoogle Scholar
  29. Dorlet, P., Di Valentin, M., Babcock, G. T. and McCracken, J. L., 1998, “Interaction of Yz with its environment in acetate-treated photosystem II membranes and reaction center cores” J. Phys. Chem. B 102, 8239–8247.CrossRefGoogle Scholar
  30. Ermler, U., Fritzsch, G., Buchanan, S. K. and Michel, H., 1994, “Structure of the photosynthetic reaction center from Rhodobacter-Sphaeroides at 2.65-angstrom resolution–Cofactors and protein-cofactor interactions” Structure 2 925–936.PubMedCrossRefGoogle Scholar
  31. Evelo, R. G., Styring, S., Rutherford, A. W. and Hoff, A. J., 1989, “EPR relaxation measurements of photosystem II reaction centers: Influence of S-state oxidation and temperature” Biochim. Biophys. Acta 973, 428–442.CrossRefGoogle Scholar
  32. Falkowski, K. M., Scholes, C. P. and Tayleo, H., 1986, “Pulse field-sweep electronparamagnetic-resonance–A method of extracting hyperfine information from inhomogeneously broadened electron-paramagnetic-resonance lines of bioinorganic systems” J. Magn. Reson. 68, 453–468.Google Scholar
  33. Feher, G., Allen, J. P., Okamura, M. Y. and Rees, D. C., 1989, “Structure and function of bacterial photosynthetic reaction centers” Nature 339, 111–116.CrossRefGoogle Scholar
  34. Feher, G., Isaacson, R. A., McElroy, J. D., Ackerson, L. C. and Okamura, M. Y., 1974, “On the question of the primary acceptor in bacterial photosynthesis:Manganese substituting for iron in reaction centers of Rhodopseudomonas Sphaeroides R-26” Biochim. Biophys. Acta 368, 135–139.PubMedCrossRefGoogle Scholar
  35. Fielding, L., More, K. M., Eaton, G. R. and Eaton, S. S., 1986, “Metal-nitroxyl interactions. 51. Collapse of iron-nitroxyl electron-electron spin-spin splitting due to the increase in the electron spin relaxation rate for high-spin iron(III) when temperature is increased” J. Amer. Chem. Soc. 108, 8194–8196.CrossRefGoogle Scholar
  36. Force, D. A., Randall, D. W. and Britt, R. D., 1997, “Proximity of acetate, manganese and exchangeable deuterons to tyrosine Yi in acetate inhibited photosystem II membranes: Implications for the direct involvement of Yi in water-splitting” Biochemistry 36, 12062–12070.PubMedCrossRefGoogle Scholar
  37. Fromme, P., Witt, H. T., Schubert, W.-D., Klukas, O., Saenger, W. and Krauß, N., 1996, “Structure of photosystem I at 4.5 A resolution: A short review including evolutionary aspects” Biochim. Biophys. Acta 1275, 76–83.CrossRefGoogle Scholar
  38. Galli, C., Inns, J. B., Hirsh, D. J. and Brudvig, G. W., 1996, “Effects of dipole-dipole interactions on microwave progressive power saturation of radicals in proteins” J. Magn. Reson. B 110, 284–287.PubMedCrossRefGoogle Scholar
  39. Ghanotakis, D. F., Babcock, G. T. and Yocum, C. F., 1985, “Structure of the oxygen-evolving complex of photosystem II–calcium and lanthanum compete for sites on the oxidizing side of photosystem II which control the binding of water-soluble polypeptides and regulate the activity of the manganese complex” Biochim. Biophys. Acta 809, 173–180.CrossRefGoogle Scholar
  40. Gilchrist, M. L., Ball, J. A., Randall, D. W. and Britt, R. D., 1995, “Proximity of the manganese cluster of photosystem II to the redox-active tyrosine Yz” Proc. Nat! Acad. Sci. USA 92, 9545–9549.PubMedCentralPubMedCrossRefGoogle Scholar
  41. Golbeck, J. H., 1992, in “Structure and function of photosystem P” Ann. Rev. Plant Phys. Plant Molec. Biol. 43, 293–324.CrossRefGoogle Scholar
  42. Golbeck, J. H., and Bryant, D. A., 1991, “Photosystem P” Current Topics in Bioenergetics 16, 83–177.CrossRefGoogle Scholar
  43. Goodman, G. and Leigh Jr., J. S., 1985, “Distance between the visible copper and cytochrome a in bovine heart cytochrome oxidase” Biochemistry 24, 2310–2317.PubMedCrossRefGoogle Scholar
  44. Guigliarelli, B., Guillaussier, J., More, C., Sétif, P., Bottin, H. and Bertrand, P., 1993, “Structural organization of the iron-sulfur clusters in Synechocystis 6803 photosystem I. EPR study of oriented thylakoid membranes and analysis of the magnetic interactions” J. Biol. Chem. 268, 900–908.PubMedGoogle Scholar
  45. Hales, B. J., 1993, “Intrinsic and extrinsic paramagnets as probes of metal-clusters” Metallobiochem., PT D 227, 384–395.Google Scholar
  46. Hara, H. and Kawamori, A., 1997, “A selective hole burning method applied to determine distances between paramagnetic species in photosystems” Appl. Magn. Reson. 13, 241–257.CrossRefGoogle Scholar
  47. Hara, H., Kawamori, A., Astashkin, A. V. and Ono, T., 1996, “The distances from tyrosine D to redox-active components on the donor side of photosystem II determined by pulsed electron-electron double resonance” Biochim. Biophys. Acta 1276, 140–146.CrossRefGoogle Scholar
  48. Hirsh, D. J., Beck, W. F., lies, J. B. and Brudvig, G. W., 1992a, “Using saturation recovery EPR to measure distances in proteins–Applications to photosystem IP” Biochemistry 31, 532–541.PubMedCrossRefGoogle Scholar
  49. Hirsh, D. J., Beck, W. F., Lynch, J. B., Que, L. J. and Brudvig, G. W., 1992b, “Using saturation-recovery EPR to measure exchange couplings in proteins: Applications to ribonucleotide reductase” J Amer. Chem. Soc. 114, 7475–7481.CrossRefGoogle Scholar
  50. Hirsh, D. J. and Brudvig, G. W., 1993, “Long-range electron spin-spin interactions in the bacterial photosynthetic reaction center” J. Phys. Chem. 97, 13216–13222.CrossRefGoogle Scholar
  51. Hoff, A. J., 1986, “Magnetic-interactions between photosynthetic reactants” Photochem. Photobiol. 43, 727–745.CrossRefGoogle Scholar
  52. Hoganson, C. W. and Babcock, G. T., 1997, “A metalloradical mechanism for the generation of oxygen from water in photosynthesis” Science 277, 1953–1956.PubMedCrossRefGoogle Scholar
  53. Hyde, J. S. and Rao, K. V. S., 1978, “Dipolar-induced electron spin-lattice relaxation in unordered solids” J. Magn. Reson. 29, 509–516.Google Scholar
  54. Innes, J. B. and Brudvig, G. W., 1989, “Location and magnetic-relaxation properties of the stable tyrosine radical in photosystem IP” Biochemistry 28, 1116–1125.PubMedCrossRefGoogle Scholar
  55. Kamlowski, A., van der Est, A., Fromme, P., Krauß, N., Schubert, W.-D., Klukas, O. and Stehlik, D., 1997a, “The structural organization of the PsaC protein in photosystem I from single crystal EPR and x-ray crystallographic studies” Biochim. Biophys. Acta 1319, 199–213.PubMedCrossRefGoogle Scholar
  56. Kamlowski, A., van der Est, A., Fromme, P. and Stehlik, D., 1997b, “Low temperature EPR on photosystem I single crystals: Orientation of the iron-sulfur centers F-A and F-B” Biochim. Biophys. Acta 1319, 185–198.CrossRefGoogle Scholar
  57. Kodera, Y., Dzuba, S. A., Hara, H. and Kawamori, A., 1994, “Distances from tyrosine D+ to the manganese cluster and the acceptor iron in photosystem II as determined by selective hole-burning in EPR spectra” Biochim. Biophys. Acta 1186, 91–99.CrossRefGoogle Scholar
  58. Kodera, Y., Hara, H., Astashkin, A. V., Kawamori, A. and Ono, T. A., 1995, “EPR study of trapped tyrosine Z+ in Ca-depleted photosystem II” Biochim. Biophys. Acta 1232, 43–51.CrossRefGoogle Scholar
  59. Kodera, Y., Takura, K. and Kawamori, A., 1992, “Distance P680 from the manganese complex in photosystem II studies by time-resolved EPR” Biochim. Biophys. Acta 1101, 23–32.CrossRefGoogle Scholar
  60. Kok, B., Forbush, B. and McGloin, M., 1970, “Cooperation of charges in photosynthetic O2 evolution.1. A linear 4 step mechanism” Photochem. Photobiol. 11, 457–475.PubMedCrossRefGoogle Scholar
  61. Koulougliotis, D., Innes, J. B. and Brudvig, G. W., 1994, “Location of chlorophyllz in photosystem IP” Biophys. J. 66, A114 - A114.CrossRefGoogle Scholar
  62. Koulougliotis, D., Schweitzer, R. H. and Brudvig, G. W., 1997, “The tetranuclear manganese cluster in photosystem II: Location and magnetic properties of the S 2 state as determined by saturation-recovery EPR spectroscopy” Biochemistry 36, 9735–9746.PubMedCrossRefGoogle Scholar
  63. Koulougliotis, D., Tang, X.-S., Diner, B. A. and Bnidvig, G. W., 1995, “Spectroscopic evidence for the symmetrical location of tyrosines D and Z in photosystem IP” Biochemistry 34, 2850–2856.PubMedCrossRefGoogle Scholar
  64. Krauß, N., Schubert, W.-D., Klukas, O., Fromme, P., Witt, H. T. and Saenger, W., 1996, “Photosystem I at 4 angstrom resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system” Nature Struct. Biot. 3, 965–969.CrossRefGoogle Scholar
  65. Kulikov, A. V. and Likhtenshtein, G. I., 1977, “Use of spin relaxation phenomena in investigation of structure of model and biological systems by method of spin labels” Adv. Mol. Relax. Interact. Processes 10, 47–79.CrossRefGoogle Scholar
  66. Lakshmi, K. V., Eaton, S. S., Eaton, G. R. and Brudvig, G. W., 1999a, “Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of photosystem II: An EPR study of the S2YZ state in oriented acetate-inhibited photosystem II membranes” Biochemistry 38, 12758–12767.PubMedCrossRefGoogle Scholar
  67. Lakshmi, K. V., Eaton, S. S., Eaton, G. R., Frank, H. A. and Brudvig, G. W., 1998, “Analysis of dipolar and exchange interactions between manganese and tyrosine Z in the S2YZ state of acetate-inhibited photosystem II via EPR spectral simulations at X- and Q-Bands” J. Phys. Chem. B 102, 8327–8335.CrossRefGoogle Scholar
  68. Lakshmi, K. V., Jung, Y.-S., Golbeck, J. H. and Brudvig, G. W., 1999b, “Location of the iron-sulfur clusters FA and FB in photosystem I: An electron paramagnetic resonance study of spin relaxation enhancement of P 700+” Biochemistry 38, 13210–13215.PubMedCrossRefGoogle Scholar
  69. Lancaster, C. R. D. and Michel, H., 1999, “Refined crystal structures of reaction centers from Rhodopseudomonas Viridis in complexes with the herbicide atrazine and two chiral atrazine derivatives also lead to a new model of the bound carotenoid” J. Mol. Biol. 286, 883–898.PubMedCrossRefGoogle Scholar
  70. Limburg, J., Szalai, V. A. and Brudvig, G. W., 1999, “A mechanistic and structural model for the formation and reactivity of a Mn-V=O species in photosynthetic water oxidation” J. Chem Soc., Dalton Trans., 1353–1361.Google Scholar
  71. Makinen, M. W. and Wells, G. B., 1987, “Application of electron-paramagnetic-resonance saturation methods to paramagnetic metal ions in proteins” Metal Ions in Biological Systems 22, 171–206.Google Scholar
  72. McLachlan, D. J. and Nugent, J. H. A., 1993, “Investigation of the S3 electron paramagnetic resonance signal from the oxygen-evolving complex of photosystem 2: Effect of inhibition of oxygen evolution by acetate” Biochemistry 32, 9772–9780.CrossRefGoogle Scholar
  73. Milov, A. D., Maryasov, A. G. and Tsvetkov, Y. D., 1998, “Pulsed electron double resonance (PELDOR) and its applications in free radicals research” Appl. Magn. Reson. 15, 107–143.CrossRefGoogle Scholar
  74. Norris, J. R., Thurnauer, M. C. and Bowman, M. K., 1980, “Electron spin echo spectroscopy and the study of biological structure and function” Adv. Biol. Med. Phys. 17, 365–416.PubMedCrossRefGoogle Scholar
  75. Okamura, M. Y., Isaacson, R. A. and Feher, G., 1975, “Primary acceptor in photosynthesis: Obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas Sphaeroides” Proc. Natl. Acad. Sci. USA 72, 3491–3495.CrossRefGoogle Scholar
  76. Oliver, M. E. and Hales, B. J., 1993, “Using dysprosium complexes to probe the nitrogenase paramagnetic centers” Biochemistry 32, 6058–6064.PubMedCrossRefGoogle Scholar
  77. Peloquin, J. M., Campbell, K. A. and Britt, R. D., 1998, “Mn-55 pulsed ENDOR demonstrates that the photosystem II ”split“ EPR signal arises From a magnetically-coupled mangano-tyrosyl complex” J. Amer. Chem. Soc. 120, 6840–6841.CrossRefGoogle Scholar
  78. Percival, P. W. and Hyde, J. S., 1975, “Pulsed EPR spectrometer 2.” Rev. Sci. Instrum. 46. 1522–1529.CrossRefGoogle Scholar
  79. Portis, M., 1953, “Electronic structure of F centers: Saturation of the electron spin resonance” Phys. Rev. 91, 1071–1079.CrossRefGoogle Scholar
  80. Rakowsky, M. H., More, K. M., Kulikov, A. V., Eaton, G. R. and Eaton, S. S., 1995, “Time-domain electron paramagnetic resonance as a probe of electron-electron spin-spin interaction in spin-labeled low-spin iron porphyrins” J. Amer. Chem. Soc. 117, 2049–2058.CrossRefGoogle Scholar
  81. Rhee, K.-H., Morris, E. P., Barber, J. and Kúhlbrandt, W., 1998, “Three-dimensional structure of the plant photosystem II at 8 A resolution” Nature 396, 283–286.PubMedCrossRefGoogle Scholar
  82. Sahlin, M., Petersson, L., Graslund, A., Ehrenberg, A., Sjoberg, B. M. and Thelander, L., 1987, “Magnetic interaction between the tyrosyl free-radical and the anti-ferromagnetically coupled iron center in ribonucleotide reductase” Biochemistry 26, 5541–5548.PubMedCrossRefGoogle Scholar
  83. Schiller, H., Dittmer, J., Iuzzolino, L., Dorner, W., Meyer-Klaucke, W., Sole, V. A., Notting, H. F. and Dau, H., 1998, “Structure and orientation of the oxygen-evolving manganese complex of green algae and higher plants investigated by x-ray absorption linear dichroism spectroscopy on oriented photosystem II membrane particles” Biochemistry 37, 7340–7350.CrossRefGoogle Scholar
  84. Shigemori, K., Hara, H., Kawamori, A. and Akabori, K., 1998, “Determination of distances from tyrosine D to QA and chlorophyllz in photosystem II studied by ‘2+1’ pulsed EPR” Biochim. Biophys. Acta 1363, 187–198.PubMedCrossRefGoogle Scholar
  85. Smigel, M. D., Dalton, L. A. and Dalton, L. R., 1974, “Very slowly tumbling spin labels–Saturation recovery” Chem. Phys. 6 183–192.CrossRefGoogle Scholar
  86. Smith, I. D. and Pilbrow, J. R., 1974, “The determination of structural properties of dimeric transition metal ion complexes from EPR spectra” Coord. Chem. Rev. 13 173–278.CrossRefGoogle Scholar
  87. Stevenson, R. C., Sands, R. H., Singer, T. P. and Beinert, H., 1986, “Studies on the spin-spin interaction between flavin and iron-sulfur cluster in an iron-sulfur flavoprotein” Biochim. Biophys. Acta 869, 81–88.PubMedCrossRefGoogle Scholar
  88. Stewart, D. H. and Brudvig, G. W., 1998, “Cytochrome b 559 of photosystem II” Biochim. Biophys. Acta 1367, 63–87.PubMedCrossRefGoogle Scholar
  89. Stewart, D. H., Cua, A., Chisholm, D. A., Diner, B. A., Bocian, D. F. and Brudvig, G. W., 1998, “Identification of histidine 118 in the D1 polypeptide of photosystem II as the axial ligand to chlorophyll Z” Biochemistry 37, 10040–10046.PubMedCrossRefGoogle Scholar
  90. Styring, S. A. and Rutherford, A. W., 1988, “The microwave power saturation of SII slow varies with the redox state of the oxygen-evolving complex in photosystem II” Biochemistry 27, 4915–4923.CrossRefGoogle Scholar
  91. Svensson, B., Etchebest, C., Tuffery, P., van Kan, P., Smith, J. and Styring, S., 1996, “A model for the photosystem II reaction center core including the structure of the primary donor P680+” Biochemistry 35, 14486–14502:Google Scholar
  92. Szalai, V. A. and Brudvig, G. W., 1996, “Formation and decay of the S3 EPR signal species in acetate-inhibited photosystem II” Biochemistry 35, 1946–1953.PubMedCrossRefGoogle Scholar
  93. Szalai, V. A., Kühne, H., Lakshmi, K. V. and Brudvig, G. W., 1998a, “Characterization of the interaction between manganese and tyrosine Z in acetate-inhibited photosystem II” Biochemistry 37, 13594–13603.PubMedCrossRefGoogle Scholar
  94. Szalai, V. A., Stone, D. A. and Brudvig, G. W., 1998b, in Photosynthesis: Mechanisms and Effects (Garab, G., Ed.) Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1403–1406.Google Scholar
  95. Tan, X. L., Gultneh, Y., Sarneski, J. E. and Scholes, C. P., 1991, “EPR-ENDOR of the electronic-structure from two nitrogenously ligated Bis(Mu-Oxo)-MnIII-MnIV model complexes spectroscopically relevant to the multi-manganese center of photosystem II” J. Amer. Chem. Soc. 113, 7853–7858.CrossRefGoogle Scholar
  96. Tang, X.-S., Randall, D. W., Force, D. A., Diner, B. A. and Britt, R. D., 1996, “Manganesetyrosine interaction in the photosystem II oxygen-evolving complex” J. Amer. Chem. Soc. 118, 7638–7639.CrossRefGoogle Scholar
  97. Un, S., Brunel, L.-C., Brill, T. M., Zimmermann, J.-L. and Rutherford, A. W., 1994, “Angular orientation of the stable tyrosyl radical within photosystem II by high-field 245GHz electron-paramagnetic-resonance” Proc. Natl. Acad. Sci. USA 91, 5262–5266.PubMedCentralPubMedCrossRefGoogle Scholar
  98. Yachandra, V. K., Sauer, K. and Klein, M. P., 1996, “Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen” Chem. Rev. 96, 2927–2950.PubMedCrossRefGoogle Scholar
  99. Yoshii, T., Kawamori, A., Tonaka, M. and Akabori, K., 1999, “Relative positions of electron transfer components in photosystem II studied by ‘2+1’ pulsed electron paramagnetic resonance: Y-D and Q(A)” Biochim. Biophys. Acta 1413, 43–49.CrossRefGoogle Scholar
  100. Zheng, M. and Dismukes, G. C., 1996, “Orbital configuration of the valence electrons, ligand field symmetry, and manganese oxidation states of the photosynthetic water oxidizing complex: Analysis of the S2 state multiline EPR signals” Inorg. Chem. 35, 3307–3319.PubMedCrossRefGoogle Scholar

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© Kluwer Academic / Plenum Publishers, New York 2002

Authors and Affiliations

  • K. V. Lakshmi
    • 1
  • Gary W. Brudvig
    • 1
  1. 1.Department of ChemistryYale UniversityNew HavenUSA

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