Signaling mechanisms in abscisic acid-mediated stomatal closure

Abstract

The plant hormone abscisic acid (ABA) plays a central role in the regulation of stomatal movements under water-deficit conditions. The identification of ABA receptors and the ABA signaling core consisting of PYR/PYL/RCAR ABA receptors, PP2C protein phosphatases and SnRK2 protein kinases has led to studies that have greatly advanced our knowledge of the molecular mechanisms mediating ABA-induced stomatal closure in the past decade. This review focuses on recent progress in illuminating the regulatory mechanisms of ABA signal transduction, and the physiological importance of basal ABA signaling in stomatal regulation by CO₂ and, as hypothesized here, vapor-pressure deficit. Furthermore, advances in understanding the interactions of ABA and other stomatal signaling pathways are reviewed here. We also review recent studies investigating the use of ABA signaling mechanisms for the manipulation of stomatal conductance and the enhancement of drought tolerance and water-use efficiency of plants.

Keywords: abscisic acid (ABA); basal ABA; drought tolerance; guard cell; water-use efficiency.

Figure 1.

Simplified model of abscisic acid (ABA) signal transduction and regulatory mechanisms in stomatal closure discussed herein. A reconstitutable ABA signaling module is enclosed in a red rectangle. Positive regulators of ABA signaling are presented in green boxes. Negative regulators of ABA signal transduction are presented in red ovals. Arrows indicate activation and bars indicate downregulation. Solid lines represent regulation pathways predicted to be direct, and dashed lines represent some of the unknown pathways that remain to be investigated further. ABA-bound PYR/PYL receptors inhibit PP2C phosphatase activity leading OST1/SnRK2.6 kinase activation by clade-B3 Raf-like M3Ks in guard cells. The S-type anion channel SLAC1, the R-type anion channel QUAC1/AtALMT12 and other diverse targets not shown here are activated via phosphorylation by the OST1/SnRK2.6, SnRK2.2 and SnRK2.3 protein kinases, thus triggering stomatal closure. Note that additional phosphorylation targets of SnRK2 protein kinases are required for stomatal closure and many of these remain to be identified. PP2Cs downregulate SnRK2 protein kinases and also additional targets (not shown), including SLAC1, thus preventing non-specific Ca²⁺-induced S-type anion channel activation by calcium-dependent protein kinase (CPKs). L-CYSTEINE DESULFHYDRASE 1 (DES1) mediates ABA-induced hydrogen sulfide (H₂S) production, and then H₂S persulfidates OST1/SnRK2.6 on cysteine residues to enhance OST1 kinase activity. OST1/SnRK2.6 kinase is inhibited by the SnRK2-interacting calcium sensor (SCS). CARK1 phosphorylates PYR/PYL/RCAR receptors to enhance ABA signal transduction. The stability of PYR/PYL/RCARs receptors is regulated by ALIX-mediated protein degradation. A PP2C-GEF-ROP control loop can ensure the off/on regulation of ABA signal transduction, with ABA triggering GEF trafficking to the prevacuolar compartment for degradation through CPK phosphorylation of GEF, thus removing ROP activity. EAR1 enhances PP2C phosphatase activity to repress ABA signal transduction, and PUB12/13, RGLG1/5 and BPMs regulate PP2C stability through the ubiquitin-26S proteasome pathway. ABA inhibits RGLG1 myristoylation through an unknown mechanism to promote its nuclear localization and PP2CA degradation.