Chapter 11

Reactive Nitrogen Species and the Role of NO in Abiotic Stress

Dagmar Procházková, Jan Sumaira, Nad'a Wilhelmová, Daniela Pavlíková and Jiřina Száková

Nitric oxide (NO) and related reactive nitrogen species have attracted the attention of plant biologists particularly in connection with stresses. Most experiments investigating the participation and effects of NO under abiotic stresses employ exogenous application of NO. The present overview offers a short summary of the influence of exogenously applied NO, of changes in endogenous NO content, and of changes in the reactive nitrogen species metabolism under the effect of various types of abiotic stresses.

Keywords

drought; waterlogging; high temperature; cold; salinity; heavy metals; air pollutants; high light; UV-B radiation

11.1 Introduction

In 1772 Joseph Priestley characterized nitric oxide (NO) as a colorless, nonflammable, odorless, and toxic gas. After the industrial revolution, this compound was studied solely as a component of air pollution because NO is involved in ozone layer destruction and in acid rain (Corpas et al., 2008a). The interest of biologists gained special momentum when this molecule was identified as a potent endogenous vasodilator (Schmidt and Walter, 1994). With the finding that NO has many functions in mammalian cells, such as regulation of vascular tone, neuronal signaling, or immune response to infection (Knowles and Moncada, 1994), various studies have reported its presence in the plant kingdom as well.

Nitric oxide produced by plants was first observed by Klepper (1979) in soybean plants treated with photosynthetic inhibitor herbicides or other chemicals, as well as under dark and anoxic conditions. Mounting evidence has proved NO to be involved in many plant physiological and metabolic processes, including adaptation to environmental stresses (Uchida et al., 2002). Because of its participation in numerous biotic and abiotic responses, NO has been proposed even as a general stress molecule (Gould et al., 2003).

11.2 The reactive nitrogen species

Nitric oxide may react with superoxide radicals forming peroxynitrite (ONOO−) (Kissner et al., 1997). ONOO− also may be produced by the enzyme nitrate reductase (NR) in the presence of oxygen and NAD(P)H (Yamasaki and Sakihama, 2000). ONOO− is a powerful oxidant that can react with DNA, lipids, and proteins under physiological conditions, resulting in cellular damage and cytotoxicity (Radi, 2004; Szabó et al., 2007). This molecule may protonate, as a result of which peroxynitrous acid is formed, a source of nitrogen dioxide (NO2) and hydroxyl radicals (Wendehenne et al., 2001).

NO can perform important post-translational protein modifications also through nitration and S-nitrosylation. Nitration is a general chemical process for the introduction of a nitro group NO2 into a chemical compound. Although there are several amino acids that are preferentially nitrated, such as tyrosine, tryptophan, cysteine, and methionine, most studies done consider tyrosine nitration. This process consists of the addition of a nitro group to one of two equivalent orthocarbons of the aromatic ring of tyrosine residues (Corpas et al., 2009). Tyrosine nitration has been shown to be competent to change the function of a protein in the following ways: (1) gain of function, as well as no effect on function; and (2) inhibition of function, which is a much more common result of protein tyrosine nitration (Radi, 2004). In plants, the latest data hint that nitrotyrosine may serve as a marker of nitrosative stress during abiotic stress in the same way as protein carbonylation or lipid peroxidation does (e.g., Wilhelmová et al., 2006; Valderrama et al., 2007; Corpas et al., 2008a; Chaki et al., 2009).

S-nitrosylation refers to the binding of an NO group to an SH group in a cysteine residue; it plays a significant role in NO-mediated signaling (Stamler et al., 2001). Proteins exhibit a striking differential susceptibility to S-nitrosylation; however, in this respect, their overall content of cysteines is not important (Wang et al., 2006). In plants, many proteins are S-nitrosylated under physiological or stress conditions. These observations led to the first insights into S-nitrosylation-dependent regulation of protein function (Lindermayr and Durner, 2009). In plant systems, S-nitrosylation of proteins was found to contribute to gene regulation (Serpa et al., 2007; Ferrarini et al., 2008; Palmieri et al., 2008; Tada et al., 2008) and modulates phytohormonal signaling (Melotto et al., 2006) and cell death (Hara et al., 2005; Belenghi et al., 2007; Holtgrefe et al., 2008). The remarkable specificity of S-nitrosylation is conferred by different factors such as the subcellular compartmentalization of NO sources and the target protein (Hess et al., 2005).

S-nitrosoglutathione is a nitric oxide-derived molecule generated by the interaction of NO with reduced glutathione (GSH) during S-nitrosylation, or by a process of transnitrosation from other nitrosothiols (RSNOs) with GSH (Corpas et al., 2013). The reaction appears to take place either through the formation of N2O3 or the addition of NO to a glutathionyl radical formed during this reaction (Broniowska et al., 2013). RSNOs, especially GSNO, may serve both as an intracellular NO deposit and as a transporter for NO throughout the cell (Singh et al., 1996a,b). The formation of RSNOs indicates the reaction of nitrosonium with a thiol group present in free cysteine, peptides, or proteins (Carver et al., 2005; Dahm et al., 2006; Sun et al., 2006; Chaki et al., 2009). These compounds carry out important biological reactions such as NO release, transnitrosation, S-thiolation, as well as direct actions (Hogg, 2000; Stamler et al., 2001). Under physiological conditions, RSNOs are considered to provide protection against cellular damage induced by oxidative and nitrosative stress (Liu et al., 2004; Sun et al., 2006; Valderrama et al., 2007; Chaki et al., 2009).

The enzyme GSNO reductase (GSNOR) can regulate the cellular level of GSNO and therefore NO content via the NADH-dependent reduction of GSNO to oxidized glutathione (GSSG) and NH3, and in this way, the content of overall RSNO (Liu et al., 2001; Lamotte et al., 2005). In microbes and in mammal cells, GSNOR may play a dual role: (1) turning off GSNO-derived NO signaling and (2) cellular protection against nitrosative stress by controlling excess S-nitrosylation (Liu et al., 2001; Sakamoto et al., 2002).

11.3 Drought stress

From the point of view of plant productivity, it is especially important to address drought stress. It causes several interlinked physiological consequences that are deleterious to plant cells, organs, and/or tissues. One of them is the overproduction of the reactive oxygen species (ROS), including superoxide anion, hydrogen peroxide, singlet oxygen, and hydroxyl radicals.

Drought promoted NO production in pea, beat, tobacco, rice, cucumber, and grapevine plants (Gould et al., 2003; Kolbert et al., 2005; Arasimowicz-Jelonek et al., 2009; Patakas et al., 2010; Xiong et al., 2012). Hao et al. (2008) noted that both NO synthase (NOS)-like activity and the rate of NO release increased substantially under dehydration stress. They suggested that NO dependence on NOS-like activity serves as a signaling component in the induction of protective responses and is associated with drought tolerance in maize seedlings. On the contrary, the activation state and maximal extractable activity of the important NO producer, NR, declined rapidly in response to drought (Foyer et al., 1998). Similarly, NR activity was significantly higher under an optimal water regime than in drought stress conditions (Kröek et al., 2008).

Correlation among signal molecules of abscisic acid (ABA), H2O2, and NO was confirmed by several reports. It has been shown that NO selectively activates intracellular Ca2+ channels in broad bean (Vicia faba) guard cells via a cGMP/cADPR-dependent signaling pathway, disentangling the participation of NO as a signaling molecule in the ABA-induced stomatal closure (Durner et al., 1998; García-Mata and Lamattina, 2003). In Arabidopsis guard cells, NR-mediated NO synthesis was sensitive to ABA treatment, and was required for stomatal closure induced by ABA (Desikan et al., 2004). In addition, ABA synthesis in wheat roots in response to water deficiency was much higher in the presence of NO donors and ROS, which suggests synergistic action of ROS and NO (Zhao et al., 2001). As a confirmation of this fact, the increase of ABA accumulation was blocked after the addition of ROS scavengers and NOS inhibitor. The accumulation of NO also proved to be necessary in bean stomata during ABA-induced stomata closure (García-Mata and Lamattina, 2003).

Exogenously applied NO donor sodium nitroprusside (SNP) reduced water loss from detached wheat leaves and decreased transpiration rate, ion leakage, and induced stomatal closure, while a specific NO scavenger suppressed all these NO actions (García-Mata and Lamattina, 2001). Liao et al. (2012) showed that SNP improved the photosynthetic performance of leaves and alleviated the negative effects of drought on carbohydrate and nitrogen accumulation in marigold (Tagetes erecta L.). Exogenously applied NO improved drought tolerance in cucumber, maize, and rice. It has been suggested that increased antioxidant protection, which scavenges ROS, facilitated better cellular membrane stability and maintained photosynthesis and water status (Hao et al., 2008; Arasimowicz-Jelonek et al., 2009; Farooq et al., 2009).

Accumulation of proline is one of the well-known adaptive responses of plants against drought stress. Exogenous application of NO alleviated osmotic stress by decreasing oxidative damage and by stimulation of proline accumulation in wheat (Tan et al., 2008). On the contrary, Xiong et al. (2012) demonstrated that although drought stress induces a simultaneous accumulation of NO and proline, NO is expendable for accumulation of proline in rice leaves. Therefore, they excluded the eventuality that NO plays a downstream role for ABA in drought-induced proline accumulation in rice leaves.

11.4 Waterlogging stress

In nature, plants are often exposed to transient or permanent waterlogging. Waterlogging, designated also as flooding, drastically influences a majority of the soil physicochemical properties, most of all soil redox potential, pH and O2 levels. Thus, conditions of hypoxia (the reduction of O2 below the optimal level) or anoxia (the complete lack of O2) are commonly encountered by plant roots. These O2 restrictive conditions significantly influence plant development, growth, and survival (Parent et al., 2008).

Waterlogging substantially promotes NO production (Sui et al., 2010). Within 12 days of waterlogging, NO production, NR, and NOS activities increased first, then decreased subsequently in Malus hupehensis roots. Similarly, Sairam et al. (2012) reported increased NO production and NR activity in V. luteola during flooding.

Hypoxic stress activated NR leading to an increase of NO synthesis and higher NO emission from plant tissues (Perazzolli et al., 2006). In plant roots, two different types of NR are known: one is located in the cytosol (cNR) and the other is attached to the plasma membrane that faces the apoplast (Stöhr and Ullrich, 1997; Stöhr and Mäck, 2001). In barley (Hordeum vulgare) roots, a 2.5-fold activation of cNR occurred under hypoxia (Botrel and Kaiser, 1997). In root cultures of Arabidopsis, two NR genes were induced under hypoxia: NR1 gene showed mild induction after 0.5 to 4 h of hypoxia and strong induction after 20 h, while NR2 gene was strongly activated in 2 to 4 h and even more after 20 h of low oxygen conditions (Klok et al., 2002).

Nitric oxide is known to be an effective inhibitor of cytochrome oxidase in the mitochondrial electron transport chain and may further reduce cell respiration and energy production (Zottini et al., 2002). The hemeproteins with the highest avidity (e.g., hexacoordinate hemoglobins) retain oxygen even under anoxic conditions, resulting in their being extremely effective NO scavengers but essentially incapable of producing NO (Igamberdiev et al., 2010). A class 1 nonsymbiotic hemoglobin (nsHbs) from Arabidopsis, barley, and alfalfa are known to detoxify NO to nitrate in an NAD(P)H-dependent manner (Seregélyes et al., 2000; Igamberdiev and Hill, 2004; Perazzolli et al., 2004). Indeed, NO accumulation, stimulated by hypoxia, was significantly suppressed in Arabidopsis plants expressing Arabidopsis class-1 nsHb in alfalfa (Medicago sativa) root cultures overexpressing barley class-1 nsHb and in maize (Zea mays) cell lines expressing the same barley nsHb (Dordas et al., 2003b; Dordas et al., 2004; Perazzolli et al., 2004). On the other hand, the transgenic lines suppressed for nsHbs expression showed increased NO concentrations (Dordas et al., 2003b; Dordas et al., 2004; Perazzolli et al., 2004). This sequence of reactions, in which NO is oxidized to nitrate, is referred to as the Hb/NO cycle (Dordas et al., 2003a). Arabidopsis class-1 nsHb is also able to metabolize GSNO through production of S-nitrosohemoglobin (Perazzolli et al., 2004).

Interestingly, NO is considered to be an attractive candidate for involvement in aerenchyma formation, which is a common solution for plants exposed to waterlogging. Depending on the NO concentration and other factors, nitric oxide is able to either accelerate or inhibit apoptosis (Kim et al., 2001). The effect may be either direct, through cell necrosis, or through regulatory pathways, and it may be selective in relation to the cells that do respond (Sairam et al., 2008).

11.5 High temperature stress

High temperature is an important limiting factor of crop productivity. Heat stress induces increased ROS production, oxidative stress, lipid peroxidation, enzyme inactivation, membrane injury, protein degradation, pigment bleaching, and DNA strand disruption in cells (Suzuki and Mittler, 2006). Hasanuzzaman et al. (2013) suggested that ABA may impart thermotolerance by raising the level of NO. High temperature treatment of lucerne cells resulted in an increase of NO synthesis (Leshem, 2001; Neill et al., 2003). Most probably the observed effects were related to the antioxidant action of NO, which elevates negative effects caused by the intensification of peroxidative metabolism under thermal stress (Neill et al., 2002). On the contrary, heat inhibited NO accumulation in cultured guard cell protoplasts of Nicotiana glauca (tree tobacco) (Beard et al., 2012).

Uchida et al. (2002) showed that pretreatment with low levels of NO induced not only ROS-scavenging enzyme activities but also expression of transcripts for oxidative stress-related gene encoding sucrose-phosphate synthase, Δ1pyrroline-5-carboxylate synthase, and the small heat shock protein 26 in rice seedlings. They suggested that NO can increase heat tolerance by acting as a signal molecule. Bouchard and Yamasaki (2008, 2009) suggested that heat stress-stimulated NO production could play a role in the induction of cell death by mediating an increase in caspase-like activity in Symbiodinium microadriaticum.

Application of two nitric oxide donors, SNP and S-nitroso-N-acetylpenicillamine (SNAP), significantly mitigated heat stress-induced ion leakage, growth suppression, and cell viability decrease in calluses of two ecotypes of reed (Phragmites communis Trin.). H2O2 and malondialdehyde contents were decreased and the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and peroxidase (POD) increased in both ecotypes (Song et al., 2006).

11.6 Low temperature stress

A low temperature (cold stress) causes many changes in biochemical and physiological processes and ROS-homeostasis in plants (Xin and Browse, 1998; Suzuki and Mittler, 2006; Zhao et al., 2009; Siddiqui et al., 2011). Low temperature stimulated an increase of NOS and S-nitrosoglutathione reductase (GSNOR) activities. This was accompanied by an increase in the contents of NO and S-nitrosothiols, and also by an intensification of the immunoreactivity with an antibody against NO2-tyrosine (Corpas et al., 2008b).

Cold acclimation induced an increase in NO production in leaves of both wild-type (WT) and mutant nitric oxide associated 1/resistant to inhibition with fosmidomycin 1 (1 AtNOA1/RIF1) A. thaliana, while the NO level in NR-defective double mutant (nia1nia2) leaves was lower compared to WT plants, although little change occurred during acclimation. Cold acclimation stimulated NR activity and induced up-regulation of NIA1 gene expression and reduced the quantity of NOA1/RIF1 protein and inhibited NOS activity. These results indicated that up-regulation of NR-dependent NO synthesis underpins cold acclimation-induced NO production. Seedlings of nia1nia2 were less tolerant to freezing than WT plants. Treatment with NR inhibitor, NO scavenger, or NO donor showed that the NR-dependent NO level was positively correlated with tolerance to freezing.

Further, cold acclimation up- and down-regulated expression of Δ1-pyrroline-5-carboxylate synthetase1 and proline dehydrogenase genes, respectively, resulting in enhanced accumulation of proline in WT plants. The stimulation of proline accumulation by cold acclimation was reduced by NR inhibitor and NO scavenger, while proline accumulation by cold acclimation was not affected by the NOS inhibitor. In contrast to WT plants, cold acclimation up-regulated proline dehydrogenase gene expression in nia1nia2 plants, leading to less accumulation of proline in them. These findings demonstrated that NR-dependent NO production plays an important role in cold acclimation and induced an increase in freezing tolerance by modulating proline accumulation in Arabidopsis (Zhao et al., 2009).

11.7 Salinity stress

Salinity is one of the important abiotic stresses affecting plant productivity due to the alterations produced in photosynthesis and respiration, and in the metabolism of proteins and nucleic acids (Hasegawa et al., 2000). The primary effects of high salinity consist of hyperosmotic stress and ion disequilibrium that produce secondary effects such as oxidative stress (Hasegawa et al., 2000; Zhu, 2001). Increase of endogenous NO under salinity stress has been observed, for example, in tobacco leaf cell suspensions and in cotton calli (Gould et al., 2003; Vital et al., 2008).

Survival of more green leaf tissue of rice seedlings under salinity stress occurred when treated with SNP; this also resulted in a higher quantum yield for photosystem (PS) II, an increase in activity of antioxidant enzymes, and the expression of specific stress-resistant genes (Uchida et al., 2002). The same NO donor promoted seed germination and root growth of yellow lupine seedlings (Kopyra and Gwóźdź, 2003) and increased the growth and dry weight of maize seedlings (Zhang et al., 2006).

It has been shown that nitric oxide can serve as a signal in inducing salt resistance by increasing the cellular K:Na ratio, which is dependent on the increased plasma membrane H+-ATPase activity in calluses from reed (Phragmites communis) plants (Zhao et al., 2004) and from Populus euphratica (Zhang et al., 2007) and in maize seedlings (Zhang et al., 2006). In olive leaves, salinity stress induced the production of NO, S-nitrosoglutathione, and S-nitrosothiols, and a rise in tyrosine-nitrated proteins mainly in the vascular tissues (Valderrama et al., 2007). Thus, vascular tissues may play an important function in the redistribution of NO-derived forms during nitrosative stress and in signaling-related processes (Valderrama et al., 2007).

Arabidopsis mutant Atnoa1 with an impaired in vivo NO synthase activity was more sensitive to NaCl stress compared to wild type (Guo et al., 2003; Zhao et al., 2007). When grown under NaCl stress, the WT Arabidopsis plants exhibited a higher survival rate than Atnoa1 plants and the latter plants had higher levels of hydrogen peroxide than wild-type plants (Zhao et al., 2007). In Atnoa1 plants, salt stress has been mitigated by SNP treatment, while the inhibition of nitric oxide accumulation in the WT plants produced the opposite effect (Zhao et al., 2007).

Vital et al. (2008) studied the roles of superoxide and NO in the NaCl-induced up-regulation on antioxidant enzyme activities in NaCl-tolerant cotton calli. The direct addition of NO gas produced no change in the activities of CAT and GR and caused a significant decrease in APX activity when compared to the controls. When the calli was treated with SNP in the absence of NaCI stress, APX and GR activities decreased significantly and CAT activity was only slightly higher than the control. Treatment with SNP in the presence of NaCl stress resulted in a significant decrease in APX activity, and GR and APX activities were not significantly different from those observed with the NaCl treatment alone. These results suggested that NO may play a role in switching “off” the response after other mechanisms in the cascade of events responsible for NaCl tolerance have been activated (Vital et al., 2008). Recently, Boldizsár et al. (2013) reported that modification of NO levels affected salt-induced, glutathione-dependent redox changes and simultaneously the free amino acid composition and the level of several free amino acids.

11.8 Heavy metal stress

Agricultural soils in many parts of the world are contaminated by heavy metals such as Cd, Cu, Zn, Ni, Co, Cr, Pb, and As (Yadav, 2010). Among the heavy metals Fe, Mo, and Mn are important as micronutrients; Zn, Ni, Cu, V, Co, W, and Cr are toxic elements with high or low importance as trace elements. As, Hg, Ag, Sb, Cd, Pb, and U have no known function as nutrients and seem to be more or less toxic to plants (Goldbold and Huttermann, 1985; Nies, 1999; Saxena and Shekhawat, 2013).

Several reports have suggested the following mechanisms by which NO helps plants resist heavy metal stress. (1) NO can indirectly scavenge ROS induced by heavy metals. Thus, NO might be involved in increasing the antioxidant content and antioxidative enzyme activity in plants (Hsu and Kao, 2004). (2) NO can affect root cell wall components, therefore nitric oxide may increase heavy metal accumulation in root cell walls and decrease its concentrations in the soluble fraction of plant leaves (Xiong et al., 2010). (3) NO could function as a signaling molecule in the cascade of events leading to changes in gene expression (Pagnussat et al., 2002, 2003; García-Mata and Lamattina, 2003; Wilson et al., 2008; Xiong et al., 2012).

11.8.1 Cadmium

Cadmium (Cd) is one of the most toxic elements with a long biological half-life. Its presence as a pollutant in agricultural soil is mainly due to anthropogenic activities (De Michele et al., 2009). The main symptoms, in addition to others, of Cd-induced toxicity in plants are: chlorosis, altered chloroplast ultrastructure, photosynthesis inhibition, inactivation of enzymes in CO2 fixation, and induced lipid peroxidation (Gill et al., 2013). Early studies have shown that Cd inhibited NR activity in pea shoots (Hernández et al., 1997), which may result in decreased NO production. Cd induced a significant lowering of nitric oxide in the vascular tissues of pea (Barrosso et al., 2006). On the other hand, NO increased in the roots of Brassica juncea L. and Pisum sativum L. (Bartha et al., 2005) and treatment with Cd for four weeks produced a 2.4-fold increase in NO (Mahmood et al., 2009). Similarly, CdCl2 treatment of A. thaliana cell suspension cultures was accompanied by a rapid increase in NO and phytochelatin synthesis, which continued to be high as long as the cells remained viable. In addition, inhibition of NO synthesis resulted in partial prevention of hydrogen peroxide increase, expression of the marker senescence-associated gene12, and mortality, indicating that NO is actually required for Cd2+-induced cell death. NO also modulated the extent of phytochelatin content, and possibly their function, by S-nitrosylation (De Michele et al., 2009). NO was also reported to be responsible for the Cd-induced growth inhibition of Arabidopsis primary roots, as well as to contribute to Cd2+ toxicity by favoring Cd2+ versus Ca2+ uptake and by initiating a cellular pathway resembling those activated on Fe deprivation (Besson-Bard et al., 2009).

Nitric oxide production under Cd stress seems to be time and concentration dependent. Treatment with 100 mM Cd for 24 h significantly decreased the NO content in the crown roots of 7-day-old rice seedlings but in the crown roots of 4-week-old rice plantlets under 0.2 mM Cd stress, the NO levels increased rapidly in the first half-hour and then began to decrease. Four h later, the NO level dropped even lower than in the control, and 24 h later, it reached its nadir (Xiong et al., 2009). Soybean cells treated with two concentrations of Cd2+ showed a dose-dependent and rapid production of NO, which may suggest that NO functions as a signal molecule involved in mitigation of the heavy metal stress (Kopyra et al., 2006).

Pretreatment with SNP improved Cd tolerance in Medicago truncatula roots by reducing oxidative damage, maintaining the auxin equilibrium, and increasing the accumulation of proline and glutathione (Xu et al., 2010a). When sunflower (Helianthus annuus) plants were pretreated with SNP, Cd-induced chlorophyll decay was evidently reduced: chlorophyll content remained in 88% of those shown by control plants (Laspina et al., 2005). In tomato plants, SNP promoted ROS-scavenging enzymes, reduced accumulation of H2O2, and induced the activity of H+-ATPase and H+-pyrophosphatase in plasma membrane or tonoplast (Cui et al., 2010).

Nitric oxide treatment also significantly elevated the depressed APX activity in barley seedlings during 10 and 15 days of CdCl2 treatment (Chen et al., 2010). In sunflower leaves treated with 0.5 mm Cd, APX activity increased even more—163% after application of exogenous NO (Laspina et al., 2005). NO stimulated SOD activity in Lupinus roots grown with Cd, which in roots preincubated with SNP was significantly higher (Kopyra and Gwóźdź, 2003).

NO also increased the content of low-molecular antioxidant ascorbate in Cd-treated rice leaves (Hsu and Kao, 2004). Similarly, exogenous NO increased glutathione peroxidase (GPX) activity in sunflower leaves treated with Cd (Laspina et al., 2005). In contrast, a decrease in GPX and CAT activities were observed when Cd-stressed wheat roots were treated with NO (Singh et al., 2008).

11.8.2 Copper

Nitric oxide increased in the adventitious roots of Panax ginseng exposed to Cu for 24 h (Tewari et al., 2008). Zhang et al. (2008) investigated the effects of various Cu concentrations and treatment times on NO concentration in Chlamydomonas reinhardtii. Their results indicated that the amount of NO increases with the duration and concentration of Cu exposure. It has been demonstrated that the addition of SNP in combination with Cu lowered the inhibition levels of carbon fixation, O2 evolution, maximum quantum yield of PSII, and significantly reduced the oxidative burst in NH4+-grown Chlorella (Singh et al., 2004).

Tewari et al. (2008) suggested that reduction of excess Cu-induced toxicity by SNP is most likely mediated through the modulation in the activities of antioxidant enzymes involved in H2O2 detoxification (CAT, POD, APX) and in the maintenance of cellular redox couples (GR), as well as the contents of molecular antioxidants (particularly nonprotein thiol, ascorbate, and its redox status). An exogenous NO supply also improved the activity of SOD, an enzyme responsible for O2− dismutation, and NADPH oxidase, an enzyme responsible for O2− generation, in excess Cu supplied adventitious roots of Panax ginseng (Tewari et al., 2008). Hu et al. (2007) reported that NO pretreatment improved wheat seed germination and alleviated oxidative stress under Cu toxicity by increasing the activities of SOD and CAT and by decreasing the lipoxygenase activity and malondialdehyde synthesis. Singh et al. (2004) proposed that the protective effect of NO could consist of suppression of superoxide production and subsequently by suppression of hydroxyl production from superoxide and peroxynitrite.

11.8.3 Arsenic

Under arsenic stress conditions, plants are subjected to different types of changes, which include element uptake and transport, metabolism, and gene expression (Catarecha et al., 2007; Verbruggen et al., 2009; Zhao et al., 2009; Guo et al., 2012; Leterrier et al., 2012). In tall fescue, the application of 100 mM SNP reduced arsenic-induced oxidative damage in leaves (Jin et al., 2010). In Arabidopsis under As treatment, NO content increased in roots and this increase was accompanied by a rise in protein tyrosine nitration in leaves (Leterrier et al., 2012), which is regarded as a marker of nitrosative stress (Corpas et al., 2008a).

S-nitrosoglutathione (GSNO) is formed by the S-nitrosylation reaction of NO with GSH. GSNO may have great physiological importance for plants since it is thought to function as a mobile reservoir of NO bioactivity (Durner and Klessig, 1999). In Arabidopsis under As conditions, GSNO content decreased. This may be due to the rise in GSNOR activity because this enzyme catalyzes the NADH-dependent reduction in GSNO to GSSG and NH3 and is thus a key player in the NO metabolism under physiological and stress conditions (Leterrier et al., 2012).

Pretreatment with SNP dramatically ameliorated the As-induced decrease in the root and coleoptile lengths of rice. Nitric oxide not only exhibited ROS scavenging activity but also partially reversed the As-induced increase in the activities of the antioxidant enzymes SOD, APX, GR, and CAT (Singh et al., 2009). In tall fescue, the application of 100 mM SNP alleviated arsenic-induced electrolyte leakage and contents of malondialdehyde, hydrogen peroxide, and superoxide radical and increased activities of SOD, CAT, and POD (Jin et al., 2010).

11.8.4 Zinc

Zinc, as a microelement, is essential and involved in numerous physiological processes, but at high concentrations is toxic. In roots of Solanum nigrum, Zn-induced NO production promoted an increase in ROS content by modulating the activities of NADPH oxidase (NOX) and antioxidant enzymes. Afterward, programmed cell death (PCD) was observed in primary root tips. Zn-induced NO production also influenced the number of lateral roots and root hair growth and thus modulated root system architecture and activity. These results demonstrated that NO-mediated plant responses increased Zn tolerance through morphological and physiological changes in the roots.

The suplementation with NO scavengers, 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (PTIO), or animal NOS inhibitor L-NAME forestalled the rhizosphere acidification in response to surplus Zn, suggesting that Zn-induced NO production improves H+-ATPase activity and root system activity; therefore, it is advantageous for the plants’ response to long-term Zn toxicity. Thus, NO production and the subsequent PCD in root tips exposed to excess Zn are favorable for the S. nigrum seedling response to long-term Zn toxicity by modulating root system architecture and subsequent adaptation to Zn stress (Xu et al., 2010b).

11.9 Air pollutants

Interestingly, during the 1970s, attention with regard to NO was focused on its participation in air pollution because nitric oxide contributes to acid rain and the depletion of the ozone layer. Both aspects have harmful effects on plants, the environment, and human health. For that reason, this molecule was considered “toxic” (Corpas, 2011). Air pollution studies with plants have shown that NO inhibits photosynthetic CO2 assimilation (Hill and Bennett, 1970; Bruggink et al., 1988; Takahashi and Yamasaki, 2002).

11.10 Exposure to high light conditions

Light is essential for plant growth and development, but when plants are subjected to excessive light, photoinhibition occurs and ROS production increases (Asada, 2006). These events often result in photooxidative damages, thus light can be one of the most deleterious environmental factors (Xu et al., 2010c). For example, NO emission by NR was higher under light conditions than in the dark in sunflower plants (Rockel et al., 2002).

In pea leaves, high-intensity light did not result in significant changes in NO content although NOS-like activity was significantly enhanced. High light intensity did not change GSNOR activity, but it did increase the content of RSNOs and tyrosine nitration (Corpas et al., 2008b).

In the thylakoid membranes of A. thaliana, leaves adapted to growth light and subsequently, when exposed to high light, changes in the nitration level of 23 tyrosine residues in five PSI and nine PSII proteins were determined. The majority of them showed a lower nitration level in PSI and PSII complexes and supercomplexes under high light conditions, as compared to growth light. On the contrary, the nitration level significantly increased in assembled/disassembled PSI and PSII subcomplexes under high light conditions (Galetskiy et al., 2011).

SNP treatment of tall fescue (Festuca arundinacea) leaves under high light stress resulted in mitigated light-induced electrolyte leakage, and in lower malondialdehyde, carbonyl, H2O2, and superoxide radical contents. At the same time, activities of SOD, CAT, and APX increased (Xu et al., 2010c).

11.11 UV-B radiation

Plants, as sessile organisms that absorb sunlight to grow and develop, are inevitably exposed to ultraviolet (UV) radiation (200–400 nm) that represents almost 7% of the electromagnetic radiation emitted from the Sun. The majority of UV-B radiation (280–320 nm) is absorbed by stratospheric ozone but a minor proportion is transmitted to the Earth’s surface (Frohnmeyer and Staiger, 2003; Tossi et al., 2012). High doses of UV-B light induce the production of ROS, causing damage to proteins, lipids, and DNA; it also affects the plant cells’ integrity, morphology, and physiology (Frohnmeyer and Staiger, 2003; Tossi et al., 2009).

Too much exposure of plants to UV-B radiation leads to an increase of ion leakage, loss of chlorophyll, and decreases the maximum efficiency of PSII photochemistry (Fv/Fm) and the quantum yield of PSII electron transport; it also increases H2O2 and thylakoid membrane protein oxidation. The endogenous NO level increased 2-fold in UV-B irradiated maize (Zea mays) leaves (Tossi et al., 2011).

Xue et al. (2006) showed that UV-B radiation significantly induced NOS activity and promoted NO release as well. Similarly, NO and H2O2 contents were increased in bean (Phaseolus vulgaris) leaves. After treatment with an inhibitor of NOS (Nω-nitro-l-arginine), nitric oxide release was blocked. Application of CAT not only effectively eliminated H2O2 in the leaves but also inhibited the activity of NOS and the emission of NO. In contrast, treatment with exogenous H2O2 increased both NOS activity and NO content. Zhang and Zhao (2008) suggested that NO production was mediated by H2O2 through higher NOS activity. NR activity of silver birch leaves irradiated with UV-B significantly increased, indicating that activity is inducible by UV-B. Further, treatment of the leaves with NR inhibitor tungstate abolished UV-B-triggered NO generation, which suggests that NR may be essential for UV-B-triggered NO. Moreover, UV-B-induced NIA1 (gene encoding NR) expression coincides with UV-B-triggered NO generation and NR activity (Zhang et al., 2011).

SNP pretreatment of A. thaliana seedlings recovered the UV-B inhibited root growth as compared to PTIO pretreatment. It has been shown that 24 h after UV-B irradiation the organization of microtubules in root epidermal cells of SNP-pretreated A. thaliana seedlings was partially recovered; with c-PTIO-pretreated ones, the organization of microtubules was not distinctly improved. Krasylenko et al. (2012) proposed that the enhanced NO levels can protect microtubule organization as well as microtubule related processes of root growth and development against disrupting effects of UV-B.

Pretreatments with SNP prevented chlorophyll loss and ion leakage in UV-B-treated soybean plants (Santa-Cruz et al., 2010). SNP also permitted the survival of more green leaf tissue, preventing chlorophyll content reduction and a higher quantum yield of PSII than in nontreated controls under UV-B stress; this suggested that NO has a protective effect on chloroplast membrane in maize leaves (Kim et al., 2001). In addition, treatment with SNP decreased chlorophyll loss, abated Fv/Fm decrease, and alleviated the increase in carbonyl groups in thylakoid membrane proteins after bean UV-B irradiation (Phaseolus vulgaris) (Shi et al., 2005). SNP application also significantly increased proline content in an algal culture of Spirulina platensis (Xue et al., 2006).

The important factor in plant protection against UV-B radiation is represented by flavonoid-ubiquitous plant secondary products that are best known as the characteristic red, blue, and purple anthocyanin pigments of plant tissues (Winkel-Shirley, 2001; Ryan et al., 2002). Given that NO is involved in secondary metabolite production, it is therefore deduced that NR should play a role in UV-B-induced flavonoid accumulation. This was confirmed by the fact that the pretreatment of silver birch leaves with NR inhibitors abolished UV-B-induced flavonoid accumulation (Zhang et al., 2011).

The involvement of nitric oxide in the up-regulation of the gene encoding chalcone synthase in response to UV-B exposure was shown by spraying A. thaliana plants with PTIO or L-NAME. Both prevented the induction of chalcone synthase expression, indicating that up-regulation of chalcone synthase by UV-B requires NO (Mackerness et al., 2001).

Nitric oxide donor SNP up-regulated the expression of three transcription factors involved in the phenylpropanoid (as flavonoids and synapate esters) biosynthesis pathway and, consequently, the expression of chalcone synthase and chalcone isomerase. The activation of this signaling pathway resulted in an increase of flavonoid and anthocyanin content (Tossi et al., 2011). In addition, maize leaves pretreated with the specific NO scavenger, cPTIO, do not accumulate NO and flavonoids in response to UV-B (Tossi et al., 2011).

11.12 Conclusion and future prospects

It is obvious that NO, a simple molecule, plays a significant role in a wide spectrum of plant responses to various abiotic stresses. With progress in the genomic and more recently proteomic access, it will be possible to define not only the NO-regulated genes but also downstream targets of nitric oxide. The identification of proteins as potential targets for nitration and S-nitrosylation in plants under various abiotic stresses will contribute to advances in the regulatory functions of NO in plants.

Acknowledgments

This work was supported by the Grant Agency of the Czech Republic, Grant No. P501/11/1239.

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