Two calcineurin B‐like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis

<jats:title>Summary</jats:title><jats:p>Calcium signalling involves sensor proteins that decode temporal and spatial changes in cellular Ca<jats:sup>2+</jats:sup> concentration. Calcineurin B‐like proteins (CBLs) represent a unique family of plant calcium sensors that relay signals by interacting with a family of protein kinases, designated as CBL‐interacting protein kinases (CIPKs). In a reverse genetic screen for altered drought tolerance, we identified a loss‐of‐function allele of <jats:italic>CIPK23</jats:italic> as exhibiting a drought‐tolerant phenotype. In the <jats:italic>cipk23</jats:italic> mutant, reduced transpirational water loss from leaves coincides with enhanced ABA sensitivity of guard cells during opening as well as closing reactions, without noticeable alterations in ABA content in the plant. We identified the calcium sensors CBL1 and CBL9 as CIPK23‐interacting proteins that targeted CIPK23 to the plasma membrane <jats:italic>in vivo</jats:italic>. Expression analysis of the <jats:italic>CIPK23</jats:italic>, <jats:italic>CBL1</jats:italic> and <jats:italic>CBL9</jats:italic> genes suggested that they may function together in diverse tissues, including guard cells and root hairs. In addition, expression of the <jats:italic>CIPK23</jats:italic> gene was induced by low‐potassium conditions, implicating a function of this gene product in potassium nutrition. Indeed, <jats:italic>cipk23</jats:italic> mutants displayed severe growth impairment on media with low concentrations of potassium. This phenotype correlates with a reduced efficiency of K<jats:sup>+</jats:sup> uptake into the roots. In support of the conclusion that CBL1 and CBL9 interact with and synergistically serve as upstream regulators of CIPK23, the <jats:italic>cbl1 cbl9</jats:italic> double mutant, but not the <jats:italic>cbl1</jats:italic> or <jats:italic>cbl9</jats:italic> single mutants, exhibit altered phenotypes for stomatal responses and low‐potassium sensitivity. Together with the recent identification of the potassium channel AKT1 as a target of CIPK23, these results imply that plasma membrane‐localized CBL1– and CBL9–CIPK23 complexes simultaneously regulate K<jats:sup>+</jats:sup> transport processes in roots and in stomatal guard cells.</jats:p>