The light reactions of photosynthesis convert harvested light into chemical energy that can be utilized by cells for metabolism. Through the translocation of protons across the thylakoid membrane coupled to electron transfer reactions, the photosynthetic proton motive force (pmf) is used to drive the production of ATP synthesis. Detailed studies have characterized the molecular processes of pmf–mediated feedback regulation of photosynthesis via changes in luminal pH from the light-induced proton gradient (ΔpH). While it is now well established that the photosynthetic pmf in higher plants consists of both a ΔpH and an electric potential (Δψ), the impact that Δψ exerts on photosynthesis in vivo is mostly unstudied. The Δψ component, however, influences the relative free-energy between redox mediators of electron transfer within membrane complexes. We found that in plants, a large in vivo Δψ increases photoinhibition through photosystem II (PSII) damage. High Δψ levels were observed in mutants with high steady-state pmf levels, as well as in wild type plants during light fluctuations. The increase in photoinhibition is primarily due to increased yields of electron recombination in PSII, which generate reactive oxygen species (ROS). The yield of PSII recombination when Δψ is large is mediated by ΔpH-dependent photosynthetic downregulation to decrease the concentration of reduced electron acceptors in PSII (QA-) capable of recombining and generating ROS. The ability to regulate photosynthetic light capture and electron transfer via pH–dependent processes as well as the need for photosynthetic organisms to mitigate a large Δψ leads me to propose that the photosynthetic organisms have evolved regulatory processes to mediate the bioenergetic limitations imposed by the Δψ effect on electron transfer. In a population of natural Arabidopsis thaliana accessions, variation in the kinetics of activating and deactivating pH-dependent downregulation of photosynthesis allowed the genetic loci responsible for the kinetics within this population to be mapped. These results suggest that photosynthetic organisms have evolved multiple mechanisms to regulate how rapidly photosynthesis is regulated by the pmf. The partitioning of pmf between Δψ and ΔpH allows a plant to balance the induction and relaxation of photoprotective mechanisms at the detriment of light utilization, while minimizing the impact of Δψ-mediated PSII recombination and ROS production. The processes work in concert to minimize potential photodamage and loss of productivity that occurs due to biophysical alterations in electron transfer processes mediated by Δψ.
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