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Malate-sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration

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Summary

Malate is a characteristic metabolite in the photosynthesis of C4 and CAM plants. Furthermore, changes in the intracellular concentration of this organic acid provide part of the osmotic motor for guard cells. Since alterations in the malate concentration influence the photosynthetic capacity on one side and stomatal action on the other, it was studied whether the extracellular malate level represents an indicator of changes in the ambient CO2 concentration and a key regulator of ion transport in guard cells.

Here it is demonstrated that alterations in the ambient CO2 level modify the extracellular malate concentration of Vicia faba leaves. Elevated external malate caused stomatal closure in a concentration-dependent manner (Kmmal = 0.3 mM). Slight variations in the external malate concentration strongly regulate the voltage-dependent properties of GCAC1, an anion-release channel in the plasma membrane of guard cells. Superfusion of guard cell protoplasts with malate levels in the physiological range (Kmmal = 0.4 mM) caused the voltage gate to shift towards the resting potential of the cell-activating GCAC1. Single-channel conductance was dependent on the extracellular chloride concentration (KmCl = 3 mM). In the absence of extracellular chloride the plasma membrane lacked anion conductance until the addition of malate induced channel opening. Isophthalate was a powerful agonist in both malate-induced processes, channel regulation and stomatal closure, indicating that modulation of GCAC1 is a key step in stomatal action. It was thus concluded that feedback regulation of volume and turgor with respect to the ambient CO2 concentration via malate-sensitive anion channels may provide a CO2 sensor to guard cells.

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