Light acclimation interacts with thylakoid ion transport to govern the dynamics of photosynthesis

Abstract Understanding photosynthesis in natural, dynamic light environments requires knowledge of long-term acclimation, short-term responses, and their mechanistic interactions. However, the latter is poorly understood. We systematically determined light-environment effects on the thylakoid ion transport-mediated responses of photosynthesis during light fluctuations. Our analyses reveal daily light intensity as the main acclimatory driver that sculps photosynthetic capacity and thereby governs the activities of the thylakoid Cl- channel VCCN1 and the H+/K+ exchanger KEA3 during high light phases. We uncover high zeaxanthin accumulation as a response to fluctuating light environments, which delays the relaxation of energy dependent quenching (qE). KEA3 partly suppresses zeaxanthin accumulation over the day and thereby further accelerates the response of photosynthesis to low light periods. In summary, both light-environment factors, intensity and variability, modulate the function of thylakoid ion transport in dynamic photosynthesis with distinct effects on lumen pH, zeaxanthin accumulation, qE and photosynthetic light use efficiency.