Abstract
The dark incubation at room temperature of photosystem II (PS II) membrane fragments in a chloride-free medium at pH 6.3 slowly leads to large chloride-restorable and non-restorable O2 evolution activity losses with time as compared with control samples incubated in the presence of 10 mM NaCl. The chloride requirement in O2 evolution generated under these conditions reveals a complex interplay among various experimental parameters, including the source of the plant material, the times of incubation, the sample concentration, the chloride concentration, as well as those treatments which are believed to specifically displace chloride from PS II such as alkaline pH pretreatment and Na2SO4 addition. The results indicate that secondary, structural changes within the PS II complex are an important factor in determining the influence of chloride on the O2 evolution activity and raise the question whether or not chloride ions actually play a direct cofactor role in the water-oxidizing reactions leading to O2 evolution.
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Abbreviations
- Chl:
-
chlorophyll
- EPR:
-
electron paramagnetic resonance
- MES:
-
2-(N-morpholino) ethanesulfonic acid
- NMR:
-
nuclear magnetic resonance
- PS II:
-
photosystem II
References
Babcock GT (1987) The photosynthetic oxygen-evolving process. In: Amesz J (ed) New Comprehensive Biochemistry, Photosynthesis, Vol 15, pp 125–158. Elsevier, Amsterdam
Baianu IC, Critchley C, Govindjee and Gutowsky HS (1984) NMR study of chloride ion interactions with thylakoid membranes. Proc Natl Acad Sci (USA) 81: 3713–3717
Beck WF and Brudvig GW (1988) Ligand-substitution reactions of the oxygen-evolving center of photosystem II. Chemica Scripta 28A: 93–98
Coleman WJ and Govindjee (1987) A model for the mechanism of chloride activation of oxygen evolution in photosystem II. Photosynth Res 13: 199–223
Coleman WJ, Govindjee and Gutowsky HS (1987a) 35Cl-NMR measurement of chloride binding to the oxygen-evolving complex of spinach photosystem II. Biochim Biophys Acta 894: 443–452
Coleman WJ, Govindjee and Gutowsky HS (1987b) The location of the chloride binding sites in the oxygen-evolving complex of spinach photosystem II. Biochim Biophys Acta 894: 453–459
Coleman WJ, Govindjee and Gutowsky HS (1988) The effect of chloride on the thermal inactivation of oxygen evolution. Photosynth Res 16: 261–276
Critchley C (1985) The role of chloride in photosystem II. Biochim Biophys Acta 811: 33–46
Critchley C and Sargeson AM (1984) A manganese-chloride cluster as the functional centre of the oxygen-evolving enzyme in photosynthetic systems. FEBS Lett 177: 2–5
Damoder R, Klimov VV and Dismukes GC (1986) The effect of Cl− depletion and X- reconstitution on the oxygen-evolution rate, the yield of the multiline manganese EPR signal and EPR signal II in the isolated photosystem II complex. Biochim Biophys Acta 848: 378–391
Dismukes CG (1986) The metal centers of the photosynthetic oxygen-evolving complex. Photochem Photobiol 43: 99–115
Forsén S and Lindman B (1981) Ion binding in biological systems as studied by NMR spectroscopy. In: Glick D (ed) Methods of Biochemical Analysis, Vol 27, pp 289–486. John Wiley & Sons, New York
Franzén L-G, Hansson Ö and Andréasson L-E (1985) The roles of the extrinsic subunits in photosystem II as revealed by EPR. Biochim Biophys Acta 808: 171–179
Hansson Ö and Wydrzynski T (1990) Current perceptions of photosystem II. Photosynth Res 23: 131–162
Hind G, Nakatani HY and Izawa S (1969) The role of chloride in photosynthesis: I. The chloride requirement of electron transport. Biochim Biophys Acta 172: 277–289
Homann PH (1985) The association of functional anions with the oxygen-evolving center of chloroplasts. Biochim Biophys Acta 809: 311–319
Homann PH (1986) The relation between the chloride status of the photosynthetic water-splitting complex and the inhibitory effectiveness of amines. Photosynth Res 10: 497–503
Homann PH (1987) The relations between the chloride, calcium and polypeptide requirements of photosynthetic water oxidation. J Bioenerg Biomembr 19: 105–123
Homann PH (1988a) Chloride relations of photosystem II membrane preparations depleted of, and reconstituted with, their 17 and 23 kDa extrinsic polypeptides. Photosynth Res 15: 205–220
Homann PH (1988b) Structural effects of chloride and other anions on the water-oxidizing complex of chloroplast photosystem II. Plant Physiol 88: 194–199
Homann PH (1988c) The chloride and calcium requirement of photosynthetic water oxidation: Effects of pH. Biochim Biophys Acta 934: 1–13
Homann PH, Gleiter H, Ono T and Inoue Y (1986) Storage of abnormal oxidants in photosynthetic water oxidases inhibited by chloride removal. Biochim Biophys Acta 850: 10–20
Itoh S and Uwano S (1986) Characteristics of the chloride action site in the oxygen-evolving reaction in photosystem II particles: Electrostatic interactions with ions. Plant Cell Physiol 27: 25–36
Itoh S, Yerkes CT, Koike H, Robinson HH and Crofts AR (1984) Effects of chloride depletion on electron donation from the water-oxidizing complex to the photosystem II reaction center as measured by microsecond rise of chlorophyll fluorescence in isolated pea chloroplasts. Biochim Biophys Acta 766: 612–622
Kok B, Forbush B and McGloin M (1970) Cooperation of charges in photosynthetic oxygen evolution: I. A linear four step mechanism. Photochem Photobiol 11: 457–475
Muallem A, Farineau J, Laine-Böszormenyi M and Izawa S (1981) Charge storage in chloride depleted chloroplasts. In: Akoyunoglou (ed) Photosynthesis, Vol II, pp 435–443. Balaban International Science Services, Philadelphia
Nash D, Miyao M and Murata N (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 807: 127–133
Ono T, Zimmerman JL, Inoue Y and Rutherford AW (1986) EPR evidence for a modified S-transition in chloride depleted photosystem II. Biochim Biophys Acta 850: 193–201
Ono T, Nakayama H, Gleiter H, Inoue Y and Kawamori A (1987) Modification of the properties of S2 state in photosynthetic oxygen-evolving center by replacement of chloride with other anions. Arch Biochem Biophys 256: 618–624
Pistorius EK and Schmid GH (1987) Effect of chloride ions on the S-state distribution and deactivation kinetics in preparations of the cyanobacterium Anacystis nidulans. Biochim Biophys Acta 890: 352–359
Preston C and Pace RJ (1985) The S-state dependence of chloride binding to plant photosystem II. Biochim Biophys Acta 810: 388–391
Reed GH and Markham GD (1984) EPR of Mn(II) complexes with enzymes and other proteins. In: Berliner LJ and Reuben J (eds) Biological Magnetic Resonance, Vol 6, pp 73–142. Plenum Press, New York
Renger G (1987a) Biological exploitation of solar energy by photosynthetic water splitting. Angew Chemie (Int Eng Ed) 26: 643–660
Renger G (1987b) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21: 203–224
Sandusky PO and Yocum CF (1984a) The mechanism of amine inhibition of the photosynthetic oxygen-evolving complex: Amines displace functional chloride from a ligand site on manganese. FEBS Lett 162: 339–343
Sandusky PO and Yocum CF (1984b) The chloride requirement for photosynthetic oxygen evolution: Analysis of the effects of chloride and other anions on amine inhibition of the oxygen-evolving complex. Biochim Biophys Acta 766: 603–611
Sandusky PO and Yocum CF (1986) The chloride requirement for photosynthetic oxygen evolution: Factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex. Biochim Biophys Acta 849: 85–93
Shen J-R and Katoh S (1990) Inactivation of oxygen evolution by low pH-treatment of two rice photosystem II preparations containing one and two bound Ca2+ ions. Proc. VIIIth Internatl. Congr. Photosynth. Baltchevsky M (ed), in press
Shen J-R, Satoh K and Katoh S (1988) Calcium contents of oxygen-evolving photosystem II preparations from higher plants: Effects of NaCl-treatment. Biochim Biophys Acta 933: 358–364
Sinclair J (1984) The influence of anions on oxygen evolution by isolated spinach chloroplasts. Biochim Biophys Acta 764: 247–252
Tamura N and Cheniae G (1985) Effects of photosystem II extrinsic proteins on microstructure of the oxygen-evolving complex and its reactivity to water analogs. Biochim Biophys Acta 809: 245–259
Theg SM and Homann PH (1982) Light, pH and uncoupler-dependent association of chloride with chloroplast thylakoids. Biochim Biophys Acta 697: 221–234
Theg SM, Jursinic PA and Homann PH (1984) Studies on the mechanism of chloride action on photosynthetic water oxidation. Biochim Biophys Acta 766: 636–646
Vass I, Ono T and Inoue Y (1987) Stability and oscillation properties of thermoluminescent charge pairs in the oxygen-evolving system depleted of chloride and the 33 kDa protein. Biochim Biophys Acta 892: 224–235
Wydrzynski T and Renger G (1986) On the interpretation of the NMR water-proton relaxivity of photosynthetic membrane samples: Ramifications in the use of EDTA. Biochim Biophysic Acta 851: 65–74
Wydrzynski T and Sauer K (1980) Periodic changes in the oxidation state of manganese in photosynthetic oxygen evolution upon illumination with flashes. Biochim Biophys Acta 589: 56–70
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Wydrzynski, T., Baumgart, F., MacMillan, F. et al. Is there a direct chloride cofactor requirement in the oxygen-evolving reactions of photosystem II?. Photosynth Res 25, 59–72 (1990). https://doi.org/10.1007/BF00051736
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DOI: https://doi.org/10.1007/BF00051736