This study provides evidence for enhanced electron flow from the stromal compartment of the photosynthetic membranes to P700+ via the cytochrome b6/f complex (Cyt b6/f) in leaves of Cucumis sativus L. submitted to chilling-induced photoinhibition. The above is deduced from the P700 oxidation-reduction kinetics studied in the absence of linear electron transport from water to NADP+, cyclic electron transfer mediated through the Q-cycle of Cyt b6/f and charge recombination in photosystem I (PSI). The segregation of these pathways for P700+ rereduction were achieved by the use of a 50-ms multiple turnover white flash or a strong pulse of white or far-red illumination together with inhibitors. In cucumber leaves, chilling-induced photoinhibition resulted in approximately 20% loss of photo-oxidizible P700. The measurement of P700+ was greatly limited by the turnover of cyclic processes in the absence of the linear mode of electron transport as electrons were rapidly transferred to the smaller pool of P700+. The above is explained by integrating the recent model of the cyclic electron flow in C3 plants based on the Cyt b6/f structural data [Joliot and Joliot (2006) Biochim Biophys Acta 1757:362-368] and a photoprotective function elicited by a low NADP+/NAD(P)H ratio [Rajagopal et al. (2003) Biochemistry 42:11839-11845]. Over-reduction of the photosynthetic apparatus results in the accumulation of NAD(P)H in vivo to prevent NADP+-induced reversible conformational changes in PSI and its extensive damage. As the ferredoxin:NADP reductase is fully reduced under these conditions, even in the absence of PSII electron transport, the reduced ferredoxin generated during illumination binds at the stromal openings in the Cyt b6/f complex and activates cyclic electron flow. On the other hand, the excess electrons from the NAD(P)H pool are routed via the Ndh complex in a slow process to maintain moderate reduction of the plastoquinone pool and redox poise required for the operation of ferredoxin:plastoquinone reductase mediated cyclic flow.