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Acta Botanica Brasilica

Print version ISSN 0102-3306On-line version ISSN 1677-941X

Acta Bot. Bras. vol.32 no.1 Belo Horizonte Jan./Mar. 2018  Epub Oct 19, 2017 


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

Cristiane J. da-Silva1 

Luzia V. Modolo1  * 

1Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Pres. Antônio Carlos, 6627, Pampulha, 31270-901, Belo Horizonte, MG, Brazil


High salinity affects plants due to stimulation of osmotic stress. Cell signaling triggered by nitric oxide (NO) and hydrogen sulfide (H2S) activates a cascade of biochemical events that culminate in plant tolerance to abiotic and biotic stresses. For instance, the NO/H2S-stimulated biochemical events that occur in plants during response to high salinity include the control of reactive oxygen species, activation of antioxidant system, accumulation of osmoprotectants in cytosol, induction of K+ uptake and Na+ cell extrusion or its vacuolar compartmentation among others. This review is a compilation of what we have learned in the last 10 years about NO participation during cell signaling in response to high salinity as well as the role of H2S, a new player in the mechanism of plant tolerance to salt stress. The main sources of NO and H2S in plant cells is also discussed together with the evidence of interplay between both signaling molecules during response to stress.

Keywords abiotic stress; cell signaling; hydrogen sulfide; nitric oxide; NO and H2S biosynthesis; salt stress


It is estimated that over 800 million hectares of land throughout the world are overloaded with salt, which represents more than 6 % of the world’s total land area (Munns & Tester 2008). High salinity leads to osmotic stress, cell toxicity by ions excess and ultimately nutrition disorders and oxidative stress in plants (Munns & Tester 2008). A signaling cascade involving expression of specific genes and accumulation of certain metabolites is pivotal for plants successfully acclimating and tolerating high salinity (Gupta & Huang 2014). Nitric oxide (NO), and more recently hydrogen sulfide (H2S), were recognized as important players in cell signaling triggered during plant response to biotic and abiotic stresses (Delledonne et al. 1998; Durner et al. 1998; Zhang et al. 2008). The role of these signaling molecules in salt stress has been explored over the past few years.

The NO is a gaseous free radical widely produced in living organisms. Its production was first reported in plants by Dr. Lowell Klepper by the end of the 1970s (Klepper 1979). Nevertheless, the advent of researches focusing on NO in plants took place 19 years later (Delledonne et al. 1998; Durner et al. 1998) when Drs. Robert F. Furchgott, Louis J. Ignarro and Ferid Murad were jointly laureate with the Nobel Prize for the disclosure of NO as an endothelium-derived relaxing factor in mammals. Since then, NO has been shown to influence plant response to salt stress by improving seed vigor and germination (Hayat et al. 2012) and controlling the cellular levels of reactive oxygen species (ROS) (Keyster et al. 2012; Ahmad et al. 2016), nutrient (Kong et al. 2016; Liu et al. 2016) and osmoprotectants (Wu et al. 2011; Tian et al. 2015). The NO biosynthesis in plant cells can occur by non-enzymatic and enzymatic means. Nitrite (NO2 -) or nitrate (NO3 -), in the presence of ascorbic acid (AsA), may be non-enzymatically converted to NO (Klepper 1990). The acidic condition of aleurone layers was also demonstrated to favor NO production in apoplast (Bethke et al. 2004). The light-dependent production of NO from nitrogen dioxide, assisted by carotenoids, has been reported (Cooney et al. 1994). On the other hand, the enzymatic mechanisms that drive NO production in plant cells are still under debate since a plethora of examples are reported in the literature.

The H2S is a small and lipophilic molecule that was pointed out as a possible cellular signaling component in mammalians (Abe & Kimura 1996). Indeed, H2S is considered the third gas transmitter in addition to NO and carbon monoxide (Wang 2002). Its ability to induce seed germination and relief copper stress was demonstrated in the late 2000s (Zhang et al. 2008). However, earlier H2S was believed to be exclusively phytotoxic. Since then, H2S was implicated in the ROS control through the activation of antioxidant system (Yu et al. 2013; Shan et al. 2014; da-Silva et al. 2017), maintenance of high K+/Na+ ratio (Lai et al. 2014; Deng et al. 2016) and accumulation of osmolytes (Shi et al. 2013) during plant response to high salt concentrations. Recent research demonstrates that H2S is primarily produced in plant tissues from L/D-cysteine or sulfide (Li 2015).

This review describes the main enzymatic sources of NO and H2S in plants and compiles what it is known from the past 10 years on the role of these signaling molecules during plants response to high salinity.

Biosynthesis of NO and H 2 S in plant cells

Enzymes involved in NO biosynthesis

A body of evidence indicates that the production of NO in plant cells may come from both reductive and oxidative pathways (Fig. 1). Reductive mechanisms for NO synthesis include NO3 - or NO2 - as the primary substrates for nitrate reductase (NR), a plasma membrane-bound nitrite:NO reductase (NI-NOR), a mitochondrial protein system or xanthine oxidoreductase (XOR). The oxidative pathway comprises the polyamines and hydroxylamines metabolisms by still unknown mechanisms (Fig. 1).

Figure 1 Schematic representation of the main pathways of NO and H2S production reported in plant cells. CAS, β-cyanoalanine synthase; CS, cysteine synthase; D/L-DES, D/L-cysteine desulfhydrase; HA, hydroxylamines; H 2 S, hydrogen sulfide; NI-NOR, plasma membrane-bound nitrite-nitric oxide reductase; NiR, nitrite reductase; NO, nitric oxide; NR, nitrate reductase; PA, polyamines; SiR, sulfite reductase; XOR, xanthine oxidoreductase. 

The NR, a cytosolic enzyme, is able to catalyze directly or indirectly the NO production from NO3 - (Yamasaki & Sakihama 2000; Modolo et al. 2005). The genes Nia1 and Nia2 encode for NR in Arabidopsis thaliana (Wilkinson & Crawford 1993). This enzyme promotes the NAD(P)H-dependent reduction of NO3 - to NO2 - and then to NO (Magalhaes et al. 2000; Yamasaki & Sakihama 2000). The direct production of NO from NR, however, represents only 1(2 % of the nitrate-reducing capacity of this enzyme (Rockel et al. 2002; Planchet et al. 2005). This is because relatively high amounts of NO2 - (K M = 100 µM) are required for NR reducing NO2 - to NO, while the formation of NO is prevented in the presence of NO3 - in amounts as low as 50 µM (Rockel et al. 2002). The NR can also indirectly contribute to NO production by catalyzing the formation of the substrate (NO2 -) for other enzymatic systems. For instance, in vitro experiments showed that a plasma membrane-bound protein (NI-NOR) of tobacco (Nicotiana tabacum) roots was able to reduce NO2 - to NO (Stöhr et al. 2001) that, in turn, yielded higher rates of tobacco root colonization by the arbuscular mycorrhizal Glomus mosseae (Moche et al. 2010). However, the gene that encodes for NI-NOR, the protein amino acid sequence and the electron donor that assists the NO2 - reduction remain unknown. Mitochondrial activities were also determined to contribute to NO production from NO2 - in Arabidopsis plants, tobacco cell suspensions and Oryza sativa (rice) (Modolo et al. 2005; Planchet et al. 2005; Stoimenova et al. 2007). The reduction of NO2 - to NO has also been reported to be catalyzed by the peroxisomal enzyme XOR. This enzyme mainly catalyzes the formation of uric acid and O2 - from xanthine oxidation. However, formation of NO from NO2 - was observed to be assisted by XOR in the presence of NADH or xanthine as reducing agents (Li et al. 2004). Production of O2 - or NO was recorded in pea (Pisum sativum) and attributed to XOR activity, depending on the cell redox state (Del Río et al. 2004) while white lupin (Lupinus albus) roots upon phosphate deficiency produced NO via XOR (Wang et al. 2010). The nitrite reductase (NiR) was also shown to be a possible source of NO in spinach (Spinacia oleracea) chloroplasts via reduction of NO2 - assisted by ferredoxin. Then, NO would be a byproduct of the pathway that leads to NH4 + formation (Kuznetsova et al. 2004). The affinity of NO2 - for mitochondrial NiR (mNiR) was determined to be very low, indicating that NO production via mNiR activity is only relevant under conditions in which NO2 - accumulates in the organelle, such as hypoxia (Gupta et al. 2011).

Metabolization of polyamines constitutes an example of oxidative process that might drive NO production in plant cells. Arabidopsis supplemented with exogenous polyamines exhibited increased NO production in cells (Tun et al. 2006). Similar results were found in cadmium-stressed wheat (Triticum aestivum) (Groppa et al. 2008) and drought-stressed cucumber (Cucumis sativus) (Arasimowicz-Jelonek et al. 2009). The increment of arginase activity in tobacco leaves upon high salinity was recently determined to be accompanied of NO accumulation in cells (da-Silva et al. 2017). Arginase catalyzes the conversion of L-arginine to urea and L-ornithine, in which the latter may originate polyamines (e.g. putrecine, spermidine and/or spermine). The mechanism by which polyamines are oxidized to NO still remains to be elucidated. Another potential oxidative pathway that leads to NO production includes hydroxylamine as substrate. Treatment of NR-deficient tobacco cell cultures with exogenous hydroxylamine resulted in cellular accumulation of large amounts of NO (Rümer et al. 2009). The NO biosynthesis from the oxidation of hydroxylamine is believed to be involved in the regulation of ROS levels in plant cells, especially during the reoxygenation of anoxic tissues (Rümer et al. 2009). Nonetheless, both, the enzymatic system involved in the hydroxylamine-dependent NO formation and the site where such pathway takes place are still unknown. Many authors suggest that plant cells are also able to produce NO from L-arginine oxidation, with concomitant formation of L-citrulline, in a reaction catalyzed by a nitric oxide synthase (NOS)-like enzyme as it occurs in mammalian cells. Despite that, no gene or protein that encodes for an NOS-like enzyme has been so far isolated from plant cells. Likewise, the Nitric Oxide-Associated protein 1 (ATNOA1) of Arabidopsis (Guo et al. 2003) was initially believed to catalyze NO biosynthesis from L-arginine oxidation. Instead, evidence suggests that ATNOA1 somehow modulates NO accumulation in plant cells according to environmental conditions as ATNOA1-defective mutant plants may present normal NO levels (Moreau et al. 2008).

Enzymes involved in H 2 S biosynthesis

Five enzymatic systems have been reported to contribute to H2S biosynthesis in plant cells (Li 2015; Fig. 1). The majority of publications that deal with H2S production in plants usually focus on the activity of L-cysteine desulfhydrase (L-DES) (Romero et al. 2013), a cytoplasmic enzyme that converts L-cysteine to pyruvate with release of H2S and NH4 + (Harrington & Smith 1980; Álvarez et al. 2010; Li 2015), using pyridoxal phosphate as a cofactor (Calderwood & Kopriva 2014). 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). The L-DES was also stimulated in heat-stressed maize (Zea mays) plants incubated with salicylic acid or H2O2 (Li et al. 2015). Arabidopsis mutant plants exhibiting low expression of LCD, an L-DES encoding gene, presented low H2S levels under drought conditions (Jin et al. 2013). In addition to L-DES, D-DES catalyzes the production of H2S in plant cells by metabolizing D-cysteine, instead (Riemenschneider et al. 2005). Despite similar functions with discrimination of cysteine enantiomers, L-DES and D-DES are not related to each other and their physiological implications remain to be clarified (Calderwood & Kopriva 2014). The expression of DCD1 (a D-DES gene) increased in cadmium-stressed chinese cabbage (Brassica rapa), which resulted in H2S accumulation in cells (Zhang et al. 2015). Increment of D-DES activity in a time-dependent manner was reported in salt-stressed alfalfa (Cui et al. 2014).

The mitochondrial enzyme β-cyanoalanine synthase (CAS) catalyzes the condensation of L-cysteine to cyanide (CN-) to yield H2S (Akopyan et al. 1975; Hatzfeld et al. 2000; Li 2015). Its activity helps plant to control the cell levels of CN- during ethylene production as this anion is a potent inhibitor of mitochondrial respiratory chain. Cysteine synthase (CS), present in cytosol, mitochondria and chloroplasts, catalyzes the reversible reaction between L-cysteine and acetate to form O-acetyl-L-serine and H2S (Wirtz & Hell 2006; Li 2015). It is also documented that high concentrations of NaCl stimulated CAS and CS activities in tobacco and resulted in H2S accumulation in leaves (da-Silva et al. 2017). Besides these sources, plant cells are able to reduce SO3 2- to H2S in the presence of ferredoxin and sulfite reductase (SiR), a chloroplast enzyme (Nakayama et al. 2000; Li 2015). The SO3 2- may originate from either SO4 2- (through sulphur nutrition) or SO2 (uptaken from atmosphere). In this sense, SO4 2- is activated by ATP sulfurylase to form adenosine 5′-phosphosulfate (APS). The formed APS is further reduced to SO3 2- via APS reductase activity (Nakayama et al. 2000; Li 2015). Notably, salt-stressed tobacco plants presented decreased SiR activity explained by the occurrence of stomatal closure, a condition that prevented SO2 from entering into plant leaves (da-Silva et al. 2017). Therefore, the enzymes L-DES, CAS and CS, but not SiR, contribute to H2S biosynthesis during tobacco response to high salinity.

Cell signaling in salt-stressed plants mediated by NO and H 2 S

Integrated plant cell signaling must be orchestrated to provide with metabolic and structural changes for individuals survival and tolerance to salt stress. The next three sections will focus on current knowledge about NO and H2S roles during plant responses to high salinity.

Nitric oxide

Important roles have been ascribed to NO in plants tolerance to abiotic stress, in which the increment of this signaling molecule in cells was associated to a variety of strategies used by plants to cope high salinity (Tab. 1). The Atnoa1 Arabidopsis mutant plants, that exhibit impaired NO biosynthesis, were demonstrated to be highly sensitive to high salinity, being more vulnerable to oxidative stress and presenting lower germination and survival rates under such condition (Zhao et al. 2007).

Table 1: Roles of nitric oxide (NO) during plant response to salt stress. 

NO effect Plant species
Activation of antioxidant system Aegiceras corniculatum (Chen et al. 2014) Cucumis sativus (Fan et al. 2007) Cynodon dactylon (Liu et al. 2016) Glycine max (Simaei et al. 2012) Gossypium hirsutum (Dong et al. 2014) Helianthus annuus (Arora & Bhatla 2015; Kaur & Bhatla 2016) Hordeum vulgare (Li et al. 2008) Nicotiana tabacum (da-Silva et al. 2017) Solanum lycopersicum (Manai et al. 2014) Spinacia oleracea (Du et al. 2015) Triticum aestivum (Zheng et al. 2008; Hasanuzzaman et al. 2011)
Increase of K+/Na+ ratio Avicennia marina (Chen et al. 2010) Cucumis sativus (Shi et al. 2007) Cynodon dactylon (Liu et al. 2016) Gossypium hirsutum (Liu et al. 2013; Kong et al. 2016) Kandelia obovata (Lang et al. 2014) Aegiceras corniculatum (Lang et al. 2014) Limonium bicolor (Ding et al. 2013) Populus euphratica (Zhang et al. 2007) Triticum aestivum (Tian et al. 2015)
Induction of osmoregulators accumulation Brassica juncea (Zeng et al. 2011; Khan et al. 2012) Cicer arietinum (Ahmad et al. 2016) Cucumis sativus (Fan et al. 2013) Gossypium hirsutum (Liu et al. 2013) Lycopersicom esculentum (Wu et al. 2011) Solanum lycopersicum (Hayat et al. 2012) Triticum aestivum (Tian et al. 2015)
Induction of polyamines accumulation Cucumis sativus (Fan et al. 2013)
Protection of photosynthetic apparatus Brassica juncea (Fatma et al. 2016) Cicer arietinum (Ahmad et al. 2016) Fragaria × ananassa (Christou et al. 2014) Gossypium hirsutum (Kong et al. 2016) Medicago truncatula (Jian et al. 2016)
Stimulation of seed germination Arabidopisis thaliana (Zhao et al. 2007) Triticum aestivum (Zheng et al. 2008) Zea mays (Bai et al. 2011)
Stimulation of plant growth Arabidopisis thaliana (Liu et al. 2015) Glycine max (Egbichi et al. 2014; Vaishnav et al. 2016) Gossypium hirsutum (Liu et al. 2014)

Activation of the antioxidant system is one of the NO roles in plants under salt stress. Several findings indicate an improvement in the performance of enzymatic and non-enzymatic antioxidant systems in salt-stressed plants treated with NO donors. Cucumber seedlings hydroponically grown in medium containing 50 mM NaCl and 100 μM sodium nitroprusside (SNP; NO+ donor) showed higher activity of superoxide dismutase (SOD), catalase (CAT), peroxidase and ascorbate peroxidase (APX) when compared to cucumber solely treated with 50 mM NaCl (Fan et al. 2007). As a result, cells from these seedlings presented lower membrane permeability and decreased levels of O2 -, H2O2 and lipid peroxides (Fan et al. 2007). The NO was found to have dual role on SOD by positively modulating the FeSOD expression and negatively affecting Cu/ZnSOD one. With this, NO furnished a differential antioxidant protection to salt-stressed sunflower (Helianthus annuus) seedlings (Arora & Bhatla 2015). Likewise, the challenge of tobacco roots with NaCl led to accumulation of endogenous NO in leaves that was accompanied by an increment of SOD and CAT activities (da-Silva et al. 2017). The activity of monodehydroascorbate reductase, dehydroascorbate reductase (DHAR), glutathione reductase (GR), glutathione S-transferase, glutathione peroxidase (GPX), glyoxalase I and glyoxalase II (both related to methylglyoxylate detoxification) was also stimulated by SNP in wheat plants treated with 300 mM NaCl (Hasanuzzaman et al. 2011). Induction of non-enzymatic antioxidant system [AsA and reduced glutathione (GSH)] was observed in wheat seedlings treated with SNP prior to NaCl exposure (Hasanuzzaman et al. 2011). The treatment with SNP decreased ferritin levels in barley (Hordeum vulgare) seedlings, which contributed to the attenuation of oxidative stress triggered by high salinity (Li et al. 2008). Likewise, exogenous NO alleviated high-salinity-triggered oxidative stress in soybean (Glycine max; Simaei et al. 2012), mangrove (Aegiceras corniculatum; Chen et al. 2014), tomato (Solanum lycopersicum; Manai et al. 2014), cotton (Gossypium hirsutum; Dong et al. 2014), spinach (Du et al. 2015), sunflower (Kaur & Bhatla 2016) and bermudagrass (Cynodon dactylon; Liu et al. 2016).

The protective role of NO on plant photosynthetic apparatus is also documented. The SNP at 100 µM restored chloroplast pigments and maximum photochemical efficiency of photosystem II to normal levels in strawberries (Fragaria × ananassa cv. ‘Camarosa’) plants challenged with high salinity (Christou et al. 2014). Similar results were observed in salt-stressed cotton seedlings wherein application of 100 µM SNP to leaves improved plants photosynthetic performance (Liu et al. 2014). The treatment of chickpea (Cicer arietinum) plants with 100 mM NaCl and 50 µM of S-nitroso-N-acetylpenicillamine (SNAP; an NO donor) provided higher amounts of chlorophylls a and b and carotenoids in plant leaves in comparison with those solely treated with NaCl (Ahmad et al. 2016). Aspersion of salt-stressed cotton plants with SNP delayed leaf senescence and increased chlorophylls content and photosynthetic rate (Kong et al. 2016). The NO and sulfur nutrition were found to prevent chloroplasts damage in salt-exposed mustard (B. juncea) plants (Fatma et al. 2016). The SNP stimulated the expression of AOX, a component of plant mitochondrial electron transport, in barrelclover (M. truncatula) under high salinity thus, alleviating oxidative stress and photosynthetic damages (Jian et al. 2016).

Inhibition of plasma membrane H+-ATPase and tonoplast H+-PPase caused by NaCl was prevented by 50 µM SNP in cucumber plants (Shi et al. 2007). Additionally, the gene expression of a plasma membrane H+-ATPase was stimulated by SNP in salt-stressed calluses of desert poplar (Populus euphratica), which in turn resulted in higher K+/Na+ ratio (Zhang et al. 2007). Plasma membrane H+-ATPase and tonoplast Na+/H+ antiporter proteins were also induced by SNP in salt-stressed Avicennia marina and caused an increment of K+/Na+ ratio due to Na+ efflux from cells towards salt glands (Chen et al. 2010). Similar results were observed in cotton (Kong et al. 2016), Kandelia obovate and A. corniculatum (Lang et al. 2014). Besides intense Na+ secretion from sea-lavender (Limonium bicolor) leaves under stress, SNP caused an increment in the number of Na+-loaded salt glands in salt-stressed plants (Ding 2013). In addition to increasing K+/Na+ ratio, SNP enhanced Ca2+ and Mg2+ uptake in salt-stressed plants (Liu et al. 2013; Tian et al. 2015; Liu et al. 2016).

Osmotic stress is a phenomenon also observed in plants under high salinity (Parihar et al. 2015). Soybean plants incubated with SNP prior to salt stress exhibited higher relative water content (RWC) than salt-stressed plants devoid of NO treatment (Dinler et al. 2014). Exogenous NO also stimulated proline accumulation in several plant species (Wu et al. 2011; Zeng et al. 2011; Hayat et al. 2012; Khan et al. 2012; Fan et al. 2013; Liu et al. 2013). The activity of pyrroline-5-carboxylate synthetase and proline dehydrogenase, enzymes involved in L-proline biosynthesis, and L-proline accumulation were boosted by SNP in cucumber seedlings under high salinity (Fan et al. 2013). Then, cellular turgor was maintained at normal levels and seedlings overcame NaCl stress. Mustard plants subjected to salt stress exhibited higher amounts of glycine betaine when treated with SNP (Khan et al. 2012), while wheat plants accumulated soluble carbohydrates in cells (Tian et al. 2015). The NO released from SNAP also induced accumulation of L-proline, L-glycine betaine, soluble proteins and carbohydrates in leaves of salt-stressed chickpea (Ahmad et al. 2016).

The combined treatment of cucumber seedlings with NaCl and SNP caused an increment of spermine levels and (spermidine + spermine)/putrescine ratio, which in turn helped plant cells to cope with the abiotic stress imposed (Fan et al. 2013). Polyamines, such as spermine and spermidine allows for protein, nucleic acid and cell membrane stabilization, besides being great osmolytes and inducers of plant growth and development (Fan et al. 2013).

The SNP-induced germination of salt-stressed wheat seeds was attributed to the maintenance of K+/Na+ balance, increase of SOD and CAT activities and decrease of the lipid peroxides, H2O2 and O2 - levels (Zheng et al. 2008). The SNAP, together with G-proteins, induced the protein accumulation, the antioxidant enzymes activity, the proteins related to cell defense, the energy metabolism and the cell division in salt-treated maize seedlings (Bai et al. 2011).

The application of an NO donor on NaCl-treated soybean improved plants growth and biomass accumulation in shoot, root and nodules (Egbichi et al. 2014; Vaishnav et al. 2016). Indeed, the NaCl-triggered disruption of Pseudomonas simiae (rhizobacteria) colonization in soybean was reverted by 100 µM SNP and allowed plant to tolerate salt stress (Vaishnav et al. 2016). Conversely, increased levels of NO triggered the decrease of root meristems growth through auxin depletion in NaCl-treated Arabidopsis (Liu et al. 2015). In fact, removal of endogenous NO from roots rescued, in part, PIN expression and destabilized IAA17 protein, involved in the repression of auxin signaling.

Hydrogen sulfide

Many physiological processes were also found to be regulated by H2S in plants capable to tolerate different types of stress, including high salinity (Tab. 2).

Table 2: Roles of hydrogen sulfide (H2S) during plant response to salt stress. 

H 2 S effect Plant species
Activation of antioxidant system Cucumis sativus (Yu et al. 2013; Sun & Luo 2014) Cynodon dactylon (Shi et al. 2013) Fragaria × ananassa (Christou et al. 2013) Medicago sativa (Wang et al. 2012; Lai et al. 2014) Nicotiana tabacum (da-Silva et al. 2017) Oryza sativa (Mostofa et al. 2015) *Triticum aestivum (Khan et al. 2017) Zea mays (Shan et al. 2014)
Increase of K+/Na+ ratio Fragaria × ananassa (Christou et al. 2013) Hordeum vulgare (Chen et al. 2015) Medicago sativa (Lai et al. 2014) Triticum aestivum (Deng et al. 2016)
Protection of photosynthetic apparatus Fragaria × ananassa (Christou et al. 2013) Oryza sativa (Mostofa et al. 2015)
Stimulation of seed germination and plant growth Arabidopsis thaliana (Li et al. 2014) Cucumis sativus (Sun & Luo 2014) Cynodon dactylon (Shi et al. 2013) Medicago sativa (Wang et al. 2012)
Induction of osmoregulators accumulation Cucumis sativus (Sun & Luo 2014) Cynodon dactylon (Shi et al. 2013) Oryza sativa (Mostofa et al. 2015)

*Osmotic stress using PEG8000

Oxidative burst, an uncontrolled overproduction of ROS, is one of the first events elicited in plants cell upon salt stress, leading to intensification of electrolytes leakage, lipid peroxidation and protein oxidation. In fact, mitigation of oxidative stress in salt-stressed plants is one of the most studied roles of H2S. The activities of SOD, CAT, APX, GR, GPX and DHAR in stressed cucumber seedlings were increased by treatment with NaHS (an H2S-donor) while H2O2 and lipid peroxide levels decreased under the same experimental conditions (Yu et al. 2013). Undeniably, the suppression of endogenous H2S by infiltration of tobacco leaves with hypotaurine negatively affected the activity of SOD, CAT and APX in NaCl stress plants (da-Silva et al. 2017). The activity of enzymes involved in GSH (γ-glutamylcysteine synthetase) and AsA (L-galactono-1,4-lactone dehydrogenase) biosyntheses and further increment of GSH/oxidized glutathione and AsA/DHR ratios were stimulated by NaHS in leaves of salt-treated maize (Shan et al. 2014). Similarly to the observed for NO donors, NaHS controlled methylglyoxylate levels in rice by increasing the activity of glyoxalase I and glyoxalase II (Mostofa et al. 2015). In addition, NaHS decreased in plants the activity of lipoxygenase, an enzyme implicated in the formation of lipid peroxides. Alleviation of NaCl-induced oxidative stress by H2S exogenous was also observed in alfalfa, bermudagrass, strawberry and cucumber (Wang et al. 2012; Christou et al. 2013; Shi et al. 2013; Lai et al. 2014; Sun & Luo 2014).

The maintenance of high K+/Na+ ratio in plant cells under salt-stress was also reported to be induced by H2S. Wheat seedlings treated with 50 µM NaHS, followed by 100 mM NaCl exposure exhibited increased K+/Na+ ratio with augment of selective transport of K+ over Na+ through nonselective cation channels and salt overly sensitive 1 (SOS1), a plasma membrane Na+/H+ antiporter (Deng et al. 2016). Induction of plasma membrane Na+/H+ antiporter genes (e.g. SOS2-like, SOS3-like and SOS4) by NaHS was also described in strawberry plants under high salinity, indicating a role for H2S in K+ uptake (Christou et al. 2013). The K+/Na+ homeostasis in salt-treated alfalfa was shown to be maintained by NaHS through the prevention of K+ efflux likely triggered by lower expression of shaker-like K+ outward-rectifying channel genes (Lai et al. 2014). Similar results were shown in roots of salt-treated barley seedlings in the presence of NaHS (Chen et al. 2015). Remarkably, H2S maintained low Na+ levels in cells by increasing the transcription of genes that encode for plasma membrane H+-ATPase, H+-ATPase subunit β and vacuolar Na+/H+ antiporter and augmenting Na+ compartmentation in vacuoles (Chen et al. 2015).

Germination of alfalfa seeds under 100 mM NaCl was stimulated by 100 µM NaHS (Wang et al. 2012). The improvement of seed germination rate caused by H2S may be a result of the induction of starch break down in the endosperm as the activity of α-amylase and β-amylase increased in salt-stressed cucumber seeds upon treatment with NaHS and ultimately led to hypocotyl and radicle growth (Sun & Luo 2014). The inhibition of root growth in Arabidopsis under salt stress was abolished by NaHS (Li et al. 2014), while this H2S donor improved the survival rate of salt-treated bermudagrass (Shi et al. 2013). The treatment of strawberry roots with NaHS prior to NaCl exposure resulted in increased photosynthetic rate, stomatal conductance and RWC in leaves in comparison with plants solely exposed to NaCl (Christou et al. 2013). Similarly, an H2S donor increased chlorophyll, carotenoid and total protein contents in rice under salinity (Mostofa et al. 2015).

Exogenous H2S also led to the accumulation of L-proline, sucrose and other soluble carbohydrates in NaCl-stressed bermudagrass cells (Shi et al. 2013). Soluble carbohydrates also accumulated in hypocotyl and radicle cells of cucumber plants stressed with sodium bicarbonate and treated with NaHS (Sun & Luo 2014).

Interplay between NO and H 2 S during plant response to salt stress

It is unquestionable that NO and H2S share roles in the signaling pathway that leads to plant tolerance to environmental stresses. Then, the extent of the cooperative function between these signaling molecules has received considerable attention recently.

Studies carried out with alfalfa seeds treated with NaCl for 24 h and barley seedlings challenged with NaCl for 48 h suggested that H2S might induce NO production during the response to the stress (Tab. 2; Wang et al. 2012; Chen et al. 2015). The simultaneous treatment of alfalfa with 100 μM NaHS (H2S donor) and 100 mM NaCl increased NO levels in cells by 30 %. This increment was accompanied of an increase in K+/Na+ ratio and transcription levels of SOD, CAT, APX and guaiacol peroxidase genes and a decrease in lipid peroxides (Wang et al. 2012). The use of a specific NO scavenger reversed the NaHS effects on alfalfa, clearly indicating the influence of exogenous H2S on NO endogenous levels. The NaHS (100 μM) also boosted NO production in barley seedlings by 30 % in comparison to control, detected in situ using a fluorophore specific to NO (Chen et al. 2015). Meanwhile, NaHS maintained ionic homeostasis through the decrease of K+ cell efflux and increase of Na+ in vacuoles. The gene expression of an inward-rectifying potassium channel (HvAKT1) and a high-affinity K+ uptake (HvHAK4) protein system also increased in barley upon concomitant treatment with NaCl and NaHS. Up-regulation of transcriptional levels of vacuolar Na+/H+ antiporter (HvVNHX2), H+-ATPase subunit β (HvVHA-β) and protein expression of vacuolar Na+/H+ antiporter (NHE1) was also observed in barley under the experimental conditions tested (Chen et al. 2015). In contrast, the treatment of NaCl-exposed strawberries plants with NaHS (100 μM) decreased NO levels in plant cells by 1.7-fold (Christou et al. 2013; Tab. 2). The decrease in the NO levels in strawberry was attributed by the authors to a possible control of nitrosative stress. Likewise, the lipid peroxide levels decreased while increment of expression of genes encoding for antioxidant enzymes and biosynthesis of AsA, GSH and SOS was recorded. Another line of evidence shows that endogenous NO and H2S stimulate the production of one another in tobacco leaves after NaCl stress for 10 days, as hypotaurine (an H2S scavenger) compromised NO accumulation in ca. 1.3-fold and cPTIO (an NO scavenger) undermined H2S production in ca. 1.6-fold (da-Silva et al. 2017; Tab. 2). Accumulation of NO and H2S stimulated the activity of CAT and SOD, decreased stomatal conductance to prevent water loss and drove to the control of oxidative stress assisted by GSH. Additionally, 200 μM S-nitrosoglutathione (an NO donor) enhanced the levels of L-cysteine by 10 % and the activity of L/D-DES and CS that, in turn, led to 20 % higher amounts of H2S in wheat seedlings under osmotic stress (Khan et al. 2017). The increase of H2S, provoked by exogenous NO, controlled oxidative stress by improving SOD, CAT, APX, GR, NR and peroxidase activities in plant cells and relieving H2O2 and O2 - effects. Accumulation of L-proline and glycine betaine was also observed in osmotic-stressed wheat seedlings supplemented with exogenous NO (Khan et al. 2017).

Figure 2 summarizes the known interactions between NO and H2S, regardless of their origin (endogenous or not), determined during plant response to high salinity.

Figure 2 Events triggered by nitric oxide (NO) and hydrogen sulfide (H2S) during plant response to high salinity. Panel A: main findings reported for alfalfa (Wang et al. 2012) and barley (Chen et al. 2015) in response to an H2S donor; Panel B: main findings reported for strawberry (Christou et al. 2013) in response to an H2S donor; Panel C: main findings reported for tobacco (da-Silva et al. 2017) highlighting the endogenous increment of both NO and H2S in plants challenged with high salinity. Standard arrows indicate stimulation of a certain event while flat-headed arrows stand for repression of a certain event. AKT1, inward-rectifying potassium channel; APX, ascorbate peroxidase; AsA, ascorbic acid; CAS, β-cyanoalanine synthase; CAT, catalase; CS, cysteine synthase; GPX, glutathione peroxidase; GR, glutathione reductase; GSH, reduced glutathione; HAK4, high-affinity K+ uptake system; L-DES, L-cysteine desulfhydrase; LOOH, lipid peroxides; NHX2, Na+/H+ antiporter; NR, nitrate reductase; SOD, superoxide dismutase; SOS, salt overly sensitive 1 protein.  

Concluding remarks

Both NO and H2S may originate in plants from several pathways in which NR seems to be indirectly the main source of NO while the majority of H2S produced comes from L-DES activity. The role of NO in the mitigation of oxidative burst in plants upon (a)biotic stress is known for roughly two decades and most recently, H2S has emerged as a new player in such signaling pathway, orchestrating biochemical events that lead plants tolerance to high salinity. Recent studies show that NO and H2S act together and influence the production of one another during plant response to relatively long periods of salt stress to improve plant antioxidant system, K+ uptake over Na+ and production of osmoprotective molecules. The extent of the interaction between these signaling molecules deserves more investigation, since there is still controversy with respect to which molecule triggers the cascade. Understanding this interplay will expand our knowledge on the complex biochemical cascade activated in plant cells with competence to cope with high salinity.


Part of the work cited in this review was financially supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). LVM is supported by a CNPq research fellowship and CJS was granted with a CNPq studentship.


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Received: June 10, 2017; Accepted: August 22, 2017

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