Lack of GDSL motif–containing proteins increases drought tolerance by altering the stomatal cuticle in Arabidopsis

Stomata facilitate gas exchange across the otherwise virtually impermeable cuticle of the plant surface. To control this gas exchange, guard cells undergo reversible changes in their shape and volume to regulate the stomatal aperture. The ability of guard cells to undergo these changes likely requires flexibility of the guard cell wall. Here, we functionally characterized GELP80, a meristemoid-expressed Gly-Asp-Ser-Leu (GDSL) lipase that is a target of SPEECHLESS, a key transcription factor regulating stomatal development. Double T-DNA insertion mutants of GELP80 and its closest homolog GELP100 exhibit aberrant stomatal pore morphology. These defects were associated with a significant reduction in stomatal aperture index independent of abscisic acid, decreased transpiration, reduced cuticle permeability, and enhanced drought tolerance. In addition, alterations in wax and cutin composition were detected at the whole-rosette level, based on analyses of entire leaves rather than guard cells. The gelp80 gelp100 guard cells have an altered wax and cell wall composition. GELP80 acts as fatty acyl-ester hydrolase leading to increased degradation of very-long-chain fatty acid (VLCF-C22:0 and C30 acyl-CoA) to free fatty acids (FAs; C22, C30). We hypothesize that these alterations decrease the flexibility of the stomata cell walls, thus impairing guard cell function.