TY - JOUR
AU - Romero, Luis, C
AB - Abstract Two cysteine metabolism-related molecules, hydrogen sulfide and hydrogen cyanide, which are considered toxic, have now been considered as signaling molecules. Hydrogen sulfide is produced in chloroplasts through the activity of sulfite reductase and in the cytosol and mitochondria by the action of sulfide-generating enzymes, and regulates/affects essential plant processes such as plant adaptation, development, photosynthesis, autophagy, and stomatal movement, where interplay with other signaling molecules occurs. The mechanism of action of sulfide, which modifies protein cysteine thiols to form persulfides, is related to its chemical features. This post-translational modification, called persulfidation, could play a protective role for thiols against oxidative damage. Hydrogen cyanide is produced during the biosynthesis of ethylene and camalexin in non-cyanogenic plants, and is detoxified by the action of sulfur-related enzymes. Cyanide functions include the breaking of seed dormancy, modifying the plant responses to biotic stress, and inhibition of root hair elongation. The mode of action of cyanide is under investigation, although it has recently been demonstrated to perform post-translational modification of protein cysteine thiols to form thiocyanate, a process called S-cyanylation. Therefore, the signaling roles of sulfide and most probably of cyanide are performed through the modification of specific cysteine residues, altering protein functions. β-Cyanoalanine synthase, cyanide, L-cysteine desulfhydrase, persulfidation, redox regulation, S-cyanylation, sulfide, thiol group Introduction Cysteine is the reduced sulfur-containing metabolite that is first synthesized by plants from the most abundant inorganic oxidized sulfur molecule in soil, sulfate (Takahashi et al., 2011; Garcia et al., 2015; Gotor et al., 2017). In all living systems, cysteine is fundamental as a proteinogenic amino acid because it defines the structure and function of proteins through the conversion of cysteine thiol groups into disulfide bridges (Tridevi et al., 2009). Specifically, the cysteine-based redox modifications are the basis of different post-translational modifications that affect and regulate the functions of many proteins (Buchanan and Balmer, 2005; Chung et al., 2013). Protein thiols are also crucial to many enzymatic reactions that require the involvement of cysteines in active sites (Richau et al., 2012), or the binding of metals in specific proteins involved in electron transfer reactions (Balk and Schaedler, 2014). Another very important feature of cysteine is its role as a precursor molecule from which the majority of sulfur-containing metabolites are synthesized. A representative of this type of metabolite is glutathione, which plays major roles in biosynthetic pathways, detoxification, transport, redox signaling, and reactive oxygen species (ROS) metabolism (Noctor et al., 2012). Due to the significance of sulfur-containing compounds in plant metabolism, an intense investigation has been progressively conducted since the late 1980s to the present. Important breakthroughs, such as the elucidation of the entire genome sequence of the model plant Arabidopsis thaliana, the development of research tools to perform functional genomics, and the blossoming of omics technologies, have allowed relevant advances in knowledge of the sulfate assimilation pathway and, in general, sulfur metabolism in plants (Takahashi et al., 2011; Ravilious and Jez, 2012; Koprivova and Kopriva, 2014; Rennenberg and Herschbach, 2014; Garcia et al., 2015; Gotor et al., 2017). Currently, the most novel aspect of research on the role of sulfur in plants is focused on plant signaling. A fundamental change in the concept of sulfur compounds and related molecules performing signaling roles and thus regulating/affecting essential processes in the plant has occurred (Romero et al., 2014; Gotor et al., 2015). In this review, we focus on two molecules related to the metabolism of cysteine, sulfide and cyanide, which have been very recently shown to be involved in signaling of different plant processes. A comparison with other signaling molecules such as nitric oxide (NO·), hydrogen peroxide (H2O2), and ethylene shows many similarities between them and hydrogen sulfide (H2S) and cyanide. Like the other established signaling molecules, sulfide and cyanide are low molecular weight molecules with high to moderate chemical reactivity that are able to modify specific targets. They are also gases that can cross membranes to reach different cell compartments and perform their roles inside. Another common feature between all of them is the duality that they show; that is, above a certain concentration threshold, they are toxic molecules, but, below that threshold, they are important signaling molecules. Sulfide: from toxic to signaling molecule H2S has long been considered a poisonous substance hazardous to life and the environment. Although it was known to be present in mammalian tissues, it was not until the late 20th century that the endogenous production and signaling role of H2S as a neuromodulator was first established (Abe and Kimura, 1996). Intense research followed; this molecule is now accepted as a relevant signaling molecule in physiology, and it is included in the family of gasotransmitters in addition to NO· and carbon monoxide (CO) (Wang, 2002; Lowicka and Beltowski, 2007; Gadalla and Snyder, 2010; Wang, 2014). H2S is produced and metabolized by the cells in an accurate way, and the physiological functions in which it has been implicated are continuously increasing. Thus, it plays important biological roles in numerous systems of the body such as the cardiovascular, nervous, endocrine, gastrointestinal, immune, and respiratory systems. Moreover, H2S has clinical relevance because the alteration of H2S metabolism is often associated with different pathologies such as diabetes and cancer (Wang, 2012; Olas, 2015; Paul and Snyder, 2015). Similar to animal systems, the change in the concept of H2S as a toxic molecule to it being a regulator has also occurred in plant systems. An exponential increase in the number of plant studies in recent decades has led H2S to be considered to have the same relevance as the signaling molecules NO· and H2O2 (Garcia-Mata and Lamattina, 2013; Lisjak et al., 2013; Calderwood and Kopriva, 2014; Guo et al., 2015; Jin and Pei, 2015). H2S has been shown to produce physiological effects on a wide range of processes vital for plant performance. Thus, it has been studied in the plant responses to many different plant stresses, mainly abiotic stresses, ranging from metal stresses to drought, salinity, hypoxia, heat, and many others (Table 1). H2S allows for plant adaptation against these adverse environmental conditions, and its beneficial effects affect important aspects of development such as seed germination, root elongation, and plant survival. In many cases, H2S alleviates oxidative damage through the increase of antioxidative defenses. The activity of several enzymes involved in ROS detoxification or the level of the antioxidants glutathione and ascorbic acid were increased by H2S treatments in stressed cucumber seedlings (Yu et al., 2013), maize (Shan et al., 2014), wheat (Khan et al., 2017; Shan et al., 2018), alfalfa (Wang et al., 2012), and rice (Mostofa et al., 2015), or during tomato fruit ripening (Yao et al., 2018) at concentrations ranging from 25 µM to 600 µM (Table 1). The role of H2S in plant resistance to pathogens has not been extensively studied, although it has been reported that the release of H2S correlated with an increased resistance to fungal infection. Therefore, the previously described concept of sulfur-induced resistance (SIR), which proposed that the sulfur fertilization of crops reduces sensitivity to pathogens, was suggested to be mediated by H2S (Bloem et al., 2004). In addition, acquired pathogen resistance has been suggested to be related to an increase in endogenous sulfide content (Alvarez et al., 2012a; Gotor et al., 2015; Shi et al., 2015). Table 1. Effects of hydrogen sulfide in plant adaptation to abiotic stresses Stress/hydrogen sulfide treatment Consequences References Aluminum stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2010) Arsenate stress/NaHS addition Induction of ascorbate–glutathione cycle Singh et al. (2015) Boron stress/NaHS addition Alleviation of inhibition of root elongation Wang et al. (2010) Cadmium stress/endogenous H2S induction Vacuolar H+-ATPase alteration Kabala et al. (2018) Cadmium stress/endogenous H2S induction Balance between H2O2 and O2·− Lv et al. (2017) Cadmium stress/NaHS pre-treatment Proline increase Tian et al. (2016) Cadmium stress/endogenous H2S induction Glutathione and ROS homeostasis Cui et al. (2014) Cadmium stress/NaHS addition Alleviation of cell death/oxidative damage Zhang et al. (2015) Cadmium stress/NaHS pre-treatment Alleviation of oxidative stress/activation of Cd transport Sun et al. (2013) Chromium stress/NaHS addition Alleviation of oxidative stress Kharbech et al. (2017) Chromium stress/ endogenous H2S induction Induction of cysteine accumulation Fang et al. (2016) Copper stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2008) Drought/endogenous H2S induction Reduction of stomatal aperture/induction of drought-associated genes Jin et al. (2011) Drought/NaHS addition Increased level of polyamines and sugars J. Chen et al. (2016) Drought/NaHS addition Induction of components of the ABA signaling pathway Ma et al. (2016) Drought/NaHS addition Alleviation of PSII damage through D1 protein level Li et al. (2015) Heat stress/NaHS pre-treatment Involvement of Ca2+ and calmodulin Li et al. (2012) Heat stress endogenous H2S induction NO•-mediated tolerance/reduction of electrolyte leakage Li et al. (2013) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of heat shock proteins and aquaporin Christou et al. (2014) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of osmolyte biosynthesis Zhou et al. (2018) Heat stress/endogenous H2S induction Induction of nicotine biosynthesis X. Chen et al. (2016) Hypoxia/endogenous H2S induction Alleviation of oxidative stress Cheng et al. (2013) Osmotic stress/endogenous H2S induction Alleviation of oxidative stress/osmolyte accumulation Khan et al. (2017) Osmotic stress/endogenous H2S induction Ethylene-mediated stomatal closure/persulfidation of ACC oxidase Jia et al. (2018) Salinity/ endogenous H2S induction Alleviation of oxidative stress da Silva et al. (2017) Salinity/NaHS pre-treatment Alleviation of oxidative stress/maintenance of Na+/K+ balance Mostofa et al. (2015) Salinity/endogenous H2S induction Alleviation of oxidative stress/maintenance of Na+/K+ balance Lai et al. (2014) Salinity/NaHS addition Alleviation of oxidative stress/maintenance of Na+/K+ balance J. Li et al. (2014) Salinity/NaHS addition Maintenance of Na+/K+ balance Zhao et al. (2018) Salinity/NaHS addition NO•-dependent maintenance of ion homeostasis Chen et al. (2015a) Salinity/NaHS pre-treatment Alleviation of oxidative stress/affecting the SOS pathway Christou et al. (2013) Iron deficiency/ NaHS addition Enhanced photosynthesis Chen et al. (2015b) Ammonium stress/endogenous H2S induction Increased ammonium incorporation/alleviation of inhibition of root growth Guo et al. (2017) Stress/hydrogen sulfide treatment Consequences References Aluminum stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2010) Arsenate stress/NaHS addition Induction of ascorbate–glutathione cycle Singh et al. (2015) Boron stress/NaHS addition Alleviation of inhibition of root elongation Wang et al. (2010) Cadmium stress/endogenous H2S induction Vacuolar H+-ATPase alteration Kabala et al. (2018) Cadmium stress/endogenous H2S induction Balance between H2O2 and O2·− Lv et al. (2017) Cadmium stress/NaHS pre-treatment Proline increase Tian et al. (2016) Cadmium stress/endogenous H2S induction Glutathione and ROS homeostasis Cui et al. (2014) Cadmium stress/NaHS addition Alleviation of cell death/oxidative damage Zhang et al. (2015) Cadmium stress/NaHS pre-treatment Alleviation of oxidative stress/activation of Cd transport Sun et al. (2013) Chromium stress/NaHS addition Alleviation of oxidative stress Kharbech et al. (2017) Chromium stress/ endogenous H2S induction Induction of cysteine accumulation Fang et al. (2016) Copper stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2008) Drought/endogenous H2S induction Reduction of stomatal aperture/induction of drought-associated genes Jin et al. (2011) Drought/NaHS addition Increased level of polyamines and sugars J. Chen et al. (2016) Drought/NaHS addition Induction of components of the ABA signaling pathway Ma et al. (2016) Drought/NaHS addition Alleviation of PSII damage through D1 protein level Li et al. (2015) Heat stress/NaHS pre-treatment Involvement of Ca2+ and calmodulin Li et al. (2012) Heat stress endogenous H2S induction NO•-mediated tolerance/reduction of electrolyte leakage Li et al. (2013) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of heat shock proteins and aquaporin Christou et al. (2014) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of osmolyte biosynthesis Zhou et al. (2018) Heat stress/endogenous H2S induction Induction of nicotine biosynthesis X. Chen et al. (2016) Hypoxia/endogenous H2S induction Alleviation of oxidative stress Cheng et al. (2013) Osmotic stress/endogenous H2S induction Alleviation of oxidative stress/osmolyte accumulation Khan et al. (2017) Osmotic stress/endogenous H2S induction Ethylene-mediated stomatal closure/persulfidation of ACC oxidase Jia et al. (2018) Salinity/ endogenous H2S induction Alleviation of oxidative stress da Silva et al. (2017) Salinity/NaHS pre-treatment Alleviation of oxidative stress/maintenance of Na+/K+ balance Mostofa et al. (2015) Salinity/endogenous H2S induction Alleviation of oxidative stress/maintenance of Na+/K+ balance Lai et al. (2014) Salinity/NaHS addition Alleviation of oxidative stress/maintenance of Na+/K+ balance J. Li et al. (2014) Salinity/NaHS addition Maintenance of Na+/K+ balance Zhao et al. (2018) Salinity/NaHS addition NO•-dependent maintenance of ion homeostasis Chen et al. (2015a) Salinity/NaHS pre-treatment Alleviation of oxidative stress/affecting the SOS pathway Christou et al. (2013) Iron deficiency/ NaHS addition Enhanced photosynthesis Chen et al. (2015b) Ammonium stress/endogenous H2S induction Increased ammonium incorporation/alleviation of inhibition of root growth Guo et al. (2017) The table shows a representation of some of the published data. View Large Table 1. Effects of hydrogen sulfide in plant adaptation to abiotic stresses Stress/hydrogen sulfide treatment Consequences References Aluminum stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2010) Arsenate stress/NaHS addition Induction of ascorbate–glutathione cycle Singh et al. (2015) Boron stress/NaHS addition Alleviation of inhibition of root elongation Wang et al. (2010) Cadmium stress/endogenous H2S induction Vacuolar H+-ATPase alteration Kabala et al. (2018) Cadmium stress/endogenous H2S induction Balance between H2O2 and O2·− Lv et al. (2017) Cadmium stress/NaHS pre-treatment Proline increase Tian et al. (2016) Cadmium stress/endogenous H2S induction Glutathione and ROS homeostasis Cui et al. (2014) Cadmium stress/NaHS addition Alleviation of cell death/oxidative damage Zhang et al. (2015) Cadmium stress/NaHS pre-treatment Alleviation of oxidative stress/activation of Cd transport Sun et al. (2013) Chromium stress/NaHS addition Alleviation of oxidative stress Kharbech et al. (2017) Chromium stress/ endogenous H2S induction Induction of cysteine accumulation Fang et al. (2016) Copper stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2008) Drought/endogenous H2S induction Reduction of stomatal aperture/induction of drought-associated genes Jin et al. (2011) Drought/NaHS addition Increased level of polyamines and sugars J. Chen et al. (2016) Drought/NaHS addition Induction of components of the ABA signaling pathway Ma et al. (2016) Drought/NaHS addition Alleviation of PSII damage through D1 protein level Li et al. (2015) Heat stress/NaHS pre-treatment Involvement of Ca2+ and calmodulin Li et al. (2012) Heat stress endogenous H2S induction NO•-mediated tolerance/reduction of electrolyte leakage Li et al. (2013) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of heat shock proteins and aquaporin Christou et al. (2014) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of osmolyte biosynthesis Zhou et al. (2018) Heat stress/endogenous H2S induction Induction of nicotine biosynthesis X. Chen et al. (2016) Hypoxia/endogenous H2S induction Alleviation of oxidative stress Cheng et al. (2013) Osmotic stress/endogenous H2S induction Alleviation of oxidative stress/osmolyte accumulation Khan et al. (2017) Osmotic stress/endogenous H2S induction Ethylene-mediated stomatal closure/persulfidation of ACC oxidase Jia et al. (2018) Salinity/ endogenous H2S induction Alleviation of oxidative stress da Silva et al. (2017) Salinity/NaHS pre-treatment Alleviation of oxidative stress/maintenance of Na+/K+ balance Mostofa et al. (2015) Salinity/endogenous H2S induction Alleviation of oxidative stress/maintenance of Na+/K+ balance Lai et al. (2014) Salinity/NaHS addition Alleviation of oxidative stress/maintenance of Na+/K+ balance J. Li et al. (2014) Salinity/NaHS addition Maintenance of Na+/K+ balance Zhao et al. (2018) Salinity/NaHS addition NO•-dependent maintenance of ion homeostasis Chen et al. (2015a) Salinity/NaHS pre-treatment Alleviation of oxidative stress/affecting the SOS pathway Christou et al. (2013) Iron deficiency/ NaHS addition Enhanced photosynthesis Chen et al. (2015b) Ammonium stress/endogenous H2S induction Increased ammonium incorporation/alleviation of inhibition of root growth Guo et al. (2017) Stress/hydrogen sulfide treatment Consequences References Aluminum stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2010) Arsenate stress/NaHS addition Induction of ascorbate–glutathione cycle Singh et al. (2015) Boron stress/NaHS addition Alleviation of inhibition of root elongation Wang et al. (2010) Cadmium stress/endogenous H2S induction Vacuolar H+-ATPase alteration Kabala et al. (2018) Cadmium stress/endogenous H2S induction Balance between H2O2 and O2·− Lv et al. (2017) Cadmium stress/NaHS pre-treatment Proline increase Tian et al. (2016) Cadmium stress/endogenous H2S induction Glutathione and ROS homeostasis Cui et al. (2014) Cadmium stress/NaHS addition Alleviation of cell death/oxidative damage Zhang et al. (2015) Cadmium stress/NaHS pre-treatment Alleviation of oxidative stress/activation of Cd transport Sun et al. (2013) Chromium stress/NaHS addition Alleviation of oxidative stress Kharbech et al. (2017) Chromium stress/ endogenous H2S induction Induction of cysteine accumulation Fang et al. (2016) Copper stress/NaHS pre-treatment Promotion of seed germination/alleviation of oxidative damage Zhang et al. (2008) Drought/endogenous H2S induction Reduction of stomatal aperture/induction of drought-associated genes Jin et al. (2011) Drought/NaHS addition Increased level of polyamines and sugars J. Chen et al. (2016) Drought/NaHS addition Induction of components of the ABA signaling pathway Ma et al. (2016) Drought/NaHS addition Alleviation of PSII damage through D1 protein level Li et al. (2015) Heat stress/NaHS pre-treatment Involvement of Ca2+ and calmodulin Li et al. (2012) Heat stress endogenous H2S induction NO•-mediated tolerance/reduction of electrolyte leakage Li et al. (2013) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of heat shock proteins and aquaporin Christou et al. (2014) Heat stress/NaHS pre-treatment Alleviation of oxidative stress/induction of osmolyte biosynthesis Zhou et al. (2018) Heat stress/endogenous H2S induction Induction of nicotine biosynthesis X. Chen et al. (2016) Hypoxia/endogenous H2S induction Alleviation of oxidative stress Cheng et al. (2013) Osmotic stress/endogenous H2S induction Alleviation of oxidative stress/osmolyte accumulation Khan et al. (2017) Osmotic stress/endogenous H2S induction Ethylene-mediated stomatal closure/persulfidation of ACC oxidase Jia et al. (2018) Salinity/ endogenous H2S induction Alleviation of oxidative stress da Silva et al. (2017) Salinity/NaHS pre-treatment Alleviation of oxidative stress/maintenance of Na+/K+ balance Mostofa et al. (2015) Salinity/endogenous H2S induction Alleviation of oxidative stress/maintenance of Na+/K+ balance Lai et al. (2014) Salinity/NaHS addition Alleviation of oxidative stress/maintenance of Na+/K+ balance J. Li et al. (2014) Salinity/NaHS addition Maintenance of Na+/K+ balance Zhao et al. (2018) Salinity/NaHS addition NO•-dependent maintenance of ion homeostasis Chen et al. (2015a) Salinity/NaHS pre-treatment Alleviation of oxidative stress/affecting the SOS pathway Christou et al. (2013) Iron deficiency/ NaHS addition Enhanced photosynthesis Chen et al. (2015b) Ammonium stress/endogenous H2S induction Increased ammonium incorporation/alleviation of inhibition of root growth Guo et al. (2017) The table shows a representation of some of the published data. View Large H2S also exerts physiological effects on processes that are critical for adequate plant performance including different aspects of the plant developmental program such as seed germination (Dooley et al., 2013; Baudouin et al., 2016), root development (Fang et al., 2014; Y.J. Li et al., 2014; Jia et al., 2015), leaf senescence (Alvarez et al., 2012b), and post-harvest senescence and fruit ripening (Huo et al., 2018; Ziogas et al., 2018). Another essential plant process, photosynthesis, is enhanced by H2S through promotion of chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification (Chen et al., 2011). H2S also delays programmed cell death by the modulation of glutathione homeostasis and heme oxyenase-1 expression (Xie et al., 2014). Moreover, the progression of autophagy is negatively regulated by H2S in a way unrelated of sulfur nutrition and by a mechanism of action independent of redox conditions (Alvarez et al., 2012b; Gotor et al., 2015; Laureano-Marín et al., 2016a , b). Of particular interest is that H2S regulates stomatal movement, which has important implications for countering osmotic and drought stress conditions. Numerous studies have demonstrated that H2S is a component of the abscisic acid (ABA) signaling network in guard cells and specifically targets ion channels. The existence of complex crosstalk with the other signaling molecules NO· and H2O2 has also been described (Garcia-Mata and Lamattina, 2010; Lisjak et al., 2010; Jin et al., 2013; Scuffi et al., 2014, 2018; Honda et al., 2015; Papanatsiou et al., 2015; Wang et al., 2016). Different interplays between H2S and other signaling molecules and phytohormones have been observed in the various processes by which sulfide exerts important physiological effects (Table 1). Biosynthesis of hydrogen sulfide inside the cells H2S is endogenously produced in animal cells mainly by the action of enzymes involved in the metabolism of sulfur amino acids: cystathionine γ-lyase, cystathionine β-synthase, and 3-mercaptopyruvate sulfurtransferase. These enzymes show differential tissue and subcellular localization and control the synthesis of H2S with different efficiencies (Kabil and Banerjee, 2010; Kimura, 2011, 2015). In addition, other pathways of H2S production are currently being identified (Olson, 2018). The endogenous production of H2S by plant cells is also related to the biosynthesis and metabolism of cysteine (Fig. 1). Its main source is located in the chloroplast, where sulfite is reduced to sulfide by the action of sulfite reductase during the photosynthetic sulfate assimilation pathway (Takahashi et al., 2011; Garcia et al., 2015). Indeed, when subcellular metabolite concentrations were estimated, plastids contained the highest sulfide concentrations (Krueger et al., 2009). It was proposed that chloroplastic H2S could reach other cellular compartments by diffusion through membranes; however, other enzymatic processes have been demonstrated to be responsible for the sulfide synthesis in other subcellular compartments in plant cells, which is described below. H2S is a weak acid with pKa1 and pKa2 of 6.9 and >12 (Kabil and Banerjee, 2010), and in aqueous solution it dissociates into the H+ and HS− ions; and the anionic forms are unable to cross the chloroplast envelope membrane. Under physiological, neutral pH conditions, two-thirds of H2S is in the form of HS−, which can dissociate to H+ and S2− at higher pH (Lowicka and Beltowski, 2007; Kabil and Banerjee, 2010). The chloroplast stroma increases the pH from neutral to relatively basic (pH 8) upon illumination for the optimization of photosynthetic reactions (Shen et al., 2013; Höhner et al., 2016). Therefore, most sulfide present inside the chloroplast is dissociated into its ionic form HS−, which is unable to permeate the membrane freely and requires a currently unknown active transporter. However, in bacteria, a hydrosulfide ion channel has already been described (Czyzewski and Wang, 2012). Fig. 1. View largeDownload slide Subcellular locations of hydrogen sulfide (H2S) production in plant cells. The main source is located in the chloroplast, where sulfite is reduced to sulfide by the action of sulfite reductase (SiR) during the photosynthetic sulfate reduction pathway and, at the chloroplast stromal basic pH, most of H2S is dissociated into its ionic form (HS−) that requires an unknown active transporter (shown as an interrogation mark) to permeate the membrane. In the cytosol, cysteine is mainly synthesized by the action of the O-acetylserine(thiol)lyase (OSATL) and this cell compartment is another source of H2S that is generated from cysteine by different cysteine-degrading enzymes, such as the l-cysteine (l-CDES) and d-cysteine (d-CDES) desulfhydrases, and the l-cysteine desulfurases (NifS-like). NifS-like proteins are also located in chloroplasts and mitochondria. Mitochondria are also a source of H2S that is generated during the detoxification of cyanide by the action of the β-cyanoalanine synthase (CAS) which uses cysteine synthesized by mitochondrial OASTL. Mitochondrial H2S is also dissociated to its ionic form at basic pH. Fig. 1. View largeDownload slide Subcellular locations of hydrogen sulfide (H2S) production in plant cells. The main source is located in the chloroplast, where sulfite is reduced to sulfide by the action of sulfite reductase (SiR) during the photosynthetic sulfate reduction pathway and, at the chloroplast stromal basic pH, most of H2S is dissociated into its ionic form (HS−) that requires an unknown active transporter (shown as an interrogation mark) to permeate the membrane. In the cytosol, cysteine is mainly synthesized by the action of the O-acetylserine(thiol)lyase (OSATL) and this cell compartment is another source of H2S that is generated from cysteine by different cysteine-degrading enzymes, such as the l-cysteine (l-CDES) and d-cysteine (d-CDES) desulfhydrases, and the l-cysteine desulfurases (NifS-like). NifS-like proteins are also located in chloroplasts and mitochondria. Mitochondria are also a source of H2S that is generated during the detoxification of cyanide by the action of the β-cyanoalanine synthase (CAS) which uses cysteine synthesized by mitochondrial OASTL. Mitochondrial H2S is also dissociated to its ionic form at basic pH. The last enzymatic step of the photosynthetic sulfate assimilation pathway consists of the synthesis of cysteine catalyzed by the O-acetylserine(thiol)lyase (OASTL) enzymes. Although different OASTLs are localized to the chloroplasts, mitochondria, and cytosol, which produces diversity in subcellular cysteine pools, it is currently known that cysteine is synthesized mainly in the cytosol (Takahashi et al., 2011; Garcia et al., 2015) (Fig. 1). Accordingly, the cytosol is the compartment with the highest cysteine concentration, which is estimated to be >300 µM, while, in other compartments, the cysteine concentrations are <10 µM (Krueger et al., 2009). Therefore, the cytosol is a source of H2S metabolically generated from cysteine, and several types of cysteine-degrading enzymes have been reported in plant systems (Papenbrock et al., 2007) (Fig. 1). The l-cysteine desulfhydrase (l-CDES) enzymes catalyze the conversion of l-cysteine to sulfide, ammonia, and pyruvate, and some l-CDES enzymes from Arabidopsis have been characterized in more detail (Alvarez et al., 2010; Gotor et al., 2010; Shen et al., 2012). In addition to l-CDES, in different plant species, d-cysteine desulfhydrase (d-CDES) enzymes that are specific for d-cysteine as a substrate and are completely different proteins from the l-CDES enzymes have been described (Riemenschneider et al., 2005; Cui et al., 2014). Other enzymes that catalyze the desulfurization of cysteine are the NifS-like proteins, which catalyze the conversion of cysteine to alanine and elemental sulfur or sulfide. These proteins provide sulfur for the synthesis of biotin and thiamine, the formation of Fe–S clusters, and the formation of molybdenum cofactors, and are located in the cytosol, chloroplasts, and mitochondria (Van Hoewyk et al., 2008). Mitochondria can also be a source of H2S that is generated during the detoxification of cyanide by the action of the β-cyanoalanine synthase (CAS), which catalyzes the formation of β-cyanoalanine (Hatzfeld et al., 2000; Yamaguchi et al., 2000) (Fig. 1). The H2S produced by CAS is incorporated by the mitochondrial isoform of OASTL into the synthesis of cysteine, which is used by CAS to detoxify cyanide, producing a cyclic pathway in the mitochondria (Alvarez et al., 2012c). In any case, if an excess of H2S occurs, similar to chloroplasts, the relatively basic pH of the mitochondrial stroma in metabolically active cells would provoke the accumulation of the charged HS− form, and its transport would be avoided (Shen et al., 2013). In addition, the endogenous production of H2S has been shown to be induced in response to various abiotic stress conditions, and different molecules related to signaling pathways are involved. Increased activities of the H2S-generating desulfhydrases correlate with the induction of sulfide levels under stress conditions (Jin et al., 2011; Lai et al., 2014; Guo et al., 2017; Kabala et al., 2018), and the involvement of ethylene (Jia et al., 2018) or NO• (da Silva et al., 2017; Khan et al., 2017) has been described. An interesting study has recently provided evidence for the regulatory mechanism of H2S production in response to chromium stress, which is enhanced through the calcium/calmodulin 2-mediated pathway, involving the transcription factor TGA3 (Fang et al., 2017). Hydrogen sulfide mechanism of action Despite the fact that the number of physiological processes known to be affected by H2S in plants has been continuously increasing, as has the evidence of its biological function in other organisms, there is an important lack of understanding of the mechanism by which H2S performs its function. Without a doubt, the mechanism of action of H2S must be related to the characteristics of its chemical reactivity with other molecules such as its affinity for metal centers in metalloproteins, its reactivity with other small oxygen and nitrogen species (ROS and RNS), and its capacity to modify protein cysteine residues to form persulfides (Fig. 2). Fig. 2. View largeDownload slide Schematic representation of the hydrogen sulfide (H2S) action mechanism in biological processes. The mechanism of action of H2S is related to its chemical reactivity with other molecules. It can coordinate the metal center of metalloproteins. It can act as a reductant reacting with biological oxidants, such as nitric oxide (NO·), hydrogen peroxide (H2O2), superoxide radical (O2·−), peroxynitrite (ONOOH), hypochlorite (HOCl), and S-nitrosothiols. It can modify proteins by the oxidation of cysteine residues to form the corresponding persulfides (-SSH), a process called persulfidation. Fig. 2. View largeDownload slide Schematic representation of the hydrogen sulfide (H2S) action mechanism in biological processes. The mechanism of action of H2S is related to its chemical reactivity with other molecules. It can coordinate the metal center of metalloproteins. It can act as a reductant reacting with biological oxidants, such as nitric oxide (NO·), hydrogen peroxide (H2O2), superoxide radical (O2·−), peroxynitrite (ONOOH), hypochlorite (HOCl), and S-nitrosothiols. It can modify proteins by the oxidation of cysteine residues to form the corresponding persulfides (-SSH), a process called persulfidation. H2S can coordinate the metal center of metalloproteins (Filipovic et al., 2018) and attach covalently to heme porphyrins, acting as a potent inhibitor of mitochondrial cytochrome c oxidase and inhibiting respiration in mitochondria where sulfide is detoxified (Birke et al., 2015). H2S can also react with leghemoglobin to reduce its iron center and form a complex in a process that can be reversed by oxidizing or reducing agents (Puppo and Davies, 1995). In mammals, the reduction of ferric cytochrome c by H2S, cytochrome c release during apoptosis, and stimulation of procaspase 9 persulfidation have also been demonstrated (Vitvitsky et al., 2018). The sulfur atom in H2S is at its lowest oxidation state (–2) and can only be oxidized; therefore, it acts as a reductant (Zaffagnini et al., 2019). The reaction of H2S with O2 is thermodynamically disfavored, but several biological oxidants such as hydroxyl radical (HO·), nitrogen dioxide (NO2·), superoxide radical (O2·−), H2O2, peroxynitrite (ONOOH), and hypochlorite (HOCl) can support its oxidation (Li and Lancaster, 2013). NO· molecules can also react with H2S, which can lead to the formation of various nitrogen (N2O, HNO) and sulfur derivatives (S0, S·−), including S-nitrosothiols (Filipovic et al., 2018). Studies of the cellular crosstalk between H2S and S-nitrosothiols suggest that sulfide species may play a role in modulating the profile of these molecules through the reaction of H2S with small or protein S-nitrosothiol molecules to form nitropersulfide (SSNO−), polysulfides (HSn−), and dinitrososulfite [ONN(OH)SO3−], three products with distinct bioactive profiles that can modulate biological processes (Filipovic et al., 2012; Cortese-Krott et al., 2015). Although the direct reactions of H2S with ROS or RNS have not been described and quantified in plants cells, the role of H2S in the activation of antioxidant systems has been described in several plants, as detailed in the previous section. The level of NO· is also elevated by H2S treatment of salt-stressed cucumbers, or tomato under excess of nitrate (Guo et al., 2018), but direct reactions between H2S and NO· have not been measured in plant systems. A third mechanism of action of H2S, based on its chemical reactivity, is the modification of proteins by the oxidation of cysteine residues to form the corresponding persulfides. The first described method for detection of persulfides consisted of an initial blocking step of the protein thiol residues in which persulfides remain free, followed by a reaction of persulfides with a biotinylating agent. In this way, all persulfide groups present in proteins are transformed into biotinylated residues, which allowed the purification and identification of modified proteins. Using this modified biotin switch assay, Snyder and colleagues described for the first time protein S-sulfhydration (now called persulfidation) in mouse liver and detected this modification in proteins such as glyceraldehyde-3-phosphate dehydrogenase, β-tubulin, and actin (Mustafa et al., 2009). The identification of persulfidated proteins in mammalian systems and the pathophysiological processes in which they are involved are numerous (Zhang et al., 2017); however, the specific chemical reactions by which this modification takes place are not clearly established due to the chemical complexity of sulfur and because there are probably several chemical scenarios, depending on the environment, that can lead to this modification (Mishanina et al., 2015; Filipovic et al., 2018). H2S, or its ionic forms, HS− and S2−, cannot react directly with protein thiols and requires the presence of an oxidant; thus, it can react with oxidized cysteine residues as sulfenic acids (R-SOH). Disulfides and S-nitrosylated cysteines can also react with H2S, leading to the formation of persulfidated residues plus thiol and HNO, respectively. Finally, oxidized sulfide species such as as polysulfides can also react and transfer a sulfane sulfur atom (S0) to cysteine thiols or be the carrier of persulfides by displacement reaction (Zhang et al., 2017). All of these processes may lead to the persulfidation of proteins. In plants, a proteomic analysis in Arabidopsis untreated leaf samples using the modified biotin switch assay described the presence of 106 persulfidated proteins and, similarly to mammalian systems, glyceraldehyde-3-phosphate dehydrogenase, β-tubulin, and actin were also detected as post-translationally modified proteins (Aroca et al., 2015). After increasing doubts about the specificity of the blocking reagent used in the modified biotin switch assay, a second method to detect the persulfidated proteins was described initially in an animal system, the tag switch assay (Zhang et al., 2014). In this method, a different blocking reagent is used that reacts equally with thiols and persulfide groups in the first step; however, the resulting derivatives show different reactivity to nucleophilic attack. In the second step, a biotin-linked cyanoacetate reagent specifically reacts with the persulfide derivatives. Thus, the number of proteins susceptible to persulfidation in Arabidopsis was later updated to 3478 in untreated wild-type leaves (present in at least one replica sample) by the use of the tag switch assay, which allowed labeling of cysteine persulfides with greater specificity (Aroca et al., 2017a). This number shows that 10% of the Arabidopsis proteome is persulfidated under normal growth conditions and that this modification could be involved in a great variety of biological processes. The major sulfide source in leaf tissue must come from chloroplast sulfate assimilation, and up to 22% of persulfidated proteins are localized to the plastid and function in the photosynthetic light reactions in thylakoids and in the Calvin–Benson cycle in the stroma (Fig. 3); with most of them with reactive cysteines reported to be redox regulated (Buchanan and Balmer, 2005; Aroca et al., 2017a). However, almost 50% of persulfidated proteins are localized in the cytosol. This observation is not strange, since the cytosol is where cysteine is mainly synthesized and several types of cysteine-degrading and sulfide-releasing enzymes are located (Fig. 1) (Heeg et al., 2008; Watanabe et al., 2008). Fig. 3. View largeDownload slide Persulfidated proteins in the plant photosynthesis pathway. The persulfidated proteins involved in the photosynthetic light reactions located in chloroplast thylakoids and in the Calvin–Benson cycle located in chloroplast stroma are shown as blue squares. Fig. 3. View largeDownload slide Persulfidated proteins in the plant photosynthesis pathway. The persulfidated proteins involved in the photosynthetic light reactions located in chloroplast thylakoids and in the Calvin–Benson cycle located in chloroplast stroma are shown as blue squares. As mentioned, autophagy and ABA signaling in guard cells are two of the physiological processes demonstrated to be regulated by H2S in plants, and proteomic analysis also shows that some proteins involved in the ABA signaling pathway can be persulfidated. Among them are the hormone receptors PYRABACTIN RESISTANCE 1 (PYR1) and PYR1-LIKE PROTEIN 1(PYL1), the SNF1-RELATED PROTEIN KINASE 2.2 (SnRK2.2) and 2.6 (OST1), and several potassium channels (KAB1 and AKT2), and therefore this proteomic analysis indicates them to be putative targeted candidates for H2S-dependent stomatal closure regulation (Scuffi et al., 2014). The presence of several autophagy-related proteins such as ATG3, ATG5, and ATG18a also highlights them as possible candidates for the regulation of autophagy by H2S (Alvarez et al., 2012b; Laureano-Marín et al., 2016a). Further investigation is required to identify the specific persulfidated proteins responsible for the H2S regulation of autophagy and stomatal movement. Although the number of proteins susceptible to persulfidation in plants is high, the biological significance of this post-translational modification on plant processes is still limited. The five glyceraldehyde-3-phosphate dehydrogenases from Arabidopsis can be persulfidated, and this modification can affect either its activity or its cytosolic/nuclear partitioning, as reported for the cytosolic GapC1 and GapC2 isoforms, which are persulfidated at Cys160 as analyzed by parallel reaction monitoring (Aroca et al., 2015, 2017b). H2S also signals and regulates the actin cytoskeleton and root hair growth; a higher level of H2S thereby causes the depolymerization of F-actin bundles by the persulfidation of Arabidopsis ACTIN 2 (ACT2) at Cys287, a conserved residue in actin sequences (Li et al., 2018). In addition, in tomato plants under osmotic stress, ethylene regulates stomatal closure and induces the production of H2S in guard cells, but H2S feedback also regulates ethylene biosynthesis through inhibiting the enzymatic activity of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1) by persulfidation at Cys60 (Jia et al., 2018). As mentioned before, H2S is produced in plant cells from several sources, ranging from chloroplastic sulfate assimilation coupled to cysteine biosynthesis through O-acetylserine(thiol)lyases to the enzymatic production of H2S in the cytosol and mitochondria from cysteine desulfhydrases or β-cyanoalanine synthase, among others (Fig. 1). Chloroplastic sulfide synthesis must occur mostly in the light coupled to photosynthesis because it requires reduced ferredoxin as an electron donor for sulfite reductase; however, enzymatically produced H2S coupled to cysteine degradation or cyanide detoxification can occur either in the light or in the dark. Since the light reactions of photosynthesis constitute an important source of ROS, we can expect that part of the H2S produced through sulfite reduction can be partially oxidized back to hydrogen disulfide or polysulfide as a stochastic event (Fig. 4). This reactive sulfur species can drive the persulfidation of proteins within the chloroplast. In fact, as mentioned, up to 22% of the proteins identified in the proteomic analysis of Arabidopsis leaf tissue are localized in the chloroplast (Aroca et al., 2017a). Although plant cells have an extensive battery of enzymes that facilitate the reduction of proteins by cysteine thiol–disulfide exchange, such as thioredoxins, glutaredoxins, protein disulfide isomerases, along with different ROS-scavenging systems in which glutathione is involved, and ROS detoxification enzymes, they are not enough to control the high level of ROS under stress conditions that can lead to the overoxidation of cysteine residues originating the irreversible sulfinic (P-SO2H) or sulfonic (P-SO3H) motif (Fig. 4). H2S reacts with sulfenic acid to form persulfide and, in fact, oxidative conditions increase the level of persulfidation in culture cells treated with H2O2 (Cuevasanta et al., 2015; Wedmann et al., 2016). Persulfidated residues have lower pKa values than their corresponding thiols, and the deprotonated forms (RSS−) are more nucleophilic, enabling reactions with ROS. At pH 7.4, it has been measured that the reaction of peroxinitrite with albumin persulfide is an order of magnitude higher than with reduced albumin (Cuevasanta et al., 2015). Analogously to the reaction of thiol with H2O2, under persistent oxidation stress, persulfidated proteins can react with ROS to form perthiosulfenic acids (R-SSOHs) as predicted by density functional theory calculation and observed in epidermal growth factor receptor (Heppner et al., 2018). In the presence of excess oxidant, perthiosulfenic acid could be oxidized to perthiosulfinic and perthiosulfonic acid, species detected in papain, albumin, and glutathione peroxidase (Benchoam et al., 2019). Although sulfinic and sulfonic acids are generally considered irreversible modifications, perthiosulfinic and perthiosulfonic acid can be easily reduced back by reductants or by thioredoxin systems to restore the free thiols (Filipovic, 2015; Millikin et al., 2016; Filipovic et al., 2018). Human thioredoxins have been shown to have 10-fold higher reactivity towards cysteine persulfides than towards cystines (Wedmann et al., 2016). Persulfidation can therefore serve to protect protein thiols from oxidative damage (Filipovic et al., 2018) (Fig. 4). Fig. 4. View largeDownload slide Schematic representation of the function of protein persulfidation in protection. The major source of sulfide in plant cells must proceed from photosynthetic sulfate assimilation by sulfite reductase (SiR) activity in chloroplasts that is coupled to the biosynthesis of cysteine within the chloroplast, the cytosol, or the mitochondria by OASTL enzymes. l/d-DES and HCN/CAS activity can also generate H2S from cysteine within the cytosol or the mitochondria. Reactive oxygen species (ROS) generated by the light reaction of photosynthesis or stress processes can lead to sulfide oxidation to H2S2 or polysulfide (H2Sn), which can react with thiol residues in proteins to form persulfides (-SSH). Thiolate residues within proteins (-SH) can be oxidized by ROS to form disulfide bridges (-SS-) or by persistent oxidizing conditions to form sulfenic (-SOH), sulfinic (-SO2H), and sulfonic acid residues (-SO3H). Free H2S can react with sulfenic acid residues to form persulfidated proteins (-SSH). Either disulfide bridges or persulfidated proteins can be reduced back by the ferredoxin (Fd)–thioredoxin reductase (Fdx)–thioredoxin (Trx) system in the light or by the NADPH-thioredoxin reductase (Ntr)–thioredoxin (Trx) system in the dark or in non-photosynthetic tissues. Similar to oxidized thiol residues (-SOH, -SO2H, and -SO3H), persulfidated protein residues can be also oxidized to perthiosulfenic, perthiosulfinic, and perthiosulfonic acid (-SSO3H, -SSO2H, and -SSO3H), which can easily be reduced by reductants or thioredoxin systems. Fig. 4. View largeDownload slide Schematic representation of the function of protein persulfidation in protection. The major source of sulfide in plant cells must proceed from photosynthetic sulfate assimilation by sulfite reductase (SiR) activity in chloroplasts that is coupled to the biosynthesis of cysteine within the chloroplast, the cytosol, or the mitochondria by OASTL enzymes. l/d-DES and HCN/CAS activity can also generate H2S from cysteine within the cytosol or the mitochondria. Reactive oxygen species (ROS) generated by the light reaction of photosynthesis or stress processes can lead to sulfide oxidation to H2S2 or polysulfide (H2Sn), which can react with thiol residues in proteins to form persulfides (-SSH). Thiolate residues within proteins (-SH) can be oxidized by ROS to form disulfide bridges (-SS-) or by persistent oxidizing conditions to form sulfenic (-SOH), sulfinic (-SO2H), and sulfonic acid residues (-SO3H). Free H2S can react with sulfenic acid residues to form persulfidated proteins (-SSH). Either disulfide bridges or persulfidated proteins can be reduced back by the ferredoxin (Fd)–thioredoxin reductase (Fdx)–thioredoxin (Trx) system in the light or by the NADPH-thioredoxin reductase (Ntr)–thioredoxin (Trx) system in the dark or in non-photosynthetic tissues. Similar to oxidized thiol residues (-SOH, -SO2H, and -SO3H), persulfidated protein residues can be also oxidized to perthiosulfenic, perthiosulfinic, and perthiosulfonic acid (-SSO3H, -SSO2H, and -SSO3H), which can easily be reduced by reductants or thioredoxin systems. Hydrogen cyanide action and signaling Cyanide is a low molecular weight molecule that is highly reactive. It reacts with Schiff bases and keto radicals, producing cyanohydrins and nitrile derivatives, respectively. Its participation in the production of ribonucleotides, lipids, and amino acids is probably due to this reactivity (Patel et al., 2015). Cyanide is able to chelate di- and trivalent metallic ions in the prosthetic groups of some metalloproteins, affecting their function (Nagahara et al., 1999). Its action is lethal in mitochondria, where it blocks electron transfer from cytochrome c to oxygen and interrupts mitochondrial oxygenic respiration (Donato et al., 2007), but it also affects photosynthetic enzymes in chloroplasts (Berg and Krogmann, 1975). Despite its toxicity, cyanide is produced naturally in organisms from all kingdoms, including bacteria, fungi, arthropods, vertebrates, and plants. In most bacteria and fungi, cyanide is produced directly and stoichiometrically from the amino acid glycine in an oxidative reaction catalyzed by the enzyme cyanide synthase (Knowles, 1976; Blumer and Haas, 2000). In the case of some cyanide-producing algae such as Chlorella vulgaris, the precursors for the synthesis of cyanide are d-histidine and other amino acids (Pistorius et al., 1977). In the animal kingdom, some arthropods produce cyanogenic glucosides or accumulate the cyanogenic compounds produced by their host plants (Zagrobelny et al., 2008). Cyanide production has also been described in mammalian cells, where glycine gives cyanide in a reaction catalyzed by peroxidases (Stelmaszynska, 1986; Borowitz et al., 1997). In plants, cyanide biosynthesis is produced through two different mechanisms, one associate with the production of ethylene and camalexin (Peiser et al., 1984; Böttcher et al., 2009) and the other associated with the degradation of cyanogenic glucosides and cyanolipids (Poulton, 1990; Møller, 2010). Only plants producing high concentrations of cyanide through the second mechanism are considered cyanogenic, and they liberate cyanide from cyanogenic glucosides and lipids when they are in contact with predatory herbivores (Miller and Conn, 1980; Conn, 2008). Cyanogenic glucosides are widely distributed in all groups of plants and, since they have been extensively studied and recently reviewed (Zagrobelny et al., 2008; Møller, 2010; Mithöfer and Boland, 2012; Gleadow and Møller, 2014; Sun et al., 2018), we will not review them here. In non-cyanogenic plants, cyanide is produced exclusively during the biosynthesis of ethylene and the antipathogenic molecule camalexin (Yip and Yang, 1988; Wang et al., 2002; Glawischnig, 2007) (Fig. 5). Fig. 5. View largeDownload slide Pathways involved in the formation of hydrogen cyanide in non-cyanogenic plants. (A) A conjugate of cysteine and the tryptophan derivative indole-3-acetonitrile (IAN), Cys(IAN), is converted either spontaneously or by the CYP71B15 (PAD3) enzymatic action in the intermediate dihydrocamalexic acid (DHCA), giving hydrogen cyanide. DHCA is then converted to camalexin by the action of CYP71B15 (PAD3). (B) Ethylene is synthesized from 1-aminocyclopropane-1-carboxylic acid (ACC) by the ACC oxidase, giving ethylene, carbon dioxide, and hydrogen cyanide. Fig. 5. View largeDownload slide Pathways involved in the formation of hydrogen cyanide in non-cyanogenic plants. (A) A conjugate of cysteine and the tryptophan derivative indole-3-acetonitrile (IAN), Cys(IAN), is converted either spontaneously or by the CYP71B15 (PAD3) enzymatic action in the intermediate dihydrocamalexic acid (DHCA), giving hydrogen cyanide. DHCA is then converted to camalexin by the action of CYP71B15 (PAD3). (B) Ethylene is synthesized from 1-aminocyclopropane-1-carboxylic acid (ACC) by the ACC oxidase, giving ethylene, carbon dioxide, and hydrogen cyanide. Cyanide functions are diverse and sometimes controversial or unknown (Knowles, 1976; Borowitz et al., 1997; Siegien and Bogatek, 2006; Zagrobelny et al., 2008, 2018). In general, cyanide is associated with toxicity mechanisms for defense towards detrimental organisms, but other roles have also been described or suggested. In bacteria, cyanogenic glucosides and cyanide itself can serve as a nitrogen source or reservoir; likewise, they participate in the biocontrol mechanisms of certain Pseudomonas strains (Kuzmanovic et al., 2018), and cyanide functions as a virulence factor in some strains of the human opportunistic pathogen P. aeruginosa (Chowdhury and Bagchi, 2017). In different cyanogenic arthropods, cyanide and cyanogenic glucosides may act as pheromones for mating (Zagrobelny et al., 2007, 2018). In neurons, cyanide production activates synaptic receptors, and it is necessary for the analgesic action of opioid compounds (Gunasekar et al., 2000, 2004). In blood, phagocytes are able to produce cyanide from thiocyanate when challenged by bacteria or T-cell stimulators (Stelmaszynska, 1986). In plants, in addition to the protective role of cyanogenic compounds, cyanide itself plays an important role in several essential biological processes that deserve special attention in this review because they have driven the change in the perception of cyanide from it being a poison to it being a signaling molecule (Fig. 6). It is well known that the exogenous addition of cyanide breaks dormancy and thus stimulates seed germination. Indeed, transient treatment with millimolar concentrations of cyanide stimulates the germination of rice, barley, apple, sunflower, and Arabidopsis seeds, among others (Cohn and Hughes, 1986; Bogatek et al., 1991; Bethke et al., 2004; Oracz et al., 2008), and cyanide emission has been observed during the pre-germination stage of many seeds, including those from non-cyanogenic plants (Esashi et al., 1991). Furthermore, the germination burst observed in many species after a wildfire is due in part to cyanohydrins present in the smoke that release cyanide (Nelson et al., 2012; Flematti et al., 2013). In apple, the effect of cyanide in dormancy alleviation depends on the transient production of ROS and indirect protein carbonylation and ethylene emission (Gniazdowska et al., 2010; Krasuska et al., 2014). However, although the alleviation of sunflower dormancy by cyanide is also dependent on ROS production and protein carbonylation (Oracz et al., 2007), it seems to be independent of ethylene production but needs the ethylene signaling pathway, suggesting that it is required for both ethylene and cyanide action (Oracz et al., 2008). Finally, sugar metabolism is increased by cyanide treatment in apple and walnut kernel embryos during cyanide-induced alleviation of dormancy (Siegien and Bogatek, 2006; Gerivani et al., 2016). The understanding of the crosstalk between cyanide and hormone signaling during germination is an open subject and requires further investigation. Fig. 6. View largeDownload slide Schematic representation of hydrogen cyanide action in plant biology and proposed mechanisms. Cyanide induces the germination process and inhibits root hair elongation and plant defense against bacterial pathogens (upper part). Several mechanisms of action have been proposed, including the S-cyanylation of cysteine residues, which modifies protein activity, and hormone and/or ROS signaling modulation (lower part). Arrows and blunt lines represent activation and repression by hydrogen cyanide, respectively. Solid lines indicate demonstrated functions and mechanisms, and dashed lines indicate proposed mechanisms. Fig. 6. View largeDownload slide Schematic representation of hydrogen cyanide action in plant biology and proposed mechanisms. Cyanide induces the germination process and inhibits root hair elongation and plant defense against bacterial pathogens (upper part). Several mechanisms of action have been proposed, including the S-cyanylation of cysteine residues, which modifies protein activity, and hormone and/or ROS signaling modulation (lower part). Arrows and blunt lines represent activation and repression by hydrogen cyanide, respectively. Solid lines indicate demonstrated functions and mechanisms, and dashed lines indicate proposed mechanisms. Exogenously applied cyanide also has an effect on the plant response to biotic stress. It enhances the resistance of tobacco and Arabidopsis plants to viral attack independently from PATHOGENESIS-RELATED (PR) protein induction or signaling mediated by NON-EXPRESSER OF PR GENES 1 (NPR1) but probably involves the alternative oxidase (Chivasa and Carr, 1998; Wong et al., 2002), and protects rice from blast fungus infection (Iwai et al., 2006; Seo et al., 2011). Nevertheless, the effects of endogenously produced cyanide have been relatively less studied thus far. Plants have two enzymatic families for the detoxification of cyanide, β-cyanoalanine synthases (CASs; EC 4.4.1.9) and sulfurtransferases (STRs; EC 2.8.1.1), which incorporate cyanide into cysteine and thiosulfate or mercaptopyruvate, respectively. In A. thaliana, cyanide remains at non-toxic levels mainly due to CAS activity, with the mitochondrion-localized CAS-C1 (formerly CYS-C1) being the main CAS (Hatzfeld et al., 2000; Arenas-Alfonseca et al., 2018b). cas-c1 T-DNA insertion mutants that accumulate between 20% and 40% more cyanide in their tissues than in those of wild-type plants show a severe defect in root hair elongation (Garcia et al., 2010). Through the measurement of cyanide in roots and treatment with exogenous cyanide, the ethylene donor 1-aminocyclopropane-1-carboxylic acid (ACC), and a cyanide antidote (hydroxocobalamin, COB), it has been shown that the inhibition of root hair elongation is due specifically to the cyanide produced by cas-c1 mutants (Garcia et al., 2010; Arenas-Alfonseca et al., 2018b). The analysis of genetic crosses between cas-c1 and root hair mutants concluded that cyanide action is exerted at the early steps of the root hair elongation pathway and that this is independent of ROS production or direct NADPH oxidase inhibition (Arenas-Alfonseca et al., 2018a, b). In addition, during compatible and incompatible plant–bacterium interactions, cyanide accumulation and CAS-C1 activity are regulated in opposite manners, resulting in an increase in cyanide concentration and a decrease in CAS-C1 expression in the case of incompatible interactions. Mutation of CAS-C1 increases the tolerance to biotrophic pathogens, and this effect is reversed in the presence of COB, indicating that the endogenously produced cyanide might activate the pathogen response mediated by salicylic acid, hence influencing the plant immune system (Garcia et al., 2013). The mechanisms that underlie cyanide modulation, the mode of action, and the specific targets of this molecule are the subjects of recent investigation. The results described here suggest that the cyanide molecule, which has a low molecular weight, a high solubility in water, and a low melting point, could act as a signaling molecule in plants, similar to other molecules with widely accepted signaling roles such as NO·, H2O2, and H2S (Siegien and Bogatek, 2006). The mode of action of these signaling molecules is by provoking post-translational modifications in proteins such as nitrosylation, oxidation, and persulfidation specifically at the -SH groups of cysteines (Aroca et al., 2018). Chemically, cyanide per se is capable of S-cyanylating oxidized cysteine residues by the nucleophilic displacement of one of the sulfur atoms of the disulfide bridge to form a thiocyanate (Gawron, 1966). Although this protein modification had never been described before in any organism, it has been shown that cyanide itself could produce the S-cyanylation by the addition of SCN groups to cysteines and thus alter or modulate the function of proteins with this new post-translational modification. It is interesting to note that cyanide can form covalent adducts with the cysteines of immunoglobulin G and serum albumin in human plasma, which could serve as an indicator of cyanide poisoning in patients (Fasco et al., 2007). Very recently, it has been shown that S-cyanylation exists naturally in plants and modifies the activity of some proteins in vitro (Garcia et al., 2019) (Fig. 6). Indeed, a method has been adapted based on the hypersensitivity to hydrolysis of the peptide bond adjacent to an S-cyanylated cysteine at basic pH, especially in the presence of NH4OH (Wu and Watson, 1998; Qi et al., 2001). By directly treating extracts of plant proteins with NH4OH to induce the cleavage of the peptide bond adjacent to an S-cyanylated cysteine, proteins that undergo hydrolysis have been identified, and their S-cyano modification at cysteine residues has been verified by MS. In addition, the massive analysis of protein extracts by LC/MS has enabled the identification of other naturally S-cyanylated proteins in plant tissues, most of which involve glycolysis, the Calvin cycle, and the metabolism of S-adenosylmethionine. Moreover, the in vitro analysis of selected target proteins has shown that treatment with cyanide and the consequent S-cyanylation modifies their activity, by either activating or inactivating them (Garcia et al., 2019). 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TI - Signaling by hydrogen sulfide and cyanide through post-translational modification
JF - Journal of Experimental Botany
DO - 10.1093/jxb/erz225
DA - 2019-08-19
UR - https://www.deepdyve.com/lp/oxford-university-press/signaling-by-hydrogen-sulfide-and-cyanide-through-post-translational-v0xXaVSSWE
SP - 4251
VL - 70
IS - 16
DP - DeepDyve
ER -