A quinone-independent photoreduction of the low potential form of cytochrome b559 has been studied using isolated reaction centers of photosystem II. Under anaerobic conditions, the cytochrome can be fully reduced by exposure to strong illumination without the addition of any redox mediators. Under high light conditions, the extent and rate of the reduction is unaffected by addition of the exogenous electron donor Mn2+ and, during this process, no irreversible damage occurs to the reaction center. However, prolonged illumination in strong light brings about irreversible bleaching of chlorophyll, indicative of photoinhibitory damage. When the cytochrome is fully reduced and excess Mn2+ is present, the effect of moderate light is to facilitate the photoaccumulation of reduced pheophytin. The dark reoxidation of the reduced cytochrome is very slow under anaerobic conditions but significantly speeded up on addition of oxidized 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone. From these results it is suggested that the low potential form of cytochrome b559 can accept electrons directly from reduced pheophytin and in so doing help to protect the reaction center against acceptor side photoinhibition as suggested by Nedbal et al. [Nedbal, J., Samson, G. & Whitmarsh, J. (1992) Proc. Natl. Acad. Sci. USA 89, 7929-7933]. This conclusion has been incorporated into a model that further suggests that in its high potential form the cytochrome primarily acts to protect against donor side photoinhibition due to increased lifetime of highly oxidized species as previously proposed by Thompson and Brudvig [Thompson, L. & Brudvig, G. W. (1988) Biochemistry 27, 6653-6658]. The particular feature of our scheme is that it incorporates reversible interconversion between the two redox forms so as to protect against either type of photoinhibition.