Levels of endogenous abscisic acid (ABA) are changed dynamically in response to environmental conditions. The ABA 8'-hydroxylase is a key enzyme in ABA catabolism and is encoded by CYP707A genes. In this study, we examined physiological roles of Arabidopsis (Arabidopsis thaliana) CYP707As in the plant's response to changes in humidity. The cyp707a1 and cyp707a3 mutants displayed lower stomatal conductance under turgid conditions (relative humidity 60%) than the wild type. When wild-type plants were transferred to high-humidity conditions (relative humidity 90%), CYP707A1 and CYP707A3 transcript levels increased, followed by the reduction of ABA levels. The cyp707a3 mutant exhibited high ABA levels even after transferring to high-humidity conditions, whereas, under similar conditions, the cyp707a1 mutant exhibited low ABA levels comparable to the wild type. Analysis of spatial expression patterns by using transgenic plants harboring a promoterbeta-glucuronidase gene indicated that high-humidity-induced expression of CYP707A1 and CYP707A3 occurred primarily in guard cells and vascular tissues, respectively. Furthermore, stomatal closure of the cyp707a1 mutant, but not cyp707a3 mutant, was ABA hypersensitive when epidermal peel was treated with exogenous ABA, suggesting that CYP707A1 is essential for ABA catabolism inside the guard cells. These results implicate that CYP707A3 reduces the amount of mobile ABA in vascular tissues in response to high humidity, whereas CYP707A1 inactivates local ABA pools inside the guard cells. Taken together, ABA catabolism in both vascular tissues and guard cells participates in the systemic ABA action that controls stomatal movement in response to high humidity.