On why thylakoids energize ATP formation using either delocalized or localized proton gradients - a Ca2+ mediated role in thylakoid stress responses

By the early 1970s, the chemiosmotic hypothesis of Peter Mitchell was widely accepted by bioenergetics researchers as the best conceptual scheme to explain how ATP is formed in oxidative and photosynthetic phosphorylation. At about the same time, however, work from a few laboratories suggested that some aspects of that elegant, relatively simple hypothesis required revision-not abandonment, but refinement to accommodate more complex movements of protons in the ATP formation mechanism than originally envisioned by Peter Mitchell. In some situations it appeared that protons were constrained to localized domains rather than always delocalized within an enclosed vesicle as envisioned by chemiosmosis. This minireview tells that story from my perspective, as one of the researchers involved in the experimental approaches that revealed more complex energy coupling proton flux patterns. Ionic conditions during isolated thylakoid storage were found to reversibly switch the Delta(mu) over tilde (H+) gradient driving ATP formation between delocalized and localized energy coupling modes. Thylakoid accessible Ca2+ ions proved to be the switching factor that was responding to the ionic conditions in the storage treatment. The mechanism of Ca2+ was at least partially demystified when it was shown that the reversible switching between Delta(mu) over tilde (H+) energy coupling modes involved Ca2+ interactions with the 8 kDa CF0 (the H+ channel) subunit in a type of H+ flux gating action. Other experiments showed that the Ca2+ gating of H+ flux into the lumen may be a critical regulatory factor in controlling the lumen pH and thereby help regulate the activity of the violaxanthin de-epoxidase enzyme, a key part of the chloroplast photoprotective response to over-energization (excess light) stress.