The conformation of the isoprenyl chain relative to the semiquinone head in the primary electron acceptor (Q(A)) of higher plant PSII (plastosemiquinone) differs from that in bacterial reaction centers (ubisemiquinone or menasemiquinone) by ca. 90°

The conformation and partial electron spin density distribution of the reduced primary electron acceptor (Q(A)^-), a plastosemiquinone-9 (PQ-9) anion radical, in photosystem II protein complexes from spinach as well as free PQ-9- in solution have been determined by EPR and ¹H ENDOR spectroscopies. The data show that the conformation of the isoprenyl chain at Cβ relative to the aromatic ring differs by 90° for Q(A)^- in higher plant PSII versus both types of bacterial reaction centers, Rhodobacter sphaeroides and Rhodopseudomonas viridis [containing ubiquinone (UQ) or menaquinone (MQ) at Q(A) site, respectively]. This conformational distinction between the Q(A)^- species in PSII vs bacterial RCs follows precisely the conformational preferences of the isolated semiquinone anion radicals free in solution; type II semiquinones like PQ-9^- have the isoprenyl CβCγ bond coplanar with the aromatic ring, while type I semiquinones like UQ^- and MQ^- place the CβCγ bond perpendicular to the ring. This conformational difference originates from nonbonded repulsions between the isoprenyl chain and the C6 methyl group present in type I semiquinones, forcing the perpendicular conformation, but absent in type II semiquinones having the smaller H atom at C6. Thus, the Q(A) binding site in both higher plant PSII and bacterial reaction centers accommodates the lower energy conformation of their native semiquinones observed in solution. The energy difference between ground (CβCγ bond perpendicular to the ring) and excited (CβCγ bond coplanar with the ring) conformations of UQ^- and vitamin K₁ ^- radicals is estimated to be sufficiently large (ca. 6 kcal/mol) to produce greater than a 10-fold difference in populations of these conformations at room temperature. For PQ- 9^-, a similar number is estimated. We propose that the strong conformational preferences of type I and type II semiquinones has lead to the evolution of different reaction center protein structures surrounding the isoprenyl/quinone head junction of Q(A) to accommodate the favored low energy conformers. This predicted difference in protein structures could explain the low effectiveness (high selectivities) observed in quinone replacement experiments for type II vs type I quinones seen in higher plant PSII and bacterial reaction centers, respectively.