Although cytochrome b-559 has long been known as a membrane-bound redox component closely linked to the reaction center of the oxygen-generating photosystem (PSII), its role in photosynthesis has remained obscure. This paper reports evidence and outlines a hypothesis in support of a "b-559 cycle"-i.e., a light-induced, cytochrome b-559-dependent, cyclic electron transport pathway around PSU that promotes translocation of protons from plastoquinol into the aqueous domain (lumen) of photosynthetic membranes (thylakoids). Light-induced proton transport coupled to lightinduced electron transport is an essential aspect of energy transduction in photosynthesis because it generates an electrochemical proton gradient that drives ATP synthesis by the process of photosynthetic phosphorylation. The principal carrier of electrons and protons in thylakoids is the plastoquinone/plastoquinol couple. We propose that the b-559 cycle functions as a redox-linked proton pump that may operate jointly with the Rieske iron-sulfur pathway in oxidizing plastoquinol. The overall effect of such concerted oxidation of plastoquinol would be the translocation into the thylakoid lumen of two protons for each electron transferred from water to plastocyanin via plastoquinone.Light-induced proton transport, coupled to light-induced electron transport, gained prominence in photosynthesis research with the recognition that it produces in photosynthetic membranes (thylakoids) an electrochemical proton gradient (A/.tH+) that drives ATP synthesis (1) in the process of photosynthetic phosphorylation (2). This process consists of cyclic (anoxygenic) photophosphorylation in which ATP is the sole product and noncyclic (oxygenic) photophosphorylation in which ATP formation is accompanied by oxygen evolution and the generation ofreducing power whose carrier is ferredoxin (2, 3). Oxygen apart, ATP and reduced ferrodoxin are the two products of transduction of sunlight's electromagnetic energy into forms of chemical energy that, directly or through intermediates, drive the biosynthetic and regulatory reactions of photosynthesis including, but not limited to, CO2 assimilation (4).In noncyclic, oxygenic photophosphorylation, A/.H+ is generated by protons released from two sources: the photooxidation of water (see Discussion) and the oxidation of plastoquinol (PQH2). As for PQH2, the accepted view is that thylakoids can oxidize it only via the Rieske iron-sulfur center pathway that is sensitive to inhibition by dibromothymoquinone (2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, DBMIB) (5, 6). However, evidence was recently obtained (7) that PQH2 is also photooxidized by an alternative, cyclic pathway not inhibited by DBMIB. The cyclic pathway was uncovered through the use of uncouplers, specifically proton conductors (protonophores). Two chemically diverse photonophores, 2,6-di-(t-butyl)-4-(2',2'-dicyanovinyl)phenol (SF 6847) (8,9) and carbonylcyanide p-trifluoromethoxyphenylhydrazone (FCCP) (10, 11), induced oxidation of PQH2 and dramatically lowered...