De-regulated expression of the plant glutamate receptor homolog AtGLR3.1 impairs long-term Ca2+-programmed stomatal closure.

Cytosolic Ca(2+) ([Ca(2+)](cyt)) mediates diverse cellular responses in both animal and plant cells in response to various stimuli. Calcium oscillation amplitude and frequency control gene expression. In stomatal guard cells, [Ca(2+)](cyt) has been shown to regulate stomatal movements, and a defined window of Ca(2+) oscillation kinetic parameters encodes necessary information for long-term stomatal movements. However, it remains unknown how the encrypted information in the cytosolic Ca(2+) signature is decoded to maintain stomatal closure. Here we report that the Arabidopsis glutamate receptor homolog AtGLR3.1 is preferentially expressed in guard cells compared to mesophyll cells. Furthermore, over-expression of AtGLR3.1 using a viral promoter resulted in impaired external Ca(2+)-induced stomatal closure. Cytosolic Ca(2+) activation of S-type anion channels, which play a central role in Ca(2+)-reactive stomatal closure, was normal in the AtGLR3.1 over-expressing plants. Interestingly, AtGLR3.1 over-expression did not affect Ca(2+)-induced Ca(2+) oscillation kinetics, but resulted in a failure to maintain long-term 'Ca(2+)-programmed' stomatal closure when Ca(2+) oscillations containing information for maintaining stomatal closure were imposed. By contrast, prompt short-term Ca(2+)-reactive closure was not affected in AtGLR3.1 over-expressing plants. In wild-type plants, the translational inhibitor cyclohexamide partially inhibited Ca(2+)-programmed stomatal closure induced by experimentally imposed Ca(2+) oscillations without affecting short-term Ca(2+)-reactive closure, mimicking the guard cell behavior of the AtGLR3.1 over-expressing plants. Our results suggest that over-expression of AtGLR3.1 impairs Ca(2+) oscillation-regulated stomatal movements, and that de novo protein synthesis contributes to the maintenance of long-term Ca(2+)-programmed stomatal closure.

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