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

Understanding photosynthesis in natural, dynamic light environments requires knowledge of long-term acclimation, short-term responses, and their mechanistic interactions. To approach the latter, we systematically determined and characterized light-environmental effects on thylakoid ion transport-mediated short-term responses during light fluctuations. For this, Arabidopsis thaliana wild-type and mutants of the Cl channel VCCN1 and the K exchange antiporter KEA3 were grown under eight different light environments and characterized for photosynthesis-associated parameters and factors in steady state and during light fluctuations. For a detailed characterization of selected light conditions, we monitored ion flux dynamics at unprecedented high temporal resolution by a modified spectroscopy approach. Our analyses reveal that daily light intensity sculpts photosynthetic capacity as a main acclimatory driver with positive and negative effects on the function of KEA3 and VCCN1 during high-light phases, respectively. Fluctuations in light intensity boost the accumulation of the photoprotective pigment zeaxanthin (Zx). We show that KEA3 suppresses Zx accumulation during the day, which together with its direct proton transport activity accelerates photosynthetic transition to lower light intensities. 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, Zx accumulation, photoprotection, and photosynthetic efficiency.