Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling

Abstract

Stomatal pores are formed by pairs of specialized epidermal guard cells and serve as major gateways for both CO(2) influx into plants from the atmosphere and transpirational water loss of plants. Because they regulate stomatal pore apertures via integration of both endogenous hormonal stimuli and environmental signals, guard cells have been highly developed as a model system to dissect the dynamics and mechanisms of plant-cell signaling. The stress hormone ABA and elevated levels of CO(2) activate complex signaling pathways in guard cells that are mediated by kinases/phosphatases, secondary messengers, and ion channel regulation. Recent research in guard cells has led to a new hypothesis for how plants achieve specificity in intracellular calcium signaling: CO(2) and ABA enhance (prime) the calcium sensitivity of downstream calcium-signaling mechanisms. Recent progress in identification of early stomatal signaling components are reviewed here, including ABA receptors and CO(2)-binding response proteins, as well as systems approaches that advance our understanding of guard cell-signaling mechanisms.

Figure 1

Summary of guard cell signaling and ion channel regulation. This model focuses on guard cell ion channel functions and ABA-induced signal transduction across the plasma membrane and vacuolar membrane of guard cells. Signaling events during stomatal closing are shown in the left guard cell, and major regulation steps for ABA-inhibition of stomatal opening mechanisms are shown in the right guard cell. Abbreviations: ABA, abscisic acid; I_Ca, inward Ca²⁺ current; S-type, slow-type; SLAC1, SLOW ANION CHANNEL ASSOCIATED 1; R-type, rapid-type; SV, slow vacuolar; VK, vacuolar K⁺ selective; TPK1, TWO PORE K⁺ CHANNEL 1; AHA1, ARABIDOPSIS H⁺ ATPASE 1; OST2, OPEN STOMATA 2.

Figure 2

A simplified model illustrating the functions of recently identified genes and mechanisms in guard cells mediating CO₂ control of stomatal movements. In this model, the HT1 protein kinase and ABCB14 proteins function as negative regulators (red ), and CA1 and CA4, GCA2, and SLAC1 function as positive mediators ( green) of high CO₂-induced stomatal closing. Convergence with abscisic acid (ABA) signaling is also indicated. Abbreviations: HT1, HIGH LEAF TEMPERATURE 1; GCA2, GROWTH CONTROLLED BY ABSCISIC ACID 2; CA, CARBONIC ANHYDRASE; SLAC1, SLOW ANION CHANNEL ASSOCIATED 1.

Figure 3

A proposed simplified model for early ABA signaling events. In the absence of ABA, PP2Cs negatively regulate activation of SnRK2 kinases. Without activation of SnRK2s, downstream ABA signaling targets are inactive. In the presence of ABA, ABA binds to PYR/PYL/RCAR proteins. The ABA ligand-PYR/PYL/RCAR-PP2C complex then inhibits PP2Cs and that activates SnRK2 kinases. Active SnRK2 kinases phosphorylate downstream target proteins, including NADPH oxidases, the SLAC1 anion channel and the ABF family proteins, and generate ABA responses. Abbreviations: ABA, abscisic acid; PYR/PYL/RCAR, PYRABACTIN RESISTANCE/PYR1 LIKE/REGULATORY COMPONENT OF ABA RECEPTOR; PP2C, type 2C protein phosphatase; SnRK2, sucrose non-fermenting 1-related protein kinase 2; ABF, ABA-RESPONSE ELEMENT BINDING FACTOR.

Figure 4

ABA-induced Ca²⁺-dependent (middle and right) and Ca²⁺-independent (left) signal transduction mechanisms in guard cells (see text for the details). Abbreviations: ABA, abscisic acid; PP2C, type 2C protein phosphatase; OST1, OPEN STOMATA 1; RbohD/F, RESPIRATORY BURST OXIDASE HOMOLOGUE D/F; I_Ca, inward C^a2+ current; AtMRP5, MULTIDRUG RESISTANCE PROTEIN 5; CPK, CALCIUM-DEPENDENT PROTEIN KINASE; GCA2, GROWTH CONTROLLED BY ABSCISIC ACID 2; S-type, slow-type; SLAC1, SLOW ANION CHANNEL ASSOCIATED 1; R-type, rapid-type.