A new plastocyanin from the fern Dryopteris crassirhizoma markedly differs from other plastocyanins in having a very large acidic surface, which extends into the area that is hydrophobic in other plastocyanins. The exceptionally large dipole moment of 439 D has a completely different orientation and protrudes through the "northwest" region of the surface, which is now acidic. Consequently, the new plastocyanin differs from its congeners in the photoinduced reaction with zinc cytochrome c: (3)Zncyt + pc(II)--> Zncyt(+) + pc(I). At ionic strength less than or equal to 20 mM and solution viscosity (less than or equal to 1.8 cp, at least three exponentials are needed to describe the oxidative quenching of 3Zncyt. Besides a bimolecular phase, then, are two distinct unimolecular phases corresponding to electron transfer within two different persistent complexes (3)Zncyt/pc(II). So-called normal and reverse titrations yield consistent values of the unimolecular rate constants: k(1) is (3.3 +/- 0.7) x 10(5) s(-1) and (3.2 +/- 0.4) x 105 s(-1), and kz is (7.6 +/- 0.8) x 10(3) s(-1) and (8.2 + 1.2) x 103 s(-1). The respective Delta H-double dagger values also differ (16 +/- 2 and 27 +/- 7 kJ/mol), but Delta S-double dagger values are the same (-88 +/- 7 and -78 +/- 23 J/K mel). Viscosity effects and also unrealistic reorganizational energies obtained in fittings of temperature effects to Marcus theory reveal that both unimolecular electron-transfer reactions (k(1) and kz) are gated by structural rearrangement of the respective binary complexes. Additional evidence for multiple persistent binary complexes is dependence on ionic strength of the apparent rate constant ii,,, for electron transfer in the transient binary complex 3Zncyt/pc(II). Analysis of this dependence indicates that rearrangement, of the: protein complexes involves relatively large migration of zinc cytochrome c, which is facilitated at higher ionic strength. When zinc cytochrome c is present in excess, a transient, but not persistent, ternary complex Zncyt/pc/Zncyt is formed; both reverse titration and analysis of the effects of protein association on the H-1 NMR chemical shifts support this conclusion. Existence of a ternary complex is consistent with the existence bf multiple binary complexes. Monte Carlo simulations show possible docking configurations of the binary Zncyt/pc complexes. These theoretical calculations, in conjunction with our I;kinetic data, suggest that: the faster (k(1)) and slower (kr) intracomplex reactions seem to occur when 3Zncyt docks, respectively, in the "'northeast" and "northwest" surface regions of fern plastocyanin lin the conventional orientation). The new type of docking, on the "northwest" side of the plastocyanin surface, is favored by new acidic residues in this region.