Non-autonomous stomatal control by pavement cell turgor via the K+ channel subunit AtKC1

Stomata optimize land plants' photosynthetic requirements and limit water vapor loss. So far, all of the molecular and electrical components identified as regulating stomatal aperture are produced, and operate, directly within the guard cells. However, a completely autonomous function of guard cells is inconsistent with anatomical and biophysical observations hinting at mechanical contributions of epidermal origins. Here, potassium (K+) assays, membrane potential measurements, microindentation, and plasmolysis experiments provide evidence that disruption of the Arabidopsis thaliana K+ channel subunit gene AtKC1 reduces pavement cell turgor, due to decreased K+ accumulation, without affecting guard cell turgor. This results in an impaired back pressure of pavement cells onto guard cells, leading to larger stomatal apertures. Poorly rectifying membrane conductances to K+ were consistently observed in pavement cells. This plasmalemma property is likely to play an essential role in K+ shuttling within the epidermis. Functional complementation reveals that restoration of the wild-type stomatal functioning requires the expression of the transgenic AtKC1 at least in the pavement cells and trichomes. Altogether, the data suggest that AtKC1 activity contributes to the building of the back pressure that pavement cells exert onto guard cells by tuning K+ distribution throughout the leaf epidermis. Inactivation of the Arabidopsis K+ channel gene AtKC1 reveals that interactions and K+ shuttling between guard cells, pavement cells, and trichomes contribute to the non-autonomous stomatal responses.

Automated summary

Gas exchange in land plants is regulated by stomata, which optimize photosynthesis and limit water vapor loss. This study reveals the mechanical contributions of epidermal cells in stomatal aperture regulation. By disrupting the Arabidopsis thaliana K+ channel subunit gene AtKC1, the researchers found that the back pressure exerted by pavement cells onto guard cells is impaired, leading to larger stomatal apertures. Potassium ion transport within the leaf epidermis plays a crucial role in stomatal functioning.