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Electron and proton transfer plays a central role in coupling light capture to the chemical reactions of carbon metabolism. Electrons, originating from charge separation in the photosystems, are eventually transferred to NADP+ to form NADPH; it is denoted as linear electron flow (LEF). Protons, coupled to electrons for neutral diffusion through the thylakoid membrane, are translocated by ATPase for the synthesis of ATP. Carbon metabolism has to keep pace with light capture and it relies on an electron transfer feedback loop: cyclic electron flow (CEF) around PSI (Whatley et al., 1955). In C3 photosynthesis, an upstream limitation bears at the level of rubisco under limiting CO2 (Farquhar et al., 1980). Electrons that cannot be extracted from NADPH to form G3P are recycled around cytochrome b6f and PSI, contributing to the proton motive force, pmf. This pmf is used for ATP synthesis and the regeneration of RuBP from G3P with limitation bearing at the level of SBPase, cytochrome b6f complex and ATPase under non-limiting CO2 (Farquhar et al., 1980; Raines, 2003; Yamori et al., 2011). The lifetime of excited chlorophyll is also decreased by the ΔpH component of pmf [qE component of non-photochemical quenching (Gilmore and Bjorkman, 1995)], thereby limiting the reducing pressure of the photosystems. In high light, nonetheless, electrons accumulate in the plastoquinone pool, favoring an increase of PSI antenna size [state transitions (Allen et al., 1981)]. The oxidized form of PSI primary electron donor P+700 can accumulate in the light, showing that intersystem electron transfer is limited upstream at the level of cytochrome b6f activity. This latter limitation, also denoted as “photosynthetic control,” is pH-dependent (Kok et al., 1969) and induced by CEF (Johnson et al., 2014b) thereby providing a feed-back down-regulation of linear electron transfer. The proton motive force equilibrates with the ATP/ADP ratio, as a function of the ATPase coupling factor. The intermeshed nature of these reactions defy our understanding of the photosynthetic process as a whole, and represents a challenge for future redesigns of photosynthesis, aiming at minimizing wasteful reactions, whether it is at the level of light capture, electron/proton transfer or carbon metabolism.

The plastoquinone pool, poised for cyclic electron flow?