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<bold>Summary</bold> Cytosolic calcium concentration ([Ca²⁺]_cyt) and heterotrimeric G‐proteins are universal eukaryotic signaling elements. In plant guard cells, extracellular calcium (Ca_o) is as strong a stimulus for stomatal closure as the phytohormone abscisic acid (ABA), but underlying mechanisms remain elusive. Here, we report that the sole Arabidopsis heterotrimeric Gβ subunit,AGB1, is required for four guard cell Ca_oresponses: induction of stomatal closure; inhibition of stomatal opening; [Ca²⁺]_cytoscillation; and inositol 1,4,5‐trisphosphate (InsP3) production. Stomata in wild‐type Arabidopsis (Col) and in mutants of the canonical Gα subunit,GPA1, showed inhibition of stomatal opening and promotion of stomatal closure by Ca_o. By contrast, stomatal movements ofagb1mutants andagb1/gpa1double‐mutants, as well as those of theagg1agg2 Gγ double‐mutant, were insensitive to Ca_o. These behaviors contrast withABA‐regulated stomatal movements, which involveGPA1 andAGB1/AGG3 dimers, illustrating differential partitioning of G‐protein subunits among stimuli with similar ultimate impacts, which may facilitate stimulus‐specific encoding.AGB1knockouts retained reactive oxygen species andNOproduction, but lostYC3.6‐detected [Ca²⁺]_cytoscillations in response to Ca_o, initiating only a single [Ca²⁺]_cytspike. Experimentally imposed [Ca²⁺]_cytoscillations restored stomatal closure inagb1. Yeast two‐hybrid and bimolecular complementation fluorescence experiments revealed thatAGB1 interacts with phospholipase Cs (PLCs), and Ca_oinduced InsP3 production in Col but not inagb1. In sum, G‐protein signaling viaAGB1/AGG1/AGG2 is essential for Ca_o‐regulation of stomatal apertures, and stomatal movements in response to Ca_oapparently require Ca²⁺‐induced Ca²⁺release that is likely dependent on Gβγ interaction withPLCs leading to InsP3 production.