Plants use sunlight as their primary energy source. During photosynthesis, absorbed light energy generates reducing power by driving electron transfer reactions. These are coupled to the transfer of protons into the thylakoid lumen, generating a proton motive force (pmf) required for ATP synthesis. Sudden alterations in light availability have to be met by regulatory mechanisms to avoid the over-accumulation of reactive intermediates and maximize energy efficiency. Here, the acidification of the lumen, as an intermediate product of photosynthesis, plays an important role by regulating photosynthesis in response to excitation energy levels. Recent findings reveal pmf regulation and the modulation of its composition as key determinants for efficient photosynthesis, plant growth, and survival in fluctuating light environments.

In nature, light availability for photosynthesis can undergo massive changes on a very short timescale. Photosynthesis in such dynamic light environments requires that plants can respond swiftly. Expanding our knowledge of the rapid responses that underlie dynamic photosynthesis is an important endeavor: it provides insights into nature's design of a highly dynamic energy conversion system and hereby can open up new strategies for improving photosynthesis in the field. The present review focuses on three processes that have previously been identified as promising engineering targets for enhancing crop yield by accelerating dynamic photosynthesis, all three of them involving or being linked to processes in the chloroplast, i.e. relaxation of non-photochemical quenching, Calvin–Benson–Bassham cycle enzyme activation/deactivation and dynamics of stomatal conductance. We dissect these three processes on the functional and molecular level to reveal gaps in our understanding and critically discuss current strategies to improve photosynthesis in the field.

Proton antiport across the thylakoid membrane up-regulates photosynthesis and growth in an Arabidopsis mutant with low chloroplast ATP synthase levels and high

Photosynthesis is limited by the slow relaxation of nonphotochemical quenching, which primarily dissipates excess absorbed light energy as heat. Because the heat dissipation process is proportional to light-driven thylakoid lumen acidification, manipulating thylakoid ion and proton flux via transport proteins could improve photosynthesis. However, an important aspect of the current understanding of the thylakoid ion transportome is inaccurate. Using fluorescent protein fusions, we show that the Arabidopsis (Arabidopsis thaliana) two-pore K⁺ channel TPK3, which had been reported to mediate thylakoid K⁺ flux, localizes to the tonoplast, not the thylakoid. The localization of TPK3 outside of the thylakoids is further supported by the absence of TPK3 in isolated thylakoids as well as the inability of isolated chloroplasts to import TPK3 protein. In line with the subcellular localization of TPK3 in the vacuole, we observed that photosynthesis in the Arabidopsis null mutant tpk3-1, which carries a transfer DNA insertion in the first exon, remains unaffected. To gain a comprehensive understanding of how thylakoid ion flux impacts photosynthetic efficiency under dynamic growth light regimes, we performed long-term photosynthesis imaging of established and newly isolated transthylakoid K⁺- and Cl⁻-flux mutants. Our results underpin the importance of the thylakoid ion transport proteins potassium cation efflux antiporter KEA3 and voltage-dependent chloride channel VCCN1 and suggest that the activity of yet unknown K⁺ channel(s), but not TPK3, is critical for optimal photosynthesis in dynamic light environments.

Significance: The light reactions of photosynthesis in algae and plants occur in thylakoid membranes within the chloroplast. Previous studies have implicated membrane contact sites, vesicle trafficking, and lipid-binding proteins in the formation of thylakoids at the chloroplast inner envelope, but the molecular basis of thylakoid biogenesis and maintenance remains enigmatic. Here we show that CPSFL1 is a chloroplast Sec14 domain protein that binds lipids and can transfer phosphoinositides between membranes in vitro. In the model plant Arabidopsis , CPSFL1 is necessary for the appearance of vesicles in chloroplasts. Our results provide molecular evidence supporting an essential role of chloroplast lipid and vesicle trafficking for photoautotrophic growth.

Summary: Plant yields heavily depend on proper macro‐ and micronutrient supply from the soil. In the leaf cells, nutrient ions fulfill specific roles in biochemical reactions, especially photosynthesis housed in the chloroplast. Here, a well‐balanced ion homeostasis is maintained by a number of ion transport proteins embedded in the envelope and thylakoid membranes. Ten years ago, the first alkali metal transporters from the K⁺ EFFLUX ANTIPORTER family were discovered in the model plant Arabidopsis. Since then, our knowledge about the physiological importance of these carriers and their substrates has greatly expanded. New insights into the role of alkali ions in plastid gene expression and photoprotective mechanisms, both prerequisites for plant productivity in natural environments, were gained. The discovery of a Cl⁻ channel in the thylakoid and several additional plastid alkali and alkali metal transport proteins have advanced the field further. Nevertheless, scientists still have long ways to go before a complete systemic understanding of the chloroplast's ion transportome will emerge. In this Tansley review, we highlight and discuss the achievements of the last decade. More importantly, we make recommendations on what areas to prioritize, so the field can reach the next milestones. One area, laid bare by our similarity‐based comparisons among phototrophs is our lack of knowledge what ion transporters are used by cyanobacteria to buffer photosynthesis fluctuations.