The proton coupled electron transfer of the light reactions of photosynthesis supply ATP and reducing power to metabolic processes within the chloroplast and, ultimately, the organism. The textbook pathway of electron transfer or `Z-scheme' of photosynthesis supplies a fixed ratio of ATP and reducing power (i.e. reduced ferredoxin and NAD(P)H), however, the downstream metabolic demands require a highly dynamic ratio. This poses a problem when downstream metabolic demands lead to a deficit of ATP, a buildup of reducing equivalents may occur in the stroma, which may then lead to the buildup of reactive oxygen species (ROS). To balance the output of the light reactions, the chloroplast employs several mechanisms to either shunt electrons out of the system, or by redirecting electrons away from downstream metabolism and back into the plastoquinone pool to generate additional ATP in a process termed cyclic electron flow around photosystem I (CEF). CEF has been proposed to be catalyzed by multiple pathways. In plants, this includes the antimycin A sensitive ferredoxin quinone reductase (FQR) and the respiratory Complex I analog, the NADPH dehydrogenase complex (NDH). We found these pathways are differentially regulated by redox status, with the FQR more active in a reducing environment (Em = -306 mV), while the NDH is activated in response to ROS. We further found that the kinetics of activation for the two pathways were different, with the FQR rapidly activated (seconds to minutes) and the NDH activated more slowly (minutes). Additionally, we have evidence that the NDH is a proton pumping plastoquinone reductase. This observation indicates the two pathways contribute different levels of pmf to offset an ATP deficit. We propose CEF pathways are differentially regulated in response to chloroplast redox state. The FQR is rapidly activated when reducing equivalents in the stroma accumulate in response to a short-term or rapidly fluctuating ATP deficit. When the FQR fails to restore homeostasis and the ATP deficit leads to ROS formation, the NDH complex is activated as a more robust mechanism of pmf generation via CEF.
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