Sulfate is Incorporated into Cysteine to Trigger ABA Production and Stomatal Closure

Abstract

Plants close stomata when root water availability becomes limiting. Recent studies have demonstrated that soil-drying induces root-to-shoot sulfate transport via the xylem and that sulfate closes stomata. Here we provide evidence for a physiologically relevant signaling pathway that underlies sulfate-induced stomatal closure in Arabidopsis (Arabidopsis thaliana). We uncovered that, in the guard cells, sulfate activates NADPH oxidases to produce reactive oxygen species (ROS) and that this ROS induction is essential for sulfate-induced stomata closure. In line with the function of ROS as the secondmessenger of abscisic acid (ABA) signaling, sulfate does not induce ROS in the ABA-synthesis mutant, aba3-1, and sulfateinduced ROS were ineffective at closing stomata in the ABA-insensitive mutant abi2-1 and a SLOW ANION CHANNEL1 loss-of-function mutant. We provided direct evidence for sulfate-induced accumulation of ABA in the cytosol of guard cells by application of the ABAleon2.1 ABA sensor, the ABA signaling reporter ProRAB18:GFP, and quantification of endogenous ABA marker genes. In concordance with previous studies, showing that ABA DEFICIENT3 uses Cys as the substrate for activation of the ABSCISIC ALDEHYDE OXIDASE3 (AAO3) enzyme catalyzing the last step of ABA production, we demonstrated that assimilation of sulfate into Cys is necessary for sulfate-induced stomatal closure and that sulfate-feeding or Cys-feeding induces transcription of NINE-CIS-EPOXYCAROTENOID DIOXYGENASE3, limiting the synthesis of the AAO3 substrate. Consequently, Cys synthesis-depleted mutants are sensitive to soil-drying due to enhanced water loss. Our data demonstrate that sulfate is incorporated into Cys and tunes ABA biosynthesis in leaves, promoting stomatal closure, and that this mechanism contributes to the physiological water limitation response.

Overexpression of the Selective Autophagy Cargo Receptor NBR1 Modifies Plant Response to Sulfur Deficit

“…Furthermore, research from the same group pointed out the links between sulfate and cysteine availability and the abscisic acid (ABA) transduction pathway, especially in stomata closure. It was concluded that the positive effect of sulfate or cysteine on stomatal closure was mediated by ABA because of the sulfur requirement for ABA synthesis [14][15][16]. Previously, we reported that expression of the gene encoding the selective autophagy cargo receptor Joka2 (NtNBR1) in tobacco was induced in plants exposed to sulfur deficit [7].…”

Coping With Water Shortage: An Update on the Role of K+, Cl-, and Water Membrane Transport Mechanisms on Drought Resistance

“…Reactive oxygen species and Ca +2 signaling enter the scene very early and allow shaping and propagation of the signal (Demidchik, 2018). When WD takes place at the soil level, a root-to-shoot transmission of the WD signal seems to be mediated to some extent by sulfate which precedes abscisic acid (ABA) synthesis in leaf tissues (Ernst et al, 2010;Malcheska et al, 2017;Batool et al, 2018). However, when WD is produced by low air humidity, this condition is perceived by guard cells which synthesize ABA and, then, stomata close (Bauer et al, 2013).…”

Plastid Sulfate Transporters Open Doors to Abiotic Stress Resistance

“…1). Despite the limited nutrient uptake from the soil during drought, SO 4 22 quickly accumulates in the xylem sap, is transported toward green tissues, is imported into the chloroplasts, and ultimately causes an increase in ABA and stomatal closure (Malcheska et al, 2017;Batool et al, 2018). Chen et al (2019) now show that this rapid drought response depends on all five SULTR3 transporters, resulting in an 80% reduction in ABA levels in the quintuple mutant compared with wildtype plants.…”