Abscisic Acid-Induced Stomatal Closure: An Important Component of Plant Defense Against Abiotic and Biotic Stress

Abstract

Abscisic acid (ABA) is a stress hormone that accumulates under different abiotic and biotic stresses. A typical effect of ABA on leaves is to reduce transpirational water loss by closing stomata and parallelly defend against microbes by restricting their entry through stomatal pores. ABA can also promote the accumulation of polyamines, sphingolipids, and even proline. Stomatal closure by compounds other than ABA also helps plant defense against both abiotic and biotic stress factors. Further, ABA can interact with other hormones, such as methyl jasmonate (MJ) and salicylic acid (SA). Such cross-talk can be an additional factor in plant adaptations against environmental stresses and microbial pathogens. The present review highlights the recent progress in understanding ABA's multifaceted role under stress conditions, particularly stomatal closure. We point out the importance of reactive oxygen species (ROS), reactive carbonyl species (RCS), nitric oxide (NO), and Ca²⁺ in guard cells as key signaling components during the ABA-mediated short-term plant defense reactions. The rise in ROS, RCS, NO, and intracellular Ca²⁺ triggered by ABA can promote additional events involved in long-term adaptive measures, including gene expression, accumulation of compatible solutes to protect the cell, hypersensitive response (HR), and programmed cell death (PCD). Several pathogens can counteract and try to reopen stomata. Similarly, pathogens attempt to trigger PCD of host tissue to their benefit. Yet, ABA-induced effects independent of stomatal closure can delay the pathogen spread and infection within leaves. Stomatal closure and other ABA influences can be among the early steps of defense and a crucial component of plants' innate immunity response. Stomatal guard cells are quite sensitive to environmental stress and are considered good model systems for signal transduction studies. Further research on the ABA-induced stomatal closure mechanism can help us design strategies for plant/crop adaptations to stress.

Keywords: guard cells; pathogen resistance; signaling components; stress adaptation; water use.

FIGURE 1

Schematic representation of eventsm during signal transduction pathway induced by ABA leading to stomatal closure. Binding of ABA to its receptor (PYR/PYL/RCAR) blocks the function of PP2C. As a result, OST1, which stays phosphorylated, activates multiple components like NADPH oxidase (to generate ROS) and anion channels [quick anion channel 1 (QUAC1) and slow anion channel 1 (SLAC1)] to trigger anion efflux. The secondary messengers: ROS, NO, and cytosolic Ca²⁺, exert multiple effects. The rise in cytosolic pH, another secondary messenger, appears to stimulate NADPH oxidase, but neither the origin nor the mode of pH action is understood. The high levels of ROS can promote NO production with the involvement of mitogen-activated protein kinases and elevate pH and Ca²⁺ in the cytosol. In turn, Ca²⁺ can activate RBOH-D/F and elevate ROS levels. The rise in NO downregulates K⁺ inward channels and elevates cytosolic Ca²⁺ levels through cyclic guanosine monophosphate (cGMP) and cyclic ADP ribose (cADPR). An increase in Ca²⁺ can activate calcium-dependent protein kinases to facilitate a further influx of Ca²⁺ from outside. Ca²⁺-activated calcium-dependent protein kinases stimulate SLAC1 and S-type anion channel 3 while inhibiting K+ influx through K⁺_in channels. When present, NO activates two enzymes, phospholipase C and phospholipase D (PLD), resulting in the synthesis of inositol 1,4,5-triphosphate (IP₃) phosphatidic acid. In turn, IP₃ releases Ca²⁺ levels from internal stores of plant cells, while phosphatidic acid can stimulate NADPH oxidase and inhibit the inward K⁺ channel. ABA can stimulate the formation of sphingosine 1-phosphate (S1P) and phytosphingosine-1P, which activate PLD through G-protein α-subunit 1 (GPA1). NO can promote K⁺ efflux channels and cytosolic alkalization while inhibiting K⁺ influx channels via calcium-dependent protein kinases. These three secondary messengers involved in ABA signaling, namely ROS, NO, Ca^2+, and their interactions, play a significant role in regulating stomatal closure. Ion channels are terminal points of signal transduction, causing the loss of turgor in guard cells and stomatal closure. Further details are described in the text. Arrows (→) indicate stimulation, and the symbol ⊣ represents inhibition. Abbreviations used here are listed in the Appendix.

FIGURE 2

Stomatal closure induced under conditions of abiotic (e.g., drought) or biotic (e.g., pathogens) stress serves as a common defense mechanism. In guard cells, ABA typically raises the levels of ROS, NO, and Ca²⁺. These three secondary messengers bring out stomatal closure through a series of signaling events (as illustrated in Figure 1). The retention of water within leaves, when stomata are closed, helps to relieve water stress. In parallel, the closed stomata restrict microbial pathogens’ entry into leaves. The trio of ROS, NO, and Ca²⁺ parallelly induce adaptive events to mitigate water stress and limit pathogen spread by triggering HR and PCD. Thus, ROS, NO, and Ca²⁺ can be considered vital regulators, participating in ABA-induced defense against abiotic and biotic stress. Further details are described in the text. Abbreviations used here are listed in the Appendix.