Abstract
Manganese in the oxygen-evolving complex is a physiological electron donor to Photosystem II. PS II depleted of manganese may oxidize exogenous reductants including benzidine and Mn2+. Using flash photolysis with electron spin resonance detection, we examined the room-temperature reaction kinetics of these reductants with Yz +, the tyrosine radical formed in PS II membranes under illumination. Kinetics were measured with membranes that did or did not contain the 33 kDa extrinsic polypeptide of PS II, whose presence had no effect on the reaction kinetics with either reductant. The rate of Yz + reduction by benzidine was a linear function of benzidine concentration. The rate of Yz + reduction by Mn2+ at pH 6 increased linearly at low Mn2+ concentrations and reached a maximum at the Mn2+ concentrations equal to several times the reaction center concentration. The rate was inhibited by K+, Ca2+ and Mg2+. These data are described by a model in which negative charge on the membrane causes a local increase in the cation concentration. The rate of Yz + reduction at pH 7.5 was biphasic with a fast 400 μs phase that suggests binding of Mn2+ near Yz + at a site that may be one of the native manganese binding sites.
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Abbreviations
- PS II:
-
Photosystem II
- YD :
-
tyrosine residue in Photosystem II that gives rise to the stable Signal II EPR spectrum
- Yz :
-
tyrosine residue in Photosystem II that mediates electron transfer between the reaction center chlorophyll and the site of water oxidation
- ESR:
-
electron spin resonance
- DPC:
-
diphenylcarbazide
- DCIP:
-
dichlorophenolindophenol
References
Amesz J (1983) The role of manganese in photosynthetic oxygen evolution. Biochim Biophys Acta 726: 1–12
Andréasson LE and Vänngård (1988) Electron transport in Photosystems I and II. Ann Rev Plant Physiol Plant Mol Biol 39: 379–411
Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, McIntosh L, Sithole I and Yocum CF (1989) Water oxidation in Photosystem II: from radical chemistry to multielectron chemistry. Biochemistry, submitted
Babcock GT (1987) The photosynthetic oxygen-evolving process. In: Amesz J (ed) New Comprehensive Biochemistry: Photosynthesis, pp 125–158. Amsterdam: Elsevier
Babcock GT and Sauer K (1975) Two electron donation sites for exogenous reductants in chloroplast Photosystem II. Biochim Biophys Acta 396: 48–62
Barber J (1980) Membrane surface charges and potentials in relation to photosynthesis. Biochim Biophys Acta 594: 253–308
Barry BA and Babcock GT (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 84: 7099–7103
Ben-Hayyim G and Avron M (1970) Mn2+ as electron donor in isolated chloroplasts. Biochim Biophys Acta 205: 86–94
Berthold D, Babcock GT and Yocum CF (1981) A highly resolved oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234
Blankenship R (1975) The role of manganese in photosynthetic oxygen evolution. PhD dissertation, University of California, Berkeley
Callahan P, Ellis F and Cheniae G (1985) Studies on the photoactivation of the water-oxidizing enzyme. Plant Physiol 79: 777–786
Casey JL and Sauer K (1984) EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochim Biophys Acta 767: 21–28
Conjeaud H and Mathis P (1986) Electron transfer in the photosynthetic membrane. Influence of pH and surface potential on the P-680 reduction kinetics. Biophys J 49: 1215–1221
Cotton FA and Wilkinson G (1967) Advanced Inorganic Chemistry. New York: Wiley and Sons, New York
Debus RJ, Barry BA, Babcock GT and McIntosh L (1988) Site-directed mutagenesis identifies a tyrosine radical involved in photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430
Debus RJ, Barry BA, Sithole I, Babcock GT and McIntosh L (1988) Directed mutagenesis indicates that the donor to P680 + in the Photosystem II is tyrosine-161 of the D1 polypeptide. Biochem 27: 9071–9074
Dismukes GC and Siderer Y (1981) Intermediates of polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–278
George GN, Prince RC and Cramer SP (1989) The manganese site of the photosynthetic water-splitting enzyme. Science 243: 789–791
Ghanotakis DF, Babcock GT and Yocum CF (1984) Structural and catalytic properties of the oxygen-evolving complex. Biochim Biophys Acta 765: 388–398
Hansson O, Aasa R and Vänngaård T (1987) The origin of the multiline and g=4.1 electron paramagnetic resonance signal from the oxygen-evolving system of Photosystem II. Biophys J 51: 825–832
Helfferich F (1962) Ion exchange, pp 158–159. New York: McGraw-Hill
Hoganson CW and Babcock GT (1988) Electron-transfer events near the reaction center in O2-evolving Photosystem II preparations. Biochemistry 27: 5848–5855
Hsu B-H, Lee J-Y and Pan R-L (1987) The high-affinity binding site for manganese in the oxidizing side of Photosytem II. Biochim Biophys Acta 890: 89–96
Inoue H, Akahor H and Noguchi M (1987) Activation of electron donation from hydrogen peroxide by manganese in nonoxygen evolving Photosystem II particles. Plant Cell Physiol 28: 1339–1343
Inoue H and Wada T (1987) Requirement of manganese for electron donation of hydrogen peroxide in Photosystem II reaction center complex. Plant Cell Physiol 28: 767–773
Izawa S (1970) Photoreduction of 2,6-dichlorophenolindophenol by chloroplasts with exogenous Mn2+ as electron donor. Biochim Biophys Acta 197: 328–331
Klimov VV, Allakhverdiev SI, Shuvalov VA and Krasnovsky AA (1982) Effect of extraction and re-addition of manganese on light reactions of Photosystem-II preparations. FEBS Lett 148: 307–312
Ono T-A and Inoue Y (1983) Requirement of divalent cations for photoactivation of the latent water-oxidation system in intact chloroplasts from flashed leaves. Biochim Biophys Acta 723: 191–201
Penner-Hahn JE, Fronko RM, Pecoraro VL, Yocum, CF, Betts SD and Bowlby NR (1989) Structural characterization of the Mn sites in the photosynthetic oxygen-evolving complex using X-ray absorption spectroscopy. J Am Chem Soc, in press
Radmer R and Cheniae G (1977) Mechanisms of oxygen-evolution. In: Barber J (ed) Primary Processes in Photosynthesis, Vol. 2, pp 301–348. Amsterdam, New York: Elsevier
Sauer K, Guiles RD, McDermott AE, Cole JL, Yachandra VK, Zimmerman J-L, Klein MP, Dexheimer SL and Britt RD (1988) Spectroscopic studies of manganese involvement in photosynthetic oxygen evolution. Chemica Scripta 28A: 87–91
Stewart AC and Bendall DS (1981) Properties of oxygen-evolving Photosystem II particles from Phormidium laminosum, a thermophilic blue-green algae. Biochem J 194: 877–887
Tamura N and Cheniae GM (1986) Requirements for the photoligation of Mn2+ in Photosystem II membranes and the expression of water-oxidizing activity of the polynuclear Mn-catalyst. FEBS Lett 200: 231–236
Tamura N and Cheniae G (1987) Photoactivation of the wateroxidizing complex by Photosystem II membranes in VIIth International Congress on Photosynthesis (Biggins J, ed). Dordrecht: Martinus Nijhoff
Tamura N, Ikeuchi M and Inoue Y (1989) Assignment of histidine residues in the D1 protein as possible ligands for functional manganese in photosynthetic water oxidizing complex. Biochim Biophys Acta 973: 281–289
Yachandra VK, Guiles RD, McDermott A, Britt RD, Dexheimer SL, Sauer K and Klein MP (1986) The state of manganese in the photosynthetic apparatus. Biochim Biophys Acta 850: 324–332
Yerkes CT and Babcock GT (1980) Photosystem II oxidation of charged electron donors: surface charge effects Biochim Biophys Acta 590: 360–372
Yerkes CT and Babcock GT (1981) Surface charge asymmetry and a specific calcium ion effect in chloroplast Photosystem II. Biochim Biophys Acta 634: 19–29
Yerkes CT, Babcock GT and Crofts AR (1983) A tris-induced change in the midpoint potential of Z, the donor to Photosystem II, as determined by the kinetics of the back reaction. FEBS Lett 158: 359–363
Zimmerman JL and Rutherford AW (1984) EPR studies on the oxygen evolving enzyme of Photosystem II. Biochim Biophys Acta 767: 160–167
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Hoganson, C.W., Ghanotakis, D.F., Babcock, G.T. et al. Mn2+ reduces Yz + in manganese-depleted Photosystem II preparations. Photosynth Res 22, 285–293 (1989). https://doi.org/10.1007/BF00048306
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DOI: https://doi.org/10.1007/BF00048306