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Phototropins are plasma membrane-associated photoreceptors of blue light and UV-A/B radiation. The <i>Arabidopsis thaliana</i> genome encodes two phototropins, <i>PHOT1</i> and <i>PHOT2</i>, that mediate phototropism, chloroplast positioning, and stomatal opening. They are well characterized in terms of photomorphogenetic processes, but so far, little was known about their involvement in photosynthesis, oxidative stress responses, and cell death. By analyzing <i>phot1</i>, <i>phot2</i> single, and <i>phot1phot2</i> double mutants, we demonstrated that both phototropins influence the photochemical and non-photochemical reactions, photosynthetic pigments composition, stomata conductance, and water-use efficiency. After oxidative stress caused by UV-C treatment, <i>phot1</i> and <i>phot2</i> single and double mutants showed a significantly reduced accumulation of H₂O₂ and more efficient photosynthetic electron transport compared to the wild type. However, all <i>phot</i> mutants exhibited higher levels of cell death four days after UV-C treatment, as well as deregulated gene expression. Taken together, our results reveal that on the one hand, both phot1 and phot2 contribute to the inhibition of UV-C-induced foliar cell death, but on the other hand, they also contribute to the maintenance of foliar H₂O₂ levels and optimal intensity of photochemical reactions and non-photochemical quenching after an exposure to UV-C stress. Our data indicate a novel role for phototropins in the condition-dependent optimization of photosynthesis, growth, and water-use efficiency as well as oxidative stress and cell death response after UV-C exposure.