Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana

Abstract

Pharmacological, laser scanning confocal microscopic (LSCM), real-time PCR and spectrophotographic approaches are used to study the roles of hydrogen sulfide (H 2 S) and nitric oxide (NO) in signaling transduction of stomatal movement response to ethylene in Arabidopsis thaliana. In the present study, inhibitors of H 2 S synthesis were found to block ethylene-induced stomatal closure of Arabidopsis. Treatment with ethylene induced H 2 S generation and increased L-/D-cysteine desulfhydrase (pyridoxalphosphate-dependent enzyme) activity in leaves. Quantitative PCR analysis showed AtL-CDes and AtD-CDes transcripts were induced by ethylene. It is suggested that ethylene-induced H 2 S levels and L-/D-cysteine desulfhydrase activity decreased when NO was compromised. The data clearly show that ethylene was able to induce H 2 S generation and stomatal closure in Atnoa1 plants, but failed in the Atnia1,nia2 mutant. Inhibitors of H 2 S synthesis had no effect on ethylene-induced NO accumulation and nitrate reductase (NR) activity in guard cells or leaves of Arabidopsis, whereas ethylene was able to induce NO synthesis. Therefore, we conclude that H 2 S and NO are involved in the signal transduction pathway of ethylene-induced stomatal closure. In Arabidopsis, H 2 S may represent a novel downstream indicator of NO during ethylene-induced stomatal movement. hydrogen sulfide, nitric oxide, L-/D-cysteine desulfhydrase, Arabidopsis thaliana, ethylene, stomatal closure Citation: Liu J, Hou L X, Liu G H, et al. Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana.

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

“…In plants, although originally associated with plant-pathogen interaction, it is now known to have an active role in diverse physiological processes such as oxidative stress, germination, and heat tolerance (Zhang et al, 2009a(Zhang et al, , 2009b(Zhang et al, , 2010a(Zhang et al, , 2010b(Zhang et al, , 2010dLi et al, 2013aLi et al, , 2013b. Recently, H 2 S has been proven to participate in ABA-or ethylene-induced stomatal closure in different plant species (García-Mata and Lamattina, 2010; Liu et al, 2011Liu et al, , 2012Jin et al, 2013). Moreover, it has been reported also that H 2 S induces stomatal opening (Lisjak et al, 2010(Lisjak et al, , 2011.…”

“…Differences in methodological procedures concerning the isolation of epidermal strips and the timing of the treatments may result in the differential response of the guard cells to the H 2 S donors between Lisjak et al (2010) and this study. Liu et al (2011) showed that stomatal closure but not NO synthesis is impaired in an Arabidopsis mutant of the L-Cys desulfhydrase AtL-CDES gene. Therefore, they suggest that NO is acting upstream of H 2 S in ethyleneinduced stomatal closure.…”

“…It has been demonstrated that, in animal systems, H 2 S and NO might interact either in an agonistic or antagonistic way, depending on the biological system and physiological process (Li et al, 2009;Kajimura et al, 2010;Yong et al, 2010). In plants, it has been recently reported that H 2 S acts downstream of NO in ethyleneinduced stomatal closure (Liu et al, 2011(Liu et al, , 2012. It was also reported that H 2 S reduces ABA-dependent NO production in Arabidopsis and Capsicum annuum guard cells (Lisjak et al, 2010(Lisjak et al, , 2011.…”

“…Using a H 2 S-releasing compound, H 2 S was later reported to confer a protective effect against oxidative (Zhang et al, 2009b(Zhang et al, , 2010b and cadmium (Sun et al, 2013) stresses, alleviate aluminum toxicity (Zhang et al, 2010c), increase antioxidant activity, and participate in root organogenesis (Zhang et al, 2009a). Several independent groups have recently reported the participation of H 2 S in ABA-and ethylene-dependent stomatal closure induction (García-Mata and Lamattina, 2010;Liu et al, 2011Liu et al, , 2012Jin et al, 2013). In this study, we used the characterized DES1 knockout Arabidopsis (Arabidopsis thaliana) mutant plants des1-1 and des1-2 to obtain new insights on the cross talk between H 2 S and NO and further evidence supporting the involvement and requirements of H 2 S in ABA-induced signaling cascade leading to stomatal closure.…”

Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings

“…In plant systems, hydrogen sulfide has been found to play multiple physiological roles in plant growth, development and the acquisition of stress tolerance like heat tolerance (Lisjak et al 2010(Lisjak et al , 2013Li 2013). The novel functions of hydrogen sulfide have been uncovered in seed germination (Zhang et al 2010a;Li et al 2012a), root organogenesis (Zhang et al 2009a) and stomata movement (Lisjak et al 2010;Liu et al 2011;Jin et al 2013), as well as in alleviation in osmotic stress (Zhang et al 2009b), salt stress (Wang et al 2012), oxidative stress (Shan et al 2011, heavy metal stress (Zhang et al 2008(Zhang et al , 2010bChen et al 2013) and pathogen infection (Bloem et al 2011). Our previous results also showed that pretreatment with sodium hydrosulfide (NaHS), a hydrogen sulfide donor, could improve resistance of tobacco cells (Li et al 2012b) and maize seedlings (Li et al 2013a(Li et al ,b, 2014 to high temperature, but its mechanism is not fully clear.…”