Suitable treatment of thylakoids with hydrazine permits a high population of the redox states S0, S-1, and S-2 in the water oxidase. Experiments performed with dark-adapted samples enriched either in the oxidized or reduced form of the redox-active tyrosine, Y(D), of PolYpeptide D2 reveal that Y(D)ox is a unique endogenous oxidant within the PS II complex which causes a one-electron abstraction from the water oxidase in states S0, S-1, and S-2, respectively. A kinetic analysis of the period four oscillation of oxygen yield induced by a train of short flashes in dark-adapted samples permits the determination of the rate constants of electron abstraction from the reduced water oxidase by Y(D)ox. A value of 9 x 10(-4) s-1 was found for the oxidation of S0 and S-2, while S-1 becomes oxidized with a rate constant of 4 x 10(-4) s-1 at 20-degrees-C and pH 7.2. The redox state S0 generated either from S1 via the three-flash-induced oxidative pathway through S4 or from a one-flash oxidation of the S-1 state obtained by S1 reduction with NH2NH2 exhibits the same kinetics as S0 oxidation by Y(D)ox. On the basis of these findings and data taken from the literature, the electronic configuration of the Manganese atoms in the tetranuclear cluster is discussed. It is assumed that the dimer model of two binuclear manganese groups within the tetranuclear cluster comprises a functional heterogeneity: (i) one binuclear center, referred to as the catalytic group, is proposed to be involved in the oxidative pathway leading to the eventual oxidation of water to dioxygen, and (ii) the other binuclear center, symbolized as component C, is redox-inert during the oxidative pathway but can be reduced by exogenous (and endogenous?) components, thereby forming the states S-1 and S-2 Of the water oxidase. An asymmetric protein matrix around the tetranuclear manganese cluster is assumed to be responsible for the functional heterogeneity of the manganese centers.