Hydrogen Sulfide Generated byl-Cysteine Desulfhydrase Acts Upstream of Nitric Oxide to Modulate Abscisic Acid-Dependent Stomatal Closure    

Abstract

Abscisic acid (ABA) is a well-studied regulator of stomatal movement. Hydrogen sulfide (H 2 S), a small signaling gas molecule involved in key physiological processes in mammals, has been recently reported as a new component of the ABA signaling network in stomatal guard cells. In Arabidopsis (Arabidopsis thaliana), H 2 S is enzymatically produced in the cytosol through the activity of L-cysteine desulfhydrase (DES1). In this work, we used DES1 knockout Arabidopsis mutant plants (des1) to study the participation of DES1 in the cross talk between H 2 S and nitric oxide (NO) in the ABA-dependent signaling network in guard cells. The results show that ABA did not close the stomata in isolated epidermal strips of des1 mutants, an effect that was restored by the application of exogenous H 2 S. Quantitative reverse transcription polymerase chain reaction analysis demonstrated that ABA induces DES1 expression in guard cell-enriched RNA extracts from wild-type Arabidopsis plants. Furthermore, stomata from isolated epidermal strips of Arabidopsis ABA receptor mutant pyrabactin-resistant1 (pyr1)/pyrabactin-like1 (pyl1)/pyl2/pyl4 close in response to exogenous H 2 S, suggesting that this gasotransmitter is acting downstream, although acting independently of the ABA receptor cannot be ruled out with this data. However, the Arabidopsis clade-A PROTEIN PHOSPHATASE2C mutant abscisic acid-insensitive1 (abi1-1) does not close the stomata when epidermal strips were treated with H 2 S, suggesting that H 2 S required a functional ABI1. Further studies to unravel the cross talk between H 2 S and NO indicate that (1) H 2 S promotes NO production, (2) DES1 is required for ABA-dependent NO production, and (3) NO is downstream of H 2 S in ABA-induced stomatal closure. Altogether, data indicate that DES1 is a unique component of ABA signaling in guard cells.Abscisic acid (ABA) regulates diverse physiological and developmental processes in plants, among which seed dormancy and stomatal movement are the most studied. Stomata are pores bordered by pairs of specialized cells named guard cells located in the epidermis of the aerial part of most land plants. Due to the waxy cuticle of plants, stomatal pores regulate approximately 90% of all the gas exchange (i.e. the uptake of CO 2 required for photosynthesis and the loss of water vapor during transpiration) between the plant and the environment (Hetherington and Woodward, 2003). Thus, stomatal movement is a key process for the regulation of plant water status and biomass production. In guard cells, ABA induces an increase of intracellular calcium concentrations, which, in turn, induces an efflux of anions that causes membrane depolarization. In this voltage milieu, ion uptake is blocked through the inactivation of inward-rectifying potassium channels, and ion efflux is induced through activation of outward-rectifying potassium channels. This solute relocation drives water out of the guard cells and closes the stomatal pore as a result of a reduction in guard cell turgor (Blatt, 2000;Kim et al...

Negative regulation of autophagy by sulfide in Arabidopsis thaliana is independent of reactive oxygen species

“…Alterations of hydrogen sulfide metabolism have important pathological consequences, establishing the clinical relevance of this molecule (Łowicka and Bełtowski, 2007;Szabó, 2007;Wang, 2012). In addition to the protective effects of hydrogen sulfide against a wide array of different stresses that have been demonstrated in plants (Zhang et al, 2008Wang et al, 2010;Jin et al, 2011;Dawood et al, 2012;Li et al, 2012aLi et al, , 2012bCheng et al, 2013;Christou et al, 2013;Sun et al, 2013), this molecule has also been shown to regulate plant processes that are critical for plant performance, such as photosynthesis (Chen et al, 2011), stomatal movement (García-Mata and Lamattina, 2010;Lisjak et al, 2010;Scuffi et al, 2014), and autophagy (Álvarez et al, 2012b; Gotor et al, 2013). In this study, we provide new experimental evidence that, together with our previous findings, demonstrates the role of hydrogen sulfide in regulating the progression of autophagy independently of the condition in which the autophagy originates.…”

“…Interestingly, hydrogen sulfide also has been identified as a component of the abscisic acid signaling pathway in guard cells (García-Mata and Lamattina, 2010;Lisjak et al, 2010). Recently, it was demonstrated that sulfide acts upstream of NO to modulate abscisic acid-dependent stomatal closure (Scuffi et al, 2014). The cross talk between NO and sulfide also has been suggested based on the induced alleviation of cadmium toxicity in alfalfa seedlings , the improved heat tolerance of maize (Zea mays) seedlings , and the enhanced salinity tolerance of alfalfa seeds during germination (Wang et al, 2012b).…”

“…This effect is restored by the application of exogenous sulfide or genetic complementation, demonstrating the involvement of DES1 in abscisic acid signaling in guard cells. Further studies have shown that DES1 is required for abscisic acid-dependent NO production (Scuffi et al, 2014). Thus, in plant cells, DES1 could be responsible for modulating the generation of sulfide for important signaling processes Gotor et al, 2015) such as autophagy.…”

Hydrogen Sulfide Regulates Inward-Rectifying K+ Channels in Conjunction with Stomatal Closure

“…H 2 S action was originally related to pathogenesis resistance (Bloem et al, 2004), but in the last decade it has been proven to have an active role in signaling, participating in key physiological processes, such as germination and root organogenesis (Zhang et al, 2008(Zhang et al, , 2009a, heat stress (Li et al, 2013a(Li et al, , 2013b, osmotic stress (Zhang et al, 2009b), and stomatal movement (García-Mata and Lamattina, 2010;Lisjak et al, 2010Lisjak et al, , 2011Jin et al, 2013). Moreover, H 2 S was reported to participate in the signaling of plant hormones, including abscisic acid (ABA; García-Mata and Lamattina, 2010;Lisjak et al, 2010;Jin et al, 2013;Scuffi et al, 2014), ethylene (Hou et al, 2013), and auxin (Zhang et al, 2009a).…”

Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity

“…The L-DES was also shown to regulate the L-cysteine homeostasis in Arabidopsis (Álvarez et al 2010). Under physiological conditions, DES1 expression, which encodes for L-DES, was induced by abscisic acid in Arabidopsis guard cells (Scuffi et al 2014). Furthermore, the treatment of alfalfa (Medicago sativa) or tobacco with high NaCl concentrations enhanced L-DES activity (Lai et al 2014;da-Silva et al 2017).…”