All photosynthetic reaction centers share a common structural theme. Two related, integral membrane polypeptides sequester electron transfer cofactors into two quasi-symmetrical branches, each of which incorporates a quinone. In type II reaction centers [photosystem (PS) II and proteobacterial reaction centers], electron transfer proceeds down only one of the branches, and the mobile quinone on the other branch is used as a terminal acceptor. PS I uses iron-sulfur clusters as terminal acceptors, and the quinone serves only as an intermediary in electron transfer. Much effort has been devoted to understanding the unidirectionality of electron transport in type II reaction centers, and it was widely thought that PS I would share this feature. We have tested this idea by examining in vivo kinetics of electron transfer from the quinone in mutant PS I reaction centers. This transfer is associated with two kinetic components, and we show that mutation of a residue near the quinone in one branch specifically affects the faster component, while the corresponding mutation in the other branch specifically affects the slower component. We conclude that both electron transfer branches in PS I are active.

The turnover of linear and cyclic electron flows has been determined in fragments of dark-adapted spinach leaf by measuring the kinetics of fluorescence yield and of the transmembrane electrical potential changes under saturating illumination. When Photosystem (PS) II is inhibited, a cyclic electron flow around PSI operates transiently at a rate close to the maximum turnover of photosynthesis. When PSII is active, the cyclic flow operates with a similar rate during the first seconds of illumination. The high efficiency of the cyclic pathway implies that the cyclic and the linear transfer chains are structurally isolated one from the other. We propose that the cyclic pathway operates within a supercomplex including one PSI, one cytochrome bf complex, one plastocyanin, and one ferredoxin. The cyclic process induces the synthesis of ATP needed for the activation of the Benson-Calvin cycle. A fraction of PSI (ϳ50%), not included in the supercomplexes, participates in the linear pathway. The illumination would induce a dissociation of the supercomplexes that progressively increases the fraction of PSI involved in the linear pathway.I t is widely assumed that the photosynthetic process in algae or plants operates according to two nonmutually exclusive modes: linear and cyclic electron flows. In the linear mode, electrons are transferred from water to the NADP via the three major complexes of the photosynthetic chain, Photosystem (PS) II, cytochrome b 6 f (cyt bf), and PSI (1). Little is known, however, about the mechanism of the cyclic process that was first characterized by Arnon (2) in broken chloroplasts. In unicellular algae, a cyclic electron flow operates in anaerobic conditions (3, 4). In higher plants, the occurrence of a cyclic flow in vivo is a subject of controversy (reviewed in refs. 5 and 6). On the basis of a parallel measurement of PSI and PSII yield, Harbinson and Foyer (7) concluded that a cyclic process operates at a significant rate during the induction period but not in steady-state conditions. Heber et al. (8) reported that a decrease of CO 2 concentration stimulates the cyclic flow. At variance, Klughammer and Schreiber (9) conclude that no significant cyclic flow contributes to PSI turnover during the induction period or in the absence of CO 2 . It is generally reported that in steady-state conditions in the presence of CO 2 , the linear pathway is largely favored with respect to the cyclic flow. Bendall and Manasse (6) concluded that the rate of the cyclic process is no more than 3% of that of the linear pathway.It is agreed that both PSI and cyt bf complexes are involved in the cyclic flow. Yet, the mechanism of electron transfer between the PSI acceptor side and the cyt bf complex is not clearly identified. It has been proposed that reduced ferredoxin (Fd) or NADP may transfer electrons to plastoquinone (PQ) by way of a membrane-bound Fd PQ-reductase or NADP dehydrogenase (NDH). Plastoquinol (PQH 2 ) is then reoxidized at the PQH 2 -oxidizing site Q o of the cyt bf complex. This hypothesis i...