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Photosystem I pp 245-269 | Cite as

EPR Studies of the Primary Electron Donor P700 in Photosystem

  • Wolfgang Lubitz
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 24)

Abstract

The primary donor P700 in Photosystem I (PS I) is a heterodimer comprised of a chlorophyll a and a chlorophyll á. The electronic structure of this species, which is related to its function in vivo, can be studied by EPR techniques applied to the paramagnetic states P700+ (cation radical) and 3P700 (triplet state) of the primary donor. In the case of P700+ observables are the electronic g tensor and the electron-nuclear hyperfine and nuclear quadrupole coupling tensors; in the case of 3P700 the electron–electron dipolar coupling tensor serves as an additional probe. In this contribution, the determination of the magnetic resonance parameters by EPR techniques are described. Conclusions about the electronic structure, in particular about the spin and charge density distribution in this species, are drawn. The results are corroborated by studies of model systems and of the primary donor in genetically modified photosystem I preparations, which gives information on the effect of the protein surroundings. Emphasis is placed on a theoretical description of P700 in its various states, which is based on a comparison with molecular orbital calculations. Implications of the experimental findings for the functional properties of the primary donor in photosystem I are discussed.

Keywords

Triplet State Spin Density Primary Donor ENDOR Spectrum Spin Density Distribution 
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. Allen JP and Williams JC (1995) Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron transfer in photosynthetic reaction centers. J Bioenerg Biomembr 27: 275–283PubMedCrossRefGoogle Scholar
  2. Amesz J and Hoff AJ (eds) 1995. Biophysical Techniques in Photosynthesis. Kluwer Academic Publishers, DordrechtGoogle Scholar
  3. Angerhofer A (1991) Chlorophyll triplets and radical pairs. In: Scheer H (ed) Chlorophylls, pp 945–991. CRC Press, Boca Raton, FLGoogle Scholar
  4. Astashkin AV, Dikanov SA, Tsvetkov YD and Goldfeld MG (1987) Comparative analysis of ESE modulation from oxidized chlorophyll a and P700 centers in chloroplasts containing N-15 nuclei. Chem Phys Lett 134: 438–443CrossRefGoogle Scholar
  5. Atherton NM (1993) Principles of Electron Spin Resonance. Ellis Horwood PTR, Prentice Hall, New YorkGoogle Scholar
  6. Ben-Shem A, Frolow F and Nelson N (2003) Crystal structure of plant photosystem I. Nature 426: 630–635PubMedCrossRefGoogle Scholar
  7. Bratt PJ, Rohrer M, Krzystek J, Evans MCW, Brunel L-C and Angerhofer A (1997) Submillimeter high-field EPR studies of the primary donor in plant photosystem I P700+. J Phys Chem 101: 9686–9689Google Scholar
  8. Bratt PJ, Poluektov OG, Thurnauer MC, Krzystek J, Brunel L-C, Schrier J, Hsiao Y-W, Zerner M and Angerhofer A (2000) The g-factor anisotropy of plant chlorophyll a·+. J Phys Chem B 104: 6973–6977CrossRefGoogle Scholar
  9. Breton J (2001) Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim Biophys Acta 1507: 180–193PubMedCrossRefGoogle Scholar
  10. Breton J, Nabedryk E and Leibl W (1999) FTIR Study of the primary electron donor of photosystem I (P700) revealing delocalization of the charge in P700+ and localization of the triplet character in 3P700. Biochemistry 38: 11585–11592PubMedCrossRefGoogle Scholar
  11. Breton J, Xu W, Diner BA and Chitnis P (2002) The two histidine axial ligands of the primary electron donor chlorophylls (P700) in photosystem I are similarly perturbed upon P700+ formation. Biochemistry 41: 11200–11210PubMedCrossRefGoogle Scholar
  12. Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318: 322–373CrossRefGoogle Scholar
  13. Brettel K and Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta 1507: 100–114PubMedCrossRefGoogle Scholar
  14. Budil DE and Thurnauer MC (1991) The chlorophyll triplet state as a probe of structure and function in photosynthesis. Biochim Biophys Acta 1057: 1–41PubMedCrossRefGoogle Scholar
  15. Carbonera D, Collareta P and Giacometti G (1997) The P700 triplet state in an intact environment detected by ODMR. A well resolved triplet minus singlet spectrum. Biochim Biophys Acta 1322: 115–128CrossRefGoogle Scholar
  16. Commoner B, Heise JJ and Townsend J (1956) Light-induced paramagnetism in chloroplasts. Proc Natl Acad Sci USA 42: 710–718PubMedCrossRefGoogle Scholar
  17. Cui LY, Bingham SE, Kuhn M, Käss H, Lubitz W and Webber AN (1995) Site-directed mutagenesis of conserved histidines in the helix-VIII domain of PsaB impairs assembly of the photosystem-I reaction-center without altering spectroscopic characteristics of P-700. Biochemistry 34: 1549–1558PubMedCrossRefGoogle Scholar
  18. Datta SN, Parandekar PV and Lochan RC (2001) Identity of green plant reaction centers from quantum chemical determination of redox potentials of special pairs. J Phys Chem B 105: 1442–1451CrossRefGoogle Scholar
  19. Davis MS, Forman A and Fajer J (1979) Ligated chlorophyll cation radicals: their function in photosystem II of plant photosynthesis. Proc Natl Acad Sci USA 76: 4170–4174PubMedCrossRefGoogle Scholar
  20. Davis IH, Heathcote P, MacLachlan DJ and Evans MCW (1993) Modulation analysis of the electron-spin echo signals of in vivo oxidized primary donor N-14 chlorophyll centers in bacterial, P870 and P960, and plant photosystem-I, P700, reaction centers. Biochim Biophys Acta 1143: 183–189CrossRefGoogle Scholar
  21. Deligiannakis Y and Rutherford AW (2001) Electron spin echo envelope modulation spectroscopy in photosystem I. Biochim Biophys Acta 1507: 226–246PubMedCrossRefGoogle Scholar
  22. Dikanov SA and Tsvetkov YD (1992) Electron Spin Echo Envelope Modulation (ESEEM) Spectroscopy. CRC Press, Boca Raton, FL, USAGoogle Scholar
  23. Dikanov SA, Astashkin AV, Tsvetkov YD and Goldfeld MG (1983) Comparative modulation analysis of electron spin echo signals from oxidized chlorophyll a in vitro and P700 centres in chloroplasts. Chem Phys Lett 101: 206–210CrossRefGoogle Scholar
  24. Döring G, Bailey JL, Kreutz W, Weikard J and Witt HT (1968) The action of two chlorophyll-a| molecules in light reaction I of photosynthesis. Naturwissenschaften 55: 219–220PubMedCrossRefGoogle Scholar
  25. Dörnemann D and Senger H (1986) The structure of chlorophyll-RC-I –a chromophore of the reaction center of photosystem-I. Photochem Photobiol 43: 573–581Google Scholar
  26. Frank HA, McLean MB and Sauer K (1979) Triplet states in photosystem I of spinach chloroplasts and subchloroplast particles. Proc Natl Acad Sci USA 76:5124–5128PubMedCrossRefGoogle Scholar
  27. Fromme P, Jordan P and Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507: 5–31PubMedCrossRefGoogle Scholar
  28. Goldsmith JO, King B and Boxer SG (1996) Mg coordination by amino acid side chains is not required for assembly and function of the special pair in bacterial photosynthetic reaction centers. Biochemistry 35: 2421–2428PubMedCrossRefGoogle Scholar
  29. Hastings G, Ramesh VM, Wang R, Sivakumar V and Webber A (2001) Primary donor photo-oxidation in photosystem I: a re-evaluation of (P700(+) − P700) Fourier transform infrared difference spectra. Biochemistry 40: 12943–12949PubMedCrossRefGoogle Scholar
  30. Hoff AJ (1979) Applications of ESR in photosynthesis. Phys Rep 54: 75–200CrossRefGoogle Scholar
  31. Hoff AJ (1996) Optically detected magnetic resonance (ODMR) of triplet states in Photosynthesis. In: Amesz J and Hoff AJ (eds) Biophysical Techniques in Photosynthesis, Advances in Photosynthesis, Vol 3, pp 277–295. Kluwer, DordrechtGoogle Scholar
  32. Huber M, Lendzian F, Lubitz W, Tränkle E, Möbius K and Wasielewski MR (1986) ENDOR and triple resonance in solutions of the chlorophyll-a and bis(chlorophyll)cyclophane radical cations. Chem Phys Lett 132: 467–473CrossRefGoogle Scholar
  33. Hyde JS and Rist GH (1968) Endor of methyl, matrix, and α protons in amorphous and polycrystalline matrices. J Phys Chem B 72: 4269–4276CrossRefGoogle Scholar
  34. Johnson ET, Müh F, Nabedryk E, Williams JC, Allen JP, Lubitz W, Breton J and Parson WW (2002) Electronic and vibronic coupling of the special pair of bacteriochlorophylls in photosynthetic reaction centers from wild-type and mutant strains of Rhodobacter sphaeroides. J Phys Chem B 106: 11859–11869CrossRefGoogle Scholar
  35. Jordan R, Fromme P, Witt HT, Klukas O, Saenger W and Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411: 909–917PubMedCrossRefGoogle Scholar
  36. Käss H (1995) Die Struktur des primären Donators P700 in photosystem I: Untersuchungen mit Methoden der stationären und gepulsten Elektronspinresonanz. Dissertation. Technische Universität BerlinGoogle Scholar
  37. Käss H and Lubitz W (1996) Evaluation of 2D-ESEEM data of N-15-labeled radical cations of the primary donor P-700 in photosystem I and chlorophyll a. Chem Phys Lett 251: 193–203CrossRefGoogle Scholar
  38. Käss H, Bittersmann-Weidlich E, Andréasson L-E, Bönigk B and Lubitz W (1995) ENDOR and ESEEM of the N-15 labelled radical cations of chlorophyll-a and the primary donor P-700 in photosystem-I. Chem Phys Lett 194: 419–432Google Scholar
  39. Käss H, Fromme P and Lubitz W (1996) Quadrupole parameters of nitrogen nuclei in the cation radical P700·+ determined by ESEEM of single crystals of photosystem I. Chem Phys Lett 257: 197–206CrossRefGoogle Scholar
  40. Käss H, Lubitz W, Hartwig G, Scheer H, Noy D and Scherz A (1998) ENDOR studies of substituted chlorophyll cation radicals. Spectrochim Acta 54A: 1141–1156Google Scholar
  41. Käss H, Fromme P, Witt HT and Lubitz W (2001) Orientation and electronic structure of the primary donor radical cation P−700·+ in photosystem I: a single crystals EPR and ENDOR study. J Phys Chem B 105: 1225–1239CrossRefGoogle Scholar
  42. Klette R, Törring JT, Plato M, Möbius K, Bönigk B and Lubitz W (1993) Determination of the g tensor of the primary donor cation radical in single-crystals of Rhodobacter-sphaeroides R-26 reaction centers by 3-mm high-field EPR. J Phys Chem 97: 2015–2020CrossRefGoogle Scholar
  43. Kobayashi M, Watanabe T, Nakazato M, Ikegami I, Hiyama T, Matsunaga T and Murata N (1988) Chlorophyll a/P-700 and pheophytin a/P-680 stoichiometries in higher plants and cyanobacteria determined by HPLC analysis. Biochim Biophys Acta 936: 81–89CrossRefGoogle Scholar
  44. Kok B (1956) On the reversible absorption change at 705 mμ in photosynthetic organisms. Biochim Biophys Acta 22: 399–401PubMedCrossRefGoogle Scholar
  45. Kok B (1957) Absorption changes induced by the photochemical reaction of photosynthesis. Nature 179: 583–584CrossRefGoogle Scholar
  46. Kok B (1961) Partial purification and determination of oxidation reduction potential of photosynthetic chlorophyll complex absorbing at 700 mμ. Biochim Biophys Acta 48: 527–533PubMedCrossRefGoogle Scholar
  47. Krabben L, Schlodder E, Jordan R, Carbonera D, Giacometti G, Lee H, Webber AN and Lubitz W (2000) Influence of the axial ligands on the spectral properties of P700 of photosystem I: a study of site-directed mutants. Biochemistry 39: 13012–13025PubMedCrossRefGoogle Scholar
  48. Kurreck H, Kirste B and Lubitz W (1988) Electron Nuclear Double Resonance Spectroscopy of Radicals in Solution –Applications to Organic and Biological Chemistry. VCH Publishers, Inc., Deerfield Beach, FloridaGoogle Scholar
  49. Labahn A and Huber C (2001) The g-tensor anisotropy of the triplet state of the primary electron donor in the photosynthetic bacterium Rhodobacter sphaeroides by high-field (95 GHz) EPR. Appl Magn Reson 21: 381–387Google Scholar
  50. Lendzian F (1982) Elektron-Kern-Mehrfachresonanz an Primärprodukten der Photosynthese. Dissertation. Technische Universität BerlinGoogle Scholar
  51. Lendzian F, Huber M, Isaacson RA, Endeward B, Plato M, Bönigk B, Möbius K, Lubitz W and Feher G (1993) The electronic-structure of the primary donor cation-radical in Rhodobacter-sphaeroides R-26 –ENDOR and triple-resonance studies in single-crystals of reaction centers. Biochim Biophys Acta 1183: 139–160CrossRefGoogle Scholar
  52. Lubitz W (1991) EPR and ENDOR studies of chlorophyll cation and anion radicals. In: Scheer H (ed) Chlorophylls, pp 903–944. CRC Press, Inc., Boca Raton, FLGoogle Scholar
  53. Lubitz W and Lendzian F (1996) ENDOR spectroscopy. In: Amesz J and Hoff AJ (eds) Biophysical Techniques in Photosynthesis, Advances in Photosynthesis, Vol 3, pp 255–275. Kluwer, DordrechtGoogle Scholar
  54. Lucken EAC (1969) Nuclear Quadrupole Couplings Constants. Academic Press, LondonGoogle Scholar
  55. Mac M, Tang X-S, Diner BA, McCracken J and Babcock GT (1996) Identification of histidine as an axial ligand to P700·+. Biochemistry 35: 13288–13293PubMedCrossRefGoogle Scholar
  56. Mac M, Bowlby NR, Babcock GT and McCracken J (1998) Monomeric spin density distribution in the primary donor of photosystem I as determined by electron magnetic resonance: functional and thermodynamic implications. J Am Chem Soc 120: 13215–13223CrossRefGoogle Scholar
  57. Mattioli TA, Lin X, Allen JP and Williams JC (1995) Correlation between multiple hydrogen-bonding and alteration of the oxidation potential of the bacteriochlorophyll dimer of reaction centers from Rhodobacter sphaeroides. Biochemistry 34: 6142–6152PubMedCrossRefGoogle Scholar
  58. Möbius K and Lubitz W (1987) ENDOR Spectroscopy in Photobiology and Biochemistry. In: Berliner LJ and Reuben J (eds) Biological Magnetic Resonance, Vol 7, pp 129–247. Plenum Press, New YorkGoogle Scholar
  59. Möbius K and Plato M (1996) Structure information on the bacterial primary donor P·+, acceptor QA ·−, and radical Pair P·+QA ·− as obtained from high-field EPR/ENDOR and MO studies. In: Michel-Beyerle MB (ed) The Reaction Center of Photosynthetic Bacteria, pp 63–80. Springer-Verlag, Berlin, Heidelberg, New YorkGoogle Scholar
  60. Müh F, Schulz C, Schlodder E, Jones MR, Rautter J, Kuhn M and Lubitz W (1998) Effects of zwitterionic detergents on the electronic structure of the primary donor and the charge recombination kinetics of P+QA in native and mutant reaction centers from Rhodobacter sphaeroides. Photosynth Res 55: 199–205CrossRefGoogle Scholar
  61. Müh F, Gardiner AT, Witt H, Schulz C, Imhoff JF, Cogdell RJ and Lubitz W (2001) Conserved electronic structure of the primary donor in reaction centers of sulfur and non-sulfur purple bacteria. Proceedings of the 12th International Congress on Photosynthesis, Brisbane, Australia. CSIRO Publishing (S7-005)Google Scholar
  62. Müh F, Lendzian F, Roy M, Williams JC, Allen JP and Lubitz W (2002) Pigment–protein interactions in bacterial reaction centers and their influence on oxidation potential and spin density distribution of the primary donor. J Phys Chem B 106: 3226–3236CrossRefGoogle Scholar
  63. Müller M, Niklas J, Lubitz W and Holzwarth AR (2003) Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in photosystem I. Biophys J 85: 3899–3822PubMedGoogle Scholar
  64. Nakamura A and Watanabe T (1998) HPLC determination of photosynthetic pigments during greening of etiolated barley leaves. FEBS Lett 426: 201–204PubMedCrossRefGoogle Scholar
  65. Norris JR, Uphaus RA, Crespi HL and Katz JJ (1971) Electron spin resonance of chlorophyll and origin of signal-I in photosynthesis. Proc Natl Acad Sci USA 68: 625–628PubMedCrossRefGoogle Scholar
  66. Norris JR, Scheer H and Katz JJ (1975) Models for antenna and reaction center chlorophylls. Ann NY Acad Sci 244: 260–280PubMedCrossRefGoogle Scholar
  67. O’Malley PJ (2000) The effect of oxidation and reduction of chlorophyll a on its geometry, vibrational and spin density properties as revealed by hybrid density functional methods. J Am Chem Soc 122: 7798–7801CrossRefGoogle Scholar
  68. O’Malley PJ and Babcock GT (1984) Electron nuclear double resonance evidence supporting a monomeric nature for P700·+ in spinach chloroplasts. Proc Natl Acad Sci USA 81: 1098–1101PubMedCrossRefGoogle Scholar
  69. O’Malley PJ and Collins SJ (2001) The effect of axial Mg ligation on the geometry and spin density distribution of chlorophyll cation free radical models: a density functional study. J Am Chem Soc 123: 11042–11046PubMedCrossRefGoogle Scholar
  70. Parson WW, Nabedryk E, and Breton J (1992) Mid- and near-IR electronic transitions of P·+: new probes of resonance interactions and structural asymmetry in reaction centers. In: Breton J and Verméglio A (eds) The Photosynthetic Bacterial Reaction Center II, pp 79–88. Plenum Press, New YorkGoogle Scholar
  71. Pashenko SV, Gast P and Hoff AJ (2001) A D-band (130 GHz) EPR study of the primary electron donor triplet state in photosynthetic reaction centers of Rhodobacter sphaeroides R26. Appl Magn Reson 21: 325–334CrossRefGoogle Scholar
  72. Pashenko SV, Proskuryakov II, Germano M, van Gorkom HJ and Gast P (2003) Triplet state in photosystem II reaction centers as studied by 130 GHz EPR. Chem Phys 294: 439–449CrossRefGoogle Scholar
  73. Petrenko A, Maniero AL, van Tol J, MacMillan F, Li Y, Brunel L-C and Redding K (2004) A high-field EPR study of P700·+ in wild-type and mutant photosystem I from Chlamydomonas reinhardtii. Biochemistry 43: 1781–1786PubMedCrossRefGoogle Scholar
  74. Plato M and Möbius K (1995) Structural characterization of the primary donor in photosynthetic bacteria by its electronic g-tensor. Chem Phys 197: 289–295CrossRefGoogle Scholar
  75. Plato M, Lubitz W, Lendzian F and Möbius K (1988a) Magnetic resonance and molecular orbital studies of the primary donor cation radical P960·+ in the photosynthetic bacterium Rhodopseudomonas viridis. Isr J Chem 28: 109–119Google Scholar
  76. Plato M, Möbius K, Michel-Beyerle MB, Bixon M and Jortner J (1988b) Intermolecular electronic interactions in the primary charge separation in bacterial photosynthesis. J Am Chem Soc 110: 7279–7285CrossRefGoogle Scholar
  77. Plato M, Möbius K, and Lubitz W (1991) Molecular orbital calculations on chlorophyll radical ions. In: Scheer H (ed) Chlorophylls, pp 1015–1046. CRC Press Inc., Boca Raton, FLGoogle Scholar
  78. Plato M, Lendzian F, Lubitz W, and Möbius K (1992) Molecular orbital study of electronic asymmetry in primary donors of bacterial reaction centers. In: Breton J and Verméglio A (eds) The Photosynthetic Bacterial Reaction Center II, pp 109–118. Plenum Press, New YorkGoogle Scholar
  79. Plato M, Krauß N, Fromme P and Lubitz W (2003) Molecular orbital study of the primary electron donor P700 of photosystem I based on a recent X-ray single crystal structure analysis. Chem Phys 294: 483–499CrossRefGoogle Scholar
  80. Poluektov OG, Utschig LM, Schlesselman SL, Lakshmi KV, Brudvig GW, Kothe G and Thurnauer MC (2002) Electronic structure of the P700 special pair from high-frequency electron paramagnetic resonance spectroscopy. J Phys Chem B 106: 8911–8916CrossRefGoogle Scholar
  81. Prisner T, McDermott AE, Un S, Norris JR, Thurnauer MC and Griffin RG (1993) Measurement of the g-tensor of the P700·+ signal from deuterated cyanobacterial photosystem-I particles. Proc Natl Acad Sci USA 90: 9485–9788PubMedCrossRefGoogle Scholar
  82. Rautter J, Lendzian F, Schulz C, Fetsch A, Kuhn M, Lin X, Williams JC, Allen JP and Lubitz W (1995) ENDOR studies of the primary donor cation-radical in mutant reaction centers of Rhodobacter sphaeroides with altered hydrogen-bond interactions. Biochemistry 34: 8130–8143PubMedCrossRefGoogle Scholar
  83. Redding K, MacMillan F, Leibl W, Brettel K, Hanley J, Rutherford AW, Breton J and Rochaix J-D (1998) A systematic survey of conserved histidines in the core subunits of photosystem I by site-directed mutagenesis reveals the likely axial ligands of P700. EMBO J. 17: 50–60PubMedCrossRefGoogle Scholar
  84. Reimers JR and Hush NS (2004) A unified description of the electrochemical, charge distribution, and spectroscopic properties of the special-pair radical cation in bacterial photosynthesis. J Am Chem Soc 126: 4132–4144PubMedCrossRefGoogle Scholar
  85. Rigby SEJ, Nugent JHA and O’Malley PJ (1994) ENDOR and special triple resonance studies of chlorophyll cation radicals in photosystem 2. Biochemistry 33: 10043–10050PubMedCrossRefGoogle Scholar
  86. Rigby SEJ, Evans MCW and Heathcote P (2001) Electron nuclear double resonance (ENDOR) spectroscopy of radicals in photosystem I and related type I photosynthetic reaction centres. Biochim Biophys Acta 1507: 247–259PubMedCrossRefGoogle Scholar
  87. Rutherford AW and Sétif P (1990) Orientation of P700, the primary electron-donor of photosystem I. Biochim Biophys Acta 1019: 128–132CrossRefGoogle Scholar
  88. Scheer H, Katz JJ and Norris JR (1977) Proton–electron hyperfine coupling constants of the chlorophyll a cation radical by ENDOR spectroscopy. J Am Chem Soc 99: 1372–1381CrossRefGoogle Scholar
  89. Schweiger A and Jeschke G (2001) Principles of Pulse Electron Paramagnetic Resonance. Oxford University Press, OxfordGoogle Scholar
  90. Sieckmann I, Brettel K, Bock H, van der Est A and Stehlik D (1993) Transient electron paramagnetic resonance of the triplet state of P700 in photosystem I. Evidence for triplet delocalization at room temperature. Biochemistry 32: 4842–4847PubMedCrossRefGoogle Scholar
  91. Sinnecker S, Koch W and Lubitz W (2002) Chlorophyll a radical ions: a density functional study. J Phys Chem B 106: 5281–5288CrossRefGoogle Scholar
  92. Stehlik D and Möbius K (1997) New EPR methods for investigating photoprocesses with paramagnetic intermediates. Annu Rev Phys Chem 48: 745–784PubMedCrossRefGoogle Scholar
  93. Stone AJ (1963a) g-Factors of aromatic free radicals. Mol Phys 6: 509–515CrossRefGoogle Scholar
  94. Stone AJ (1963b) Gauge invariance of g-tensor. Proc R Soc Lond A 271: 424–424CrossRefGoogle Scholar
  95. Sun Y, Wang H, Zhao F and Sun J (2004) The effect of axial Mg2 + ligation and peripheral hydrogen bonding on chlorophyll a. Chem Phys Lett 387: 12–16CrossRefGoogle Scholar
  96. Thurnauer MC, Katz JJ and Norris JR (1975) The triplet state in bacterial photosynthesis: possible mechanisms of the primary photo-act. Proc Natl Acad Sci USA 72:3270–3274PubMedCrossRefGoogle Scholar
  97. Vrieze J, Gast P and Hoff AJ (1996) Structure of the reaction center of photosystem I of plants. An investigation with linear-dichroic absorbance-detected magnetic resonance. J Phys Chem 100: 9960–9967CrossRefGoogle Scholar
  98. Wang R, Sivakumar V, Li Y, Redding K and Hastings G (2003) Mutation induced modulation of hydrogen bonding to P700 studied using FTIR difference spectroscopy. Biochemistry 42: 9889–9897PubMedCrossRefGoogle Scholar
  99. Wasielewski MR, Norris JR, Crespi HL and Harper J (1981a) Photoinduced ESR signals from the primary electron donors in deuterated highly 13C enriched photosynthetic bacteria and algae. J Am Chem Soc 103: 7664–7665CrossRefGoogle Scholar
  100. Wasielewski MR, Norris JR, Shipman LL, Lin C-P and Svec WA (1981b) Monomeric chlorophyll a enol: evidence for its possible role as the primary electron donor in photosystem I of plant photosynthesis. Proc Natl Acad Sci USA 78: 2957–2961CrossRefGoogle Scholar
  101. Watanabe T and Kobayashi M (1991) Electrochemistry of chlorophylls. In: Scheer H (ed) Chlorophylls, pp 287–315. CRC Press Inc., Boca Raton, FLGoogle Scholar
  102. Webber AN and Lubitz W (2001) P700: the primary electron donor of photosystem I. Biochim Biophys Acta 1507: 61–79PubMedCrossRefGoogle Scholar
  103. Webber AN, Su H, Bingham SE, Käss H, Krabben L, Kuhn M, Jordan R, Schlodder E and Lubitz W (1996) Site-directed mutations affecting the spectroscopic characteristics and midpoint potential of the primary donor in photosystem I. Biochemistry 35: 12857–12863PubMedCrossRefGoogle Scholar
  104. Witt H, Müller A and Rumberg B (1961) Oxidized cytochrome and chlorophyll in photosynthesis. Nature 192: 967–969PubMedCrossRefGoogle Scholar
  105. Witt H, Schlodder E, Teutloff C, Niklas J, Bordignon E, Carbonera D, Kohler S, Labahn A and Lubitz W (2002) Hydrogen bonding to P700: site-directed mutagenesis of threonine A739 of photosystem I in Chlamydomonas reinhardtii. Biochemistry 41: 8557–8569PubMedCrossRefGoogle Scholar
  106. Witt H, Bordignon E, Carbonera D, Dekker JP, Karapetyan N, Teutloff C, Webber A, Lubitz W and Schlodder E (2003) Species specific differences of the spectroscopic properties of P700 –analysis of the influence of non-conserved amino acid residues investigated by site-directed mutagenesis of photosystem I from Chlamydomonas reinhardtii. J Biol Chem 278: 46760–46771PubMedCrossRefGoogle Scholar
  107. Zech S, Hofbauer W, Kamlowski A, Fromme P, Stehlik D, Lubitz W and Bittl R (2000) A structural model for the charge separated state P700·+A1 ·− in photosystem I from the orientation of the magnetic interaction tensors. J Phys Chem B 104: 9728–9739CrossRefGoogle Scholar
  108. Zeng RH, van Tol J, Deal A, Frank HA and Budil DE (2003) Temperature dependence of the primary donor triplet state g-tensor in photosynthetic reaction centers of Rhodobacter sphaeroides R-26 observed by transient 240 GHz electron paramagnetic resonance. J Phys Chem B 107: 4624–4631CrossRefGoogle Scholar

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© Springer 2006

Authors and Affiliations

  • Wolfgang Lubitz
    • 1
  1. 1.Max-Planck-Institut fÜr Bioanorganische ChemieMÜlheim an der RuhrGermany

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