A cell surface receptor mediates extracellular Ca2+ sensing in guard cells

Abstract

Extracellular Ca(2+) (Ca(2+)(o)) is required for various physiological and developmental processes in animals and plants. In response to varied Ca(2+)(o) levels, plants maintain relatively constant internal Ca(2+) content, suggesting a precise regulatory mechanism for Ca(2+) homeostasis. However, little is known about how plants monitor Ca(2+)(o) status and whether Ca(2+)(o)-sensing receptors exist. The effects of Ca(2+)(o) on guard cells in promoting stomatal closure by inducing increases in the concentration of cytosolic Ca(2+) ([Ca(2+)](i)) provide a clue to Ca(2+)(o) sensing. Here we have used a functional screening assay in mammalian cells to isolate an Arabidopsis complementary DNA clone encoding a Ca(2+)-sensing receptor, CAS. CAS is localized to the plasma membrane, exhibits low-affinity/high-capacity Ca(2+) binding, and mediates Ca(2+)(o)-induced [Ca(2+)](i) increases. CAS is expressed predominantly in the shoot, including guard cells. Repression of CAS disrupts Ca(2+)(o) signalling in guard cells, and impairs bolting (swift upward growth at the transition to seed production) in response to Ca(2+) deficiency, so we conclude that CAS may be a primary transducer of Ca(2+)(o) in plants.

VIH2 Regulates the Synthesis of Inositol Pyrophosphate InsP8 and Jasmonate-Dependent Defenses in Arabidopsis

“…The stereochemistry of D-myo-inositol suggested that the inositol ring represents a 6-bit signaling scaffold with the potential to "encode" 64 unique signaling states (York, 2006). In plants, InsP 3 has been associated with a wide range of cellular functions, such as guard cell physiology (Blatt et al, 1990;Gilroy et al, 1990;Burnette et al, 2003;Han et al, 2003), drought tolerance (Knight et al, 1997;Perera et al, 2008), heat shock responses (Liu et al, 2006), blue light perception (Chen et al, 2008), root gravitropism (Wang et al, 2009;Zhang et al, 2011), response to mechanical wounding (Mosblech et al, 2008), and pollen dormancy (Y. . However, the role of InsP 3 and other inositol phosphates in plant signaling remains controversial as no inositol phosphate receptor has been identified to date (Munnik and Vermeer, 2010;Munnik and Nielsen, 2011;Gillaspy, 2013).…”

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

“…It has been shown that external Ca 2+ concentration ([Ca 2+ ] o ) promotes stomatal closure and induces oscillation in [Ca 2+ ] i in guard cells (MacRobbie, 1992;McAinsh et al, 1995;Allen et al, 2001). However, how the guard cells perceive [Ca 2+ ] o concentration and convert [Ca 2+ ] o changes into [Ca 2+ ] i changes was not understood until a calciumsensing receptor (CAS) in the plasma membrane of guard cells in Arabidopsis (Arabidopsis thaliana) was identified (Han et al, 2003). The external Ca 2+ (Ca 2+ o )-induced [Ca 2+ ] i increase is abolished in CAS antisense lines (Han et al, 2003).…”

“…However, how the guard cells perceive [Ca 2+ ] o concentration and convert [Ca 2+ ] o changes into [Ca 2+ ] i changes was not understood until a calciumsensing receptor (CAS) in the plasma membrane of guard cells in Arabidopsis (Arabidopsis thaliana) was identified (Han et al, 2003). The external Ca 2+ (Ca 2+ o )-induced [Ca 2+ ] i increase is abolished in CAS antisense lines (Han et al, 2003). Both [Ca 2+ ] o and [Ca 2+ ] i show diurnal oscillation that is determined by stomatal conductance, whereas the amplitude of [Ca 2+ ] i oscillation is reduced in CAS antisense lines (Tang et al, 2007).…”

Extracellular Calmodulin-Induced Stomatal Closure Is Mediated by Heterotrimeric G Protein and H2O2

“…A plasma membrane-localized extracellular CAS has been shown to regulate guard cell [Ca 21 ] cyt (Han et al, 2003 elevation is similar to that of ABA, it might be possible that a new regulatory factor naturally existing in guard cell walls regulates stomatal movements together with ABA. These findings not only extend the functions of ExtCaM, but also provide clues to understanding the regulatory mechanisms for stomatal movements.…”

“…Recently, guard cell-specific NADPH oxidases AtrbohD (Arabidopsis respiratory burst oxidase homologs D) and AtrbohF have been identified, and the double mutants of atrbohD/F are impaired in ABA-induced ROS generation, [Ca 21 ] cyt increases, and stomatal closing (Kwak et al, 2003), suggesting that AtrbohD and AtrbohF NADPH oxidases and ROS play an important role in ABA signal transduction in guard cells. The evidence that Ca 21 -sensing receptor (CAS) in Arabidopsis plasma membrane, which mediates extracellular Ca 21 induced cytosolic Ca 21 increase in guard cells (Han et al, 2003) Vetter and Leclerc, 2003). Recently, it has been found that CaM exists extracellularly to exert many functions in both animals and plants.…”