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The mechanical properties of guard cell (GC) walls are important for stomatal development and stomatal response to external stimuli. However, the molecular mechanisms of pectin synthesis and pectin composition controlling stomatal development and dynamics remain poorly explored. Here, we characterized the role of two Arabidopsis (Arabidopsis thaliana) galacturonosyltransferases, GAUT10 and GAUT11, in plant growth, stomatal development, and stomatal dynamics. GAUT10 and GAUT11 double mutations reduced pectin synthesis and promoted homogalacturonan (HG) demethylesterification and demethylesterified HG degradation, resulting in larger stomatal complexes and smaller pore areas, increased stomatal dynamics, and enhanced drought tolerance of plants. In contrast, increased GAUT10 or GAUT11 expression impaired stomatal dynamics and drought sensitivity. Genetic interaction analyses together with immunolabeling analyses suggest that the methylesterified HG level is important in stomatal dynamics, and pectin abundance with the demethylesterified HG level controls stomatal dimension and stomatal size. Our results provide insight into the molecular mechanism of GC wall properties in stomatal dynamics, and highlight the role of GAUT10 and GAUT11 in stomatal dimension and dynamics through modulation of pectin biosynthesis and distribution in GC walls.

Two galacturonosyltransferases function in plant growth, stomatal development, and dynamics