Abstract
Nitric oxide (·NO) and derived molecules, referred to as reactive nitrogen species (RNS), have become a new area of plant research. These molecules are involved in almost all physiological plant processes, ranging from seed germination, development, senescence, stomatal movement, fruit ripening, and reproduction to mechanisms of response to adverse environmental conditions possibly associated with nitro-oxidative stress. ·NO can perform a dual function depending on its rate of production; at low concentrations, it acts as a signal molecule and, at high concentrations, like a stress molecule. Although in some cases the simultaneous high ·NO production with other reactive oxygen species (ROS) can be useful to the cells as mechanism of defense, for example, against pathogens. All these processes are usually mediated by the chemical interactions of ·NO whose functions are affected by other molecules. It is worth pointing out that the post-translational modifications of target proteins caused by nitration and S-nitrosylation have been best described in plants. However, ·NO can also regulate gene expression through direct interaction with DNA or through interaction with transcription factors. This review provides a comprehensive overview of the role played by RNS in the physiology of plants and their involvement in the mechanism of response to a diverse range of adverse environmental conditions.
Access provided by CONRICYT-eBooks. Download chapter PDF
Similar content being viewed by others
Keywords
- Nitric Oxide
- Reactive Nitrogen Species
- Adverse Environmental Condition
- Lateral Root Formation
- Protein Nitration
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
1 Introduction
Endogenously generated nitric oxide (·NO) is currently one of the most studied bioactive gas molecules in plant cells. This is due to its involvement in a wide spectrum of plant physiological processes including seed germination, primary and lateral root growth, flowering, pollen tube growth regulation, stomatal movement, fruit ripening, and senescence; nevertheless, new functions of ·NO are gradually being added to the list. This key signaling molecule in different intracellular processes also participates in the mechanism of response to biotic and abiotic stresses (Neill et al. 2003; Lamotte et al. 2005; Besson-Bard et al. 2008; Corpas et al. 2011; Domingos et al. 2015; Corpas and Barroso 2015a). However, nitric oxide’s versatility depends on its chemical properties, enabling it to interact with many molecules that affect its biochemical interactions and consequently its functions in plant cells (Pfeiffer et al. 1999).
2 Nitric Oxide and Reactive Nitrogen Species
The gasotransmitter nitric oxide, also referred to as nitrogen monoxide, is a free radical whose π orbital contains an unpaired electron represented by a dot on the N atom (·NO); however, for simplification purposes, this dot is omitted in many publications. Nitric oxide has a family of NO-derived molecules generally referred to as reactive nitrogen species (RNS). Table 1 shows the most representative RNS including radical and non-radical molecules. Thus, ·NO can react with many inorganic and organic molecules such as peptides, proteins, lipids, and nucleotides; this reactivity explains its numerous biochemical interactions. Figure 1 shows a simple model of ·NO metabolism in plant cells. ·NO in both its gas phase and aqueous solution form can react with O2 to form dinitrogen trioxide (N2O3) and nitrogen dioxide (·NO2). In aqueous solution, N2O3 and ·NO2 produce stoichiometric amounts of nitrite (NO2 −) and nitrate (NO3 −). Nitrogen dioxide is 1.5 times more soluble in a lipid membrane than in water (Signorelli et al. 2011). ·NO is also able to react with the superoxide radical (O2 ·−) to yield peroxynitrite (ONOO−), with the rate constant (~ 1010 M−1 s−1) for this reaction being considerably very high (Estévez and Jordán 2002), virtually ensuring that ONOO− will be formed in any plant cell or tissue where both radicals are present simultaneously. This chemical reaction is very fast given a rate constant of 2 × 109 M−1 s−1 for O2 ·− dismutation by the CuZn superoxide dismutase (SOD) enzyme (Gray and Carmichael 1992). The production site of ONOO− must therefore be associated with the sources of O2 ·− and ·NO including the main plant cell organelles, such as chloroplasts, mitochondria, and peroxisomes (Blokhina and Fagerstedt 2010; Corpas and Barroso 2014). Peroxynitrite, a powerful oxidant, plays a highly important role as it can mediate nitration processes and cause cellular injury (Szabó et al. 2007; Corpas et al. 2009a; Arasimowicz-Jelonek and Floryszak-Wieczorek 2011; Calcerrada et al. 2011; Berton et al. 2012; Szuba et al. 2015).
Nevertheless, one of the most controversial issues with respect to higher plants is the way in which ·NO is endogenously generated in the cell. At least two main enzymatic pathways for generating endogenous ·NO, using the amino acid l-arginine and/or the nitrite-dependent pathway as well as non-enzymatic ·NO generation, have been described (Wojtaszek 2000). The involvement of at least one of these pathways in a specific process is supported by experimental data although it is important to note that, depending on the plant species, developmental stage, and/or environment conditions involved, the participation of both pathways cannot be ruled out. In the case of l-arginine-dependent nitric oxide synthase (NOS) activity, there is a strong biochemical evidence of the presence of this activity in plants, which requires the presence of all the co-factors of animal NOS using NADPH as an electron donor (see Corpas et al. 2009b); new data also confirm the existence of an NOS-like protein in the green alga Ostreococcus tauri (Foresi et al. 2010). Additionally, l-arginine is a precursor of the biosynthesis of polyamines which, according to some experimental data, could be involved in ·NO biosynthesis (Tun et al. 2006; Wimalasekera et al. 2011a, b). The production of ·NO by the nitrite-dependent pathway depends on nitrate reductase (NR) activity which uses NADH as an electron donor instead of NADPH. This classic enzyme is involved in the nitrogen metabolism and has been widely accepted as an ·NO source candidate (Yamasaki et al. 1999; Rockel et al. 2002; Lozano-Juste and Leon 2010).
As mentioned previously, ·NO directly or indirectly performs its biological actions through different RNS by interacting with many other molecules. In the case of proteins, the most studied post-translational modifications (PTMs) in plant cells are nitration and S-nitrosylation (Fig. 1). On the other hand, regulation of gene expression by ·NO has also been reported to produce specific transcriptional responses (Begara-Morales et al. 2014a), indicating that ·NO is perceived differentially. This could occur through the impact of ·NO on transcription factors or through direct interaction with the DNA (Serpa et al. 2007; Tavares et al. 2014).
3 Post-translational Modifications Mediated by RNS
3.1 Nitration
Nitration is a chemical reaction that enables a nitro group (-NO2) to be added to molecules including proteins, lipids, and nucleotide acids (Rubbo and Radi 2008). In proteins, some amino acids, such as tyrosine (Tyr), cysteine (Cys), methionine (Met), and tryptophan (Trp), are preferentially nitrated. However, in plants, most studies focus on tyrosine nitration (Tyr-NO2), which involves adding a nitro group to one of the two equivalent ortho-carbons of the aromatic ring of tyrosine residues. This transforms Tyr into a negatively charged hydrophilic Tyr-NO2 moiety and causes a marked shift in the hydroxyl group’s local pKa from 10.1 in tyrosine to 7.5 in nitrotyrosine. This process depends on different intrinsic and extrinsic features such as protein structure, nitration mechanism, and the environmental compartments where the targeted protein is located (Corpas et al. 2013). These covalent changes may result in several potential effects such as protein function loss, gain, or no functional change, with loss of function being the most common. It is important to remember that there is a physiological nitration in plant cells; however, under internal or external adverse conditions, an increase in protein nitration or free nitrotyrosine could be regarded as a reliable marker of nitrosative stress (Corpas et al. 2007; Berton et al. 2012). Many new potential target proteins, which undergo this PTM in plant cells under physiological or stress conditions, have been identified (Corpas et al. 2015). However, this process is closely associated with the ROS metabolism and consequently with oxidative stress, therefore it should be called nitro-oxidative stress (Corpas and Barroso 2013). A good example of this connection is the way in which important antioxidant enzymes, such as catalase (Clark et al. 2000; Chaki et al. 2015a), ascorbate peroxidase (Begara-Morales et al. 2014b), monodehydroascorbate reductase (Begara-Morales et al. 2015), and SOD (Holzmeister et al. 2015), are negatively regulated by nitration (see Table 2).
A new promising area of plant research is the identification and characterization of nitro-fatty acids (Sánchez-Calvo et al. 2013). These molecules together with their signaling component have been under intense study in animal cells; they can trigger signaling cascades via covalent and reversible PTMs of susceptible nucleophilic amino acids in target proteins which have important physiological functions such as an anti-inflammatory mechanism (Trostchansky et al. 2013). However, there are very few experimental data on this area of research in plants (Fazzari et al. 2014).
3.2 S-Nitrosylation
S-Nitrosylation, more appropriately called S-nitrosation, consists of the covalent attachment of an ·NO group to the thiol (-SH) side chain of cysteine (Cys) present in peptides or proteins in order to produce a family of NO-derived molecules called S-nitrosothiols (SNOs). This covalent modification is highly labile under physiological conditions as their stability depends on the presence of trace metal ions (such as copper and iron) or reducing agents (such as thiols and ascorbate) which enhance their degradation (Askew et al. 1995; Vanin et al. 1997), thus making it difficult to study SNOs in cells. Furthermore, this process, which is selective and reversible, can alter protein conformation and/or protein properties. Different biochemical approaches such as biotin switch assays, resin-assisted capture (SNO-RAC), fluorescence switch, or protein microarray-based analysis (Jaffrey 2005; Han et al. 2008; Foster et al. 2009; Wang and Xian 2011; Fares et al. 2014) combined with mass spectrometry techniques have facilitated the study of SNO modulation and identification of a significant number of potential protein targets in different plant species under physiological and stress conditions (Lindermayr et al. 2005; Vanzo et al. 2014; Chaki et al. 2015b).
4 Nitric Oxide in Plant Development
Plant development involves many phases including seed germination, plant growth and differentiation of cells, tissues, and organs, flower formation, fruit ripening, and senescence. In all these processes, the direct involvement of ·NO or indirectly through its interaction with different phytohormones (auxins, ethylene, and abscisic acids) and molecules such as ROS (superoxide radical, H2O2) has been described to some degree (Zhao 2007; Freschi 2013; Airaki et al. 2015; Corpas and Barroso 2015b; Sanz et al. 2015).
Many metabolic pathways are involved in seed germination and seedling establishment which begin with water imbibition, a catabolic and anabolic process using lipid mobilization to support the development of the new seedling during the transition from dark to light conditions until the seedling can initiate photosynthesis. ·NO acts as a stimulator of germination and photo-morphogenesis (Beligni and Lamattina 2000; Kopyra and Gwózdz 2003; Simontacchi et al. 2004; Gniazdowska et al. 2010). Moreover, an increasing amount of data shows that ·NO interacts with other molecules including calcium, H2O2, auxin, and gibberellins in the regulation of primary and lateral root growth, which eventually determines root architecture (Pagnussat et al. 2002; Correa-Aragunde et al. 2004; Guo et al. 2008; Fernández-Marcos et al. 2011; Duan et al. 2014; Sanz et al. 2015). During seedling development in different plant species such as pea, Arabidopsis, and pepper, cellular analyses employing specific NO-sensitive fluorophores and confocal laser scanning microscopy (CLSM) reveal that the steady-state levels of ·NO content change depending on cell type in the main organs including roots, stems, and leaves (Corpas et al. 2006, 2009a; Airaki et al. 2015). Furthermore, in some cases, a temporal correlation between organ development and ·NO production from l-arginine-dependent NOS activity has been described (Corpas et al. 2004, 2006). In addition, in the presence of other NO-derived molecules such as S-nitrosoglutathione and peroxynitrite, protein nitration has also been reported to be modulated during organ development (Airaki et al. 2015; Begara-Morales et al. 2013), indicating that these organs have a highly active ·NO metabolism.
The enzyme nitrosoglutathione reductase (GSNOR) is a conserved protein in prokaryotes and eukaryotes which catalyzes the NADH-dependent reduction of GSNO to GSSG and NH3 regulating the level of GSNO and consequently cellular SNO homeostasis (Sakamoto et al. 2002; Leterrier et al. 2011). This activity is necessary for normal development under optimal growth conditions (Lee et al. 2008; Kubienová et al. 2013; Xu et al. 2013). Analysis of GSNOR in Arabidopsis thaliana indicates that roots and leaves from the initial stages of development have higher activity levels (Espunya et al. 2006). The importance of GSNOR in plant development has also been demonstrated by genetic approaches, as the over-expressing and knock-down GSNOR gene in Arabidopsis plants show an atypical phenotype with a short-root system, which correlates with a lowering of intracellular GSH levels and an alteration in its spatial distribution in the roots (Lee et al. 2008; Chen et al. 2009; Leterrier et al. 2011; Kwon et al. 2012). Moreover, new experimental data have begun to elucidate the molecular mechanism involved in the relationship between ·NO and auxin, a phytohormone that regulates growth and development processes such as lateral root formation, cell division, and elongation, as ·NO has the capacity to inhibit auxin transport through a mechanism of S-nitrosylation (Fernández-Marcos et al. 2011; Terrile et al. 2012; Shi et al. 2015).
·NO is also involved in the final development processes of senescence and fruit ripening. In senescent pea plants, ·NO content is down-regulated in leaves, which closely correlates with the lower l-arginine-dependent NOS activity detected as compared to that determined in the leaves of young plants (Corpas et al. 2004). However, a similar analysis in the root systems of both young and senescent plants reveals a different behavior, characterized by increased ·NO and ONOO− content and protein nitration (Begara-Morales et al. 2013), suggesting some kind of specificity in the function of ·NO and related molecules depending on the analyzed organ and stage of development, as was mentioned previously.
Nitric oxide is also involved in reproductive organs and has the capacity to repress floral transition in Arabidopsis thaliana by inhibiting CONSTANS and GIGANTEA gene expression (He et al. 2004) which promotes flowering and regulates photoperiodic flowering, respectively. The rate and orientation of pollen tube growth is regulated by the level of ·NO at the pollen tube tip which appears to be mediated by cGMP (Prado et al. 2004). On the other hand, ·NO is involved in pollen–pistil interactions, in which ·NO appears to influence the targeting of pollen tubes to the ovule’s micropyle by modulating the action of its diffusible factors (McInnis et al. 2006; Prado et al. 2008). Analysis carried out during olive flower development shows that ·NO content is also modulated depending on the developmental stage and tissue, with an increase in ·NO production in pollen grains and tubes observed during the receptive phase in the stigma (Zafra et al. 2010).
Fruit ripening is another complex process that is regulated by ethylene production which is characterized by increased ROS production. ·NO has also been shown to interact with ethylene and the ROS metabolism (Leshem and Pinchasov 2000; Manjunatha et al. 2010). During pepper fruit ripening, apart from the more apparent change in color from green to red, there are also significant biochemical adjustments. Thus, analysis of ·NO metabolism using proteomic approaches shows that, during ripening, the nitration of proteins such as catalase, NADP-dependent glyceraldehyde-3-phosphate dehydrogenase, a transketolase 1, a 20S proteasome alpha 6 subunit, or ferredoxin-dependent glutamate synthase 1 involved in redox, oxidative, protein, and carbohydrate metabolisms changes, with the antioxidant catalase being among the most affected. However, it has been shown that the application of exogenous ·NO gas can prevent protein nitration and delay fruit ripening (Chaki et al. 2015a).
5 Nitro-Oxidative Stress Under Abiotic Conditions
Adverse environmental conditions including drought, salinity, soil mineral toxicity, cold, and heat can limit agricultural production considerably. It has been well established that all these abiotic stresses may lead to oxidative stress characterized by uncontrollable overproduction of ROS that generates molecular damage in lipids, proteins, and nucleic acid. With the discovery of ·NO and NO-derived molecules, many researchers set out to show that these adverse conditions are also associated with nitrosative stress (Valderrama et al. 2007; Corpas et al. 2008, 2011). Thus, it has been proposed that an increase in protein nitration could be a reliable biomarker of a specific stress similar to protein oxidation which is a marker of oxidative stress (Corpas et al. 2007; Arasimowicz-Jelonek and Floryszak-Wieczorek 2011). However, given the metabolic interplay between these two families of molecules (ROS and RNS) in which many enzymes involved in ROS metabolism are targets of PTMs mediated by ·NO (see Table 2), nitro-oxidative stress would be a more appropriate term (Corpas et al. 2013).
5.1 Heavy Metals
Contamination by heavy metals such as cadmium, arsenic, lead, or mercury is an increasingly serious problem for the environment and consequently for agriculture and human health (World Health Organization 2007; Hernández et al. 2015). Although it has been well established that heavy metals usually trigger an oxidative stress response, recent analysis of the plant ·NO metabolism has demonstrated that they also induce nitro-oxidative stress.
Arsenic (As) is a metalloid naturally present in the environment, with arsenate (AsV) being the main arsenic species in aerobic soils and arsenite (AsIII) in soils under anaerobic and reducing conditions. In higher plants, inorganic arsenic can be accumulated in the form of arsenite (AsIII) throughout nodulin 26-like intrinsic (NIP) aquaporin channels or in the form of arsenate (AsV) throughout the phosphate transporter system (Zhao et al. 2010). Various studies have demonstrated that arsenic triggers nitro-oxidative stress. For example, Arabidopsis thaliana seedlings exposed to 500 μM AsV trigger a significant increase in ·NO content, GSNOR activity, and protein tyrosine nitration as well as a concomitant decrease in glutathione and GSNO content (Leterrier et al. 2012). Curiously, the exogenous application of ·NO can alleviate arsenic-induced oxidative stress in different plant species by enhancing antioxidant defenses (Singh et al. 2009, 2013; Hasanuzzaman and Fujita 2013), thus corroborating the aforementioned cross talk between the families of ROS and RNS molecules.
Cadmium toxicity in plants is well established (Chmielowska-Bąk et al. 2014) and generally causes an augmentation of ROS production and consequently oxidative stress (Dixit et al. 2001). In addition, the ·NO metabolism is differentially affected under cadmium stress. In pea, 50 μM CdCl2 provoked a lower GSNOR activity with a decrease in ·NO and GSNO content but accompanied with a rise of ROS production and an increase in salicylic acid, jasmonic acid, and ethylene (Barroso et al. 2006; Rodríguez-Serrano et al. 2006), indicating the presence of nitro-oxidative stress where ·NO plays an essential role as a signaling molecule (Arasimowicz-Jelonek et al. 2011) and participates in homeostasis in order to maintain the metabolic equilibrium in the presence of cadmium (Gill et al. 2013; Liu et al. 2015). In Arabidopsis thaliana, cadmium induces ·NO generation from NOS activity, which contributes to the inhibition of root growth partly caused by iron deprivation (Besson-Bard et al. 2009; Han et al. 2014). At the subcellular level, Cd stress in Arabidopsis has recently been shown to trigger the production of both O2 ·− and ·NO in peroxisomes with a concomitant generation of ONOO−, thus corroborating reports that these organelles participate in the mechanism of response to this metal (Corpas and Barroso 2014).
5.2 Salinity
Over 6 % of the world’s land mass has been estimated to be affected by either salinity or sodicity which negatively affect plant productivity by inhibiting plant growth, ion balance, and water relations (Hasegawa et al. 2000). As mentioned previously, salinity is commonly accompanied by oxidative stress, with an increasing number of studies pointing to the involvement of RNS in these processes (Valderrama et al. 2007; Molassiotis et al. 2010). Although its effects may vary somewhat depending on the plant species and the severity of the salinity treatment, salinity generally triggers the ·NO metabolism, which has been observed to cause an increase in ·NO production and the number of S-nitrosylated and nitrated proteins as well as a modulation in redox homeostasis and the antioxidant system (Valderrama et al. 2007; Tanou et al. 2009b, 2012; Manai et al. 2014a). Some studies have also demonstrated that ·NO appears to modulate and enhance the expression of Na+/H+ antiporter genes under high salinity conditions which contributes to mitigating the negative effects of sodium (Zhang et al. 2006; Lu et al. 2013; Chen et al. 2013). Proteomic approaches have also identified a significant number of proteins affected by S-nitrosylation and nitration (Tanou et al. 2009a). Data on the ·NO metabolism under salinity stress by the application of exogenous ·NO appear to provide a certain level of resistance to salinity stress. Thus, in 5-month-old bitter orange (Citrus aurantium) trees, pretreatment of the root system with 100 μM sodium nitroprusside (SNP; a ·NO donor) induces considerable antioxidant resistance in the form of catalase, SOD, ascorbate peroxidase, and glutathione reductase (Tanou et al. 2009a, b). Similarly, tomato (Solanum lycopersicum) plants exposed simultaneously to 120 mM NaCl and a ·NO donor (100 μM or 300 μM SNP) through their root system show a decrease in NaCl-induced lipid oxidation in leaves, which was accompanied by an increase in the antioxidant system’s SOD, APX, GR, and POD activities in roots and leaves and also increased ascorbate and proline content. It is also worth noting that a newly CuZnSOD is induced in roots, suggesting that the ·NO performs a regulatory function at the protein and gene levels of this antioxidant enzyme (Manai et al. 2014b). Tomato plants have also shown an increase in the activity of some enzymes such as nitrate reductase (NR) and nitrite reductase (NiR) involved in the nitrogen metabolism. On the other hand, genetic approaches using overexpression of rat neuronal NOS (nNOS) in rice show increases in both NOS activity and ·NO accumulation, resulting in improved tolerance of transgenic rice to salt and drought stresses (Cai et al. 2015).
5.3 Drought or Water Stress
Drought affects plants at many levels, ranging from the morphological to the molecular one. The visual symptoms of drought stress include the reduction of shoots (leaves and stem) and root proliferation which disturbs plant–water relations and reduces water-use efficiency. At the biochemical level, drought stress disturbs the balance between ROS production and antioxidant defenses, thus causing oxidative stress. As with other types of stress, ·NO plays a prominent role in response mechanisms (Santisree et al. 2015). For example, in the legume Lotus japonicus exposed to water stress, the spatial distribution of nitro-oxidative stress has been described; oxidative stress levels increased in leaves while nitrosative stress levels were higher in roots in which ·NO content increased whereas GSNO reductase activity diminished, which may explain the rise in protein tyrosine nitration (Signorelli et al. 2013). On the other hand, in white clover (Trifolium repens), ·NO mediates drought tolerance through the activation of antioxidant enzymes such as SOD, APX, and catalase (Peng et al. 2015).
Abscisic acid (ABA), defined as a stress plant hormone due to its rapid accumulation in response to water stress, plays a major role in the regulation of plant growth, development, and tolerance under stress conditions. Under water deficiency conditions, plants use a stomatal closure strategy. The movement of guard cells is highly regulated, involving molecules such as ABA, H2O2, NO, and NADPH (Neill et al. 2008; Gayatri et al. 2013; Leterrier et al. 2016). ·NO is known to induce stomatal closure, although the interplay between the different players is complex. A recent in vitro analysis has demonstrated that ABA receptors are targeted by tyrosine nitration which reduces receptor activity (Castillo et al. 2015). Therefore, under stress conditions, the production of both ·NO and superoxide together with a concomitant generation of ONOO− could explain how ·NO limits ABA signaling through nitration. On the other hand, ·NO negatively regulates ABA signaling in guard cells by inhibiting open stomata 1 (OST1)/sucrose nonfermenting 1 (SNF1)-related protein kinase 2.6 (SnRK2.6) through S-nitrosylation, specifically in the Cys137 (Wang et al. 2015).
5.4 Low and High Temperature
Extreme temperatures are environmental stresses that affect crop production and quality, involving the expression of many genes as well as significant numbers of proteins and metabolites. New data have shown that ·NO metabolism is affected at different levels depending on the plant species or temperature intensity among other factors (Corpas et al. 2008; Piterková et al. 2013; Puyaubert and Baudouin 2014; Sehrawat and Deswal 2014).
For example, pepper plants exposed to low temperature (LT) for several days undergo significant changes in the metabolism of RNS and ROS together with an increase in both protein tyrosine nitration (NO2-Tyr) and lipid peroxidation, indicating that LT induces nitro-oxidative stress (Airaki et al. 2012). In Medicago sativa under cold stress, the interaction of ·NO, H2O2, and ABA mediates the induction of the S-adenosylmethionine synthetase (SAMS), an enzyme that catalyzes the formation of S-adenosylmethionine (SAM), a precursor of polyamines and ethylene, which is involved in cold tolerance (Guo et al. 2014). The C-repeat binding factor (CBF) is one of the most studied cold stress-signaling pathways in plants. Recently, tomato seedlings under LT stress have been shown to undergo dual regulation of the CBF by ·NO at the transcriptional and translational level through S-nitrosylation (Kashyap et al. 2015). Furthermore, in poplar tree, the existence of a feedback mechanism between GSNOR activity and protein S-nitrosylation has been shown which is regulated in response to cold stress (Cheng et al. 2015).
On the other hand, sunflower seedlings exposed to high temperature (HT) experience oxidative stress; this impairs the ·NO metabolism by lowering ·NO content and reducing GSNOR activity and gene expression with a concomitant accumulation of total SNOs including GSNO as well as peroxynitrite formation and increased protein nitration; ferredoxin–NADP reductase is one of these inhibited nitrated proteins that affect photosynthesis (Chaki et al. 2011). The identification and characterization of the GSNOR knock-out mutant in Arabidopsis through the use of genetic techniques demonstrate the involvement of this important gene under physiological and stress conditions including HT. For example, analysis of the mutant HOT5 (sensitive to hot temperatures) shows that GSNOR modulates the intracellular level of SNOs, resulting in thermotolerance as well as regulation of plant growth and development (Lee et al. 2008). Similarly, the mutant paraquat resistant 2 (PAR2) which encodes a GSNOR has a higher level of ·NO, shows an anti-cell death phenotype (Chen et al. 2009; Xu et al. 2013).
6 Nitric Oxide in Plant–Pathogen Interactions
Systemic acquired resistance (SAR) is a cellular mechanism of disease resistance that is induced in response to initial infection and that protects uninfected areas of the plant against potential secondary infections by related or unrelated pathogens. In this process, the RNS and ROS families of molecules interact with each other to provide an adequate response to different pathogen organisms including bacteria, fungi, nematodes, and insects (Prats et al. 2005; Chaki et al. 2009; Wünsche et al. 2011; Scheler et al. 2013; Wendehenne et al. 2014; Zhou et al. 2015).
As a model plant, Arabidopsis thaliana has been extensively used to study the many ways in which ·NO and derived molecules are involved in plant–pathogen interactions (Yu et al. 2012; Chen et al. 2014; Kovacs et al. 2015). This plant’s available genomic database information combined with the use of proteomic techniques have facilitated the identification of the protein targets of S-nitrosylation (Romero-Puertas et al. 2008; Chaki et al. 2015b) and nitration (Cecconi et al. 2009) during pathogen infection. This information has enabled researchers to gain a deeper understanding of the ·NO metabolism in this type of interaction. For example, it has been well established that plants use oxidative burst to respond to pathogen attacks, in this case, membrane-bound NADPH oxidase (NOX), also called the respiratory burst oxidase homologue (RBOH), a key element in the generation of O2 −·. Interestingly, S-nitrosylation of AtRBOH type D at Cys890 has been shown to abolish its ability to synthesize O2 ·− (Yun et al. 2011). However, there is complementary information on other plant species. For example, the infection of a susceptible cultivar of sunflower seedlings with the fungus Plasmopara halstedii, causing downy mildew, has been observed to increase protein nitration accompanied by an augmentation in SNOs; however, in the resistant sunflower cultivar, with its higher SNO content, a redistribution of these SNOs in the penetration site has been observed in the presence of the pathogen, which prevents the spread of infection (Chaki et al. 2009), thus confirming the importance of SNOs under this type of biotic stress. On the other hand, in tobacco cells exposed to the fungal elicitin cryptogein, analysis of S-nitrosylated proteins has identified 11 candidates for S-nitrosylation including the cell division cycle 48 (CDC48) protein, a member of the AAA+ ATPase family that mediates resistance to certain pathogens. However, S-nitrosylation abolishes NtCDC48 ATPase activity (Astier et al. 2012). In tobacco cells exposed to cryptogein, ·NO has also been observed to require NtRBOHD activity to induce cell death (Kulik et al. 2015).
7 Nitric Oxide in Plant Beneficial Interactions
Plants can also establish specific and beneficial interactions with other organisms, in which ·NO and other elements have been found to act as signal molecules. In this context, the most studied interaction is the symbiosis between Legume–Rhizobium, characterized by the formation of differentiated organs called nodules, where ·NO is required for the optimal establishment of the symbiotic interaction (Meilhoc et al. 2011; del Giudice et al. 2011; Hichri et al. 2015). Root nodules, enabling atmospheric N2 to be fixed to ammonia, have two critical elements: leghemoglobin (Lb) and nitrogenase. Lb is an oxygen carrier whose function is to prevent the presence of O2 which reduces the activity of oxygen-sensitive nitrogenase, the enzyme responsible for fixing atmospheric nitrogen to ammonia. Interestingly, nitrogenase activity is inhibited by ·NO, indicating that ·NO levels in rhizobia are a determining factor in efficient symbiotic processes (Cabrera et al. 2011). A rise in ROS and RNS has also been observed in senescent nodules which cause nitro-oxidative stress, leading to a reduction in the ability of symbiotic leghemoglobins to scavenge oxygen due to the modifications mediated by these ROS/RNS (Sainz et al. 2013). However, the formation of nitrated leghemoglobins during normal metabolism has been detected in functional nodules which, it has been suggested, may act as a sink for toxic peroxynitrite to protect nodule functionality (Sainz et al. 2015).
Another group of bacteria, Azospirillum brasilense, has the capacity to produce ·NO from ammonia. When this bacterium interacts with tomato roots, the ·NO produced stimulates lateral root formation (Creus et al. 2005; Molina-Favero et al. 2008). ·NO is also generated in other interactions such as those between plant roots and arbuscular mycorrhizal fungi where ·NO is produced in the roots of Medicago truncatula when they come in contact with the exudates of the fungus Gigaspora margarita (Calcagno et al. 2012).
8 Conclusions and Future Perspectives
Since it was discovered that ·NO could be endogenously produced in plant cells, the number of biochemical and physiological actions found to be mediated by this free radical has increased continually (Corpas and Barroso 2015a). It is now well established that ·NO is responsible for a wide spectrum of actions which are based on a complex network of biochemical interactions with a diverse range of molecules, both small and large, such as metals, superoxide radicals, glutathione, proteins, lipids, and nucleic acid, that affect its structure and functions. In this context, although certain authors have begun to regard ·NO as a “new phytohormone,” some important issues still need to be addressed by the scientific community. For example, it is necessary to determine how and where ·NO is produced in specific processes and also to identify the molecules which are targets under physiological and stress conditions, with nitro-fatty acids being a good example of these. A major effort is therefore being made to determine the way in which ·NO can be sensed in order to control the concentrations of RNS. On the other hand, research into the beneficial effects of applying exogenous ·NO to treat plants against certain environmental stresses has been increasing. In fact, many studies have shown that exogenous ·NO can ameliorate oxidative damage caused by stress by activating a diverse range of antioxidant systems and can even modulate physiological processes such as senescence and fruit ripening which are good examples of the biotechnological applications of ·NO. Nevertheless, it is important to keep in mind than production levels of ·NO into cells may determine its physiological function because when it is produced at low level, NO could have signaling functions but when it is overproduced it may have toxic effects.
References
Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295
Airaki M, Leterrier M, Valderrama R, Chaki M, Begara-Morales JC, Barroso JB, del Río LA, Palma JM, Corpas FJ (2015) Spatial and temporal regulation of the metabolism of reactive oxygen and nitrogen species during the early development of pepper (Capsicum annuum) seedlings. Ann Bot 116:679–693
Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2011) Understanding the fate of peroxynitrite in plant cells--from physiology to pathophysiology. Phytochemistry 72:681–688
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620
Askew SC, Barnett DJ, McAninly J, Williams DLH (1995) Catalysis by Cu2+ of nitric oxide release from S-nitrosothiols (RSNO). J Chem Soc Perkin Trans 2:741–745
Astier J, Besson-Bard A, Lamotte O, Bertoldo J, Bourque S, Terenzi H, Wendehenne D (2012) Nitric oxide inhibits the ATPase activity of the chaperone-like AAA+ ATPase CDC48, a target for S-nitrosylation in cryptogein signalling in tobacco cells. Biochem J 447:249–260
Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793
Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64:1121–1134
Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014a) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014b) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996
Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221
Berton P, Domínguez-Romero JC, Wuilloud RG, Sánchez-Calvo B, Chaki M, Carreras A, Valderrama R, Begara-Morales JC, Corpas FJ, Barroso JB, Gilbert-López B, García-Reyes JF, Molina-Díaz A (2012) Determination of nitrotyrosine in Arabidopsis thaliana cell cultures with a mixed-mode solid-phase extraction cleanup followed by liquid chromatography time-of-flight mass spectrometry. Anal Bioanal Chem 404:1495–1503
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39
Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315
Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462
Cabrera JJ, Sánchez C, Gates AJ, Bedmar EJ, Mesa S, Richardson DJ, Delgado MJ (2011) The nitric oxide response in plant-associated endosymbiotic bacteria. Biochem Soc Trans 39:1880–1885
Cai W, Liu W, Wang WS, Fu ZW, Han TT, Lu YT (2015) Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS One 10(6), e0131599
Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L (2012) The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots. Mycorrhiza 22:259–269
Calcerrada P, Peluffo G, Radi R (2011) Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr Pharm Des 17:3905–3932
Camejo D, Jiménez A, Palma JM, Sevilla F (2015) Proteomic identification of mitochondrial carbonylated proteins in two maturation stages of pepper fruits. Proteomics 15:2634–2642
Castillo MC, Lozano-Juste J, González-Guzmán M, Rodriguez L, Rodriguez PL, León J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8(392):ra89.
Cecconi D, Orzetti S, Vandelle E, Rinalducci S, Zolla L, Delledonne M (2009) Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis 30:2460–2468
Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol 50:265–279
Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ 34:1803–1818
Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015a) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116:637–647
Chaki M, Shekariesfahlan A, Ageeva A, Mengel A, von Toerne C, Durner J, Lindermayr C (2015b) Identification of nuclear target proteins for S-nitrosylation in pathogen-treated Arabidopsis thaliana cell cultures. Plant Sci 238:115–126
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J, Zuo J (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387
Chen J, Xiong DY, Wang WH, Hu WJ, Simon M, Xiao Q, Chen J, Liu TW, Liu X, Zheng HL (2013) Nitric oxide mediates root K+/Na + balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+ antiporter under high salinity. PLoS One 8(8), e71543
Chen J, Vandelle E, Bellin D, Delledonne M (2014) Detection and function of nitric oxide during the hypersensitive response in Arabidopsis thaliana: where there’s a will there’s a way. Nitric Oxide 43:81–88
Cheng T, Chen J, Allah EFA, Wang P, Wang G, Hu X, Shi J (2015) Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress. Planta 242:1361–1390
Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245
Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384
Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199:633–635
Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO-) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96
Corpas FJ, Barroso JB (2015a) Nitric oxide from a green perspective. Nitric Oxide 45:15–19
Corpas FJ, Barroso JB (2015b) Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants 4:240–252
Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733
Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254
Corpas FJ, del Río LA, Barroso JB (2007) Need of biomarkers of nitrosative stress in plants. Trends Plant Sci 12:436–438
Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722
Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009a) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2894
Corpas FJ, Palma JM, del Río LA, Barroso JB (2009b) Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14
Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611
Corpas FJ, Palma JM, del Río LA, Barroso JB (2013) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 4:29
Corpas FJ, Begara-Morales JC, Sánchez-Calvo B, Chaki C, Barroso JB (2015) Nitration and S-nitrosylation: two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) and their role in signalling processes of plant cells. In: KJ Gupta, AU Igamberdiev (eds) Reactive oxygen and nitrogen species signaling and communication in plants, signaling and communication in plants, vol 23. Springer International Publishing, Switzerland, pp 267–281. ISBN: 978-3-319-10078-4
Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905
Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303
del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405–417
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520
Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y (2014) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotoxicol Environ Saf 113C:95–102
Espunya MC, Diaz M, Moreno-Romero J, Martinez MC (2006) Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. Plant Cell Environ 29:1002–1011
Estévez AG, Jordán J (2002) Nitric oxide and superoxide, a deadly cocktail. Ann N Y Acad Sci 962:207–211
Fares A, Nespoulous C, Rossignol M, Peltier JB (2014) Simultaneous identification and quantification of nitrosylation sites by combination of biotin switch and ICAT labeling. Methods Mol Biol 1072:609–620
Fazzari M, Trostchansky A, Schopfer FJ, Salvatore SR, Sánchez-Calvo B, Vitturi D, Valderrama R, Barroso JB, Radi R, Freeman BA, Rubbo H (2014) Olives and olive oil are sources of electrophilic fatty acid nitroalkenes. PLoS One 9(1), e84884
Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PINFORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci U S A 108:18506–18511
Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830
Foster MW, Forrester MT, Stamler JS (2009) A protein microarray-based analysis of S-nitrosylation. Proc Natl Acad Sci U S A 106:18948–18953
Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398
Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci 4:425
Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261
Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R (2010) The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta 232:999–1005
Gray B, Carmichael AJ (1992) Kinetics of superoxide scavenging by dismutase enzymes and manganese mimics determined by electron spin resonance. Biochem J 281:795–802
Guo K, Xia K, Yang Z-M (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452
Guo Z, Tan J, Zhuo C, Wang C, Xiang B, Wang Z (2014) Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. falcata that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnol J 12:601–612
Han P, Zhou X, Huang B, Zhang X, Chen C (2008) On-gel fluorescent visualization and the site identification of S-nitrosylated proteins. Anal Biochem 377:150–155
Han B, Yang Z, Xie Y, Nie L, Cui J, Shen W (2014) Arabidopsis HY1 confers cadmium tolerance by decreasing nitric oxide production and improving iron homeostasis. Mol Plant 7:388–403
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911
Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887
Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999
Jaffrey SR (2005) Detection and characterization of protein nitrosothiols. Methods Enzymol 396:105–118
Kashyap P, Sehrawat A, Deswal R (2015) Nitric oxide modulates Lycopersicon esculentum C-repeat binding factor 1 (LeCBF1) transcriptionally as well as post-translationally by nitrosylation. Plant Physiol Biochem 96:115–123
Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plantarum 148:371–386
Kopyra M, Gwózdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017
Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. 208:860–872
Kubienová L, Kopečný D, Tylichová M, Briozzo P, Skopalová J, Šebela M, Navrátil M, Tâche R, Luhová L, Barroso JB, Petřivalský M (2013) Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95:889–902
Kulik A, Noirot E, Grandperret V, Bourque S, Fromentin J, Salloignon P, Truntzer C, Dobrowolska G, Simon-Plas F, Wendehenne D (2015) Interplays between nitric oxide and reactive oxygen species in cryptogein signalling. Plant Cell Environ 38:331–348
Kwon E, Feechan A, Yun BW, Hwang BH, Pallas JA, Kang JG, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236:887–900
Lamotte O, Courtois C, Barnavon L, Pugin A, Wendehenne D (2005) Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta 221:1–4
Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20:786–802
Leshem YY, Pinchasov Y (2000) Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria ananassa (Dutch.) and avocados Persea americana (Mill.). J Exp Bot 51:1471–1473
Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso JB, Corpas FJ (2011) Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal Behav 6:789–793
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143
Leterrier M, Barroso JB, Valderrama R, Begara-Morales JC, Sánchez-Calvo B, Chaki M, Luque F, Viñegla B, Palma JM, Corpas FJ (2016) Peroxisomal NADP-isocitrate dehydrogenase is required for Arabidopsis stomatal movement. Protoplasma. 253:403–415
Lindermayr C, Saalbac G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
Liu S, Yang R, Pan Y, Ma M, Pan J, Zhao Y, Cheng Q, Wu M, Wang M, Zhang L (2015) Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol Environ Saf 119:35–46
Lozano-Juste J, Leon J (2010) Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol 152:891–903
Lu Y, Li N, Sun J, Hou P, Jing X, Zhu H, Deng S, Han Y, Huang X, Ma X, Zhao N, Zhang Y, Shen X, Chen S (2013) Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol 33:81–95
Manai J, Gouia H, Corpas FJ (2014a) Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J Plant Physiol 171:1028–1035
Manai J, Kalai T, Gouia H, Corpas FJ (2014b) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14:433–446
Manjunatha G, Lokesh V, Neelwarne B (2010) Nitric oxide in fruit ripening: trends and opportunities. Biotechnol Adv 28:489–499
McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol 172:221–228
Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R (2011) Nitric oxide in Legume-Rhizobium symbiosis. Plant Sci 181:573–581
Molassiotis A, Tanou G, Diamantidis G (2010) NO says more than ‘YES’ to salt tolerance: salt priming and systemic nitric oxide signaling in plants. Plant Signal Behav 5:209–212
Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant Microbe Interact 21:1001–1009
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176
Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y, He X, Zhang X, Ma X, Huang L, Yan Y (2015) NO is involved in spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes. Protoplasma. doi:10.1007/s00709-015-0880-8
Pfeiffer S, Mayer B, Hemmens B (1999) Nitric oxide: chemical puzzles posed by a biological messenger. Angew Chem Int Ed 38:1714–1731
Piterková J, Luhová L, Mieslerová B, Lebeda A, Petřivalský M (2013) Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Sci 207:57–65
Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714
Prado AM, Colaço R, Moreno N, Silva AC, Feijó JA (2008) Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 1:703–714
Prats E, Mur LA, Sanderson R, Carver TL (2005) Nitric oxide contributes both to papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp. hordei. Mol Plant Pathol 6:65–78
Puyaubert J, Baudouin E (2014) New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ 37:2623–2630
Rockel P, Strube F, Rockel AJ, Wildt JWM, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110
Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544
Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130
Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469
Rubbo H, Radi R (2008) Protein and lipid nitration: role in redox signaling and injury. Biochim Biophys Acta 1780:1318–1324
Sainz M, Pérez-Rontomé C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M (2013) Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. Plant J 76:875–887
Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M (2015) Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J 81:723–735
Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24
Sánchez-Calvo B, Barroso JB, Corpas FJ (2013) Hypothesis: nitro-fatty acids play a role in plant metabolism. Plant Sci 199–200:1–6
Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci 239:44–55
Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868
Scheler C, Durner J, Astier J (2013) Nitric oxide and reactive oxygen species in plant biotic interactions. Curr Opin Plant Biol 16:534–539
Sehrawat A, Deswal R (2014) S-nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signalling. J Proteome Res 13:2599–25619
Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Biophys Res Commun 361:1048–1053
Shi YF, Wang DL, Wang C, Culler AH, Kreiser MA, Suresh J, Cohen JD, Pan J, Baker B, Liu JZ (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8:1350–1365
Signorelli S, Möller MN, Coitiño EL, Denicola A (2011) Nitrogen dioxide solubility and permeation in lipid membranes. Arch Biochem Biophys 512:190–196
Signorelli S, Corpas FJ, Borsani O, Barroso JB, Monza J (2013) Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Sci 201–202:137–146
Simontacchi M, Jasid S, Puntarulo S (2004) Nitric oxide generation during early germination of Sorghum seeds. Plant Sci 167:839–847
Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297
Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiol Biochem 71:155–163
Szabó C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6:662–680
Szuba A, Kasprowicz-Maluśki A, Wojtaszek P (2015) Nitration of plant apoplastic proteins from cell suspension cultures. J Proteomics 120:158–168
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009a) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804
Tanou G, Molassiotis A, Diamantidis G (2009b) Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913
Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599
Tavares CP, Vernal J, Delena RA, Lamattina L, Cassia R, Terenzi H (2014) S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana. Biochim Biophys Acta 1844:810–817
Terrile MC, París R, Calderón-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500
Trostchansky A, Bonilla L, González-Perilli L, Rubbo H (2013) Nitro-fatty acids: formation, redox signaling, and therapeutic potential. Antioxid Redox Signal 19:1257–1265
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, Del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461
Vanin AF, Malenkova IV, Serezhenkov VA (1997) Iron catalyzes both decomposition and synthesis of S-nitrosothiols: optical and electron paramagnetic resonance studies. Nitric Oxide 1:191–203
Vanzo E, Ghirardo A, Merl-Pham J, Lindermayr C, Heller W, Hauck SM, Durner J, Schnitzler JP (2014) S-nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS One 9(9), e106886
Wang H, Xian M (2011) Chemical methods to detect S-nitrosation. Curr Opin Chem Biol 15:32–37
Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618
Wendehenne D, Gao QM, Kachroo A, Kachroo P (2014) Free radical-mediated systemic immunity in plants. Curr Opin Plant Biol 20:127–134
Wimalasekera R, Tebartz F, Scherer GFE (2011a) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603
Wimalasekera R, Villar C, Begum T, Scherer GF (2011b) COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678
Wojtaszek P (2000) Nitric oxide in plants. To NO or not to NO. Phytochemistry 54:1–4
World Health Organization (2007) Health risks of heavy metals from long-range transboundary air pollution, p 130. Germany, ISBN: 978 92 890 7179 6
Wünsche H, Baldwin IT, Wu J (2011) S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J Exp Bot 62:4605–4616
Xu S, Guerra D, Lee U, Vierling E (2013) S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front Plant Sci 4:430
Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129
Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615
Yu M, Yun BW, Spoel SH, Loake GJ (2012) A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. Curr Opin Plant Biol 15:424–430
Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268
Zafra A, Rodríguez-García MI, Alché JD (2010) Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol 10:36
Zhang YY, Wang LL, Liu YL, Zhang Q, Wei QP, Zhang WH (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555
Zhao J (2007) Interplay among nitric oxide and reactive oxygen species: a complex network determining cell survival or death. Plant Signal Behav 2:544–547
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559
Zhou J, Jia F, Shao S, Zhang H, Li G, Xia X, Zhou Y, Yu J, Shi K (2015) Involvement of nitric oxide in the jasmonate-dependent basal defense against root-knot nematode in tomato plants. Front Plant Sci 6:193
Acknowledgements
Work in my laboratory is supported by ERDF co-financed grants from the Ministry of Science and Innovation (Recupera 2020-20134R056) and the Junta de Andalucía (group BIO192) in Spain.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Corpas, F.J. (2016). Reactive Nitrogen Species (RNS) in Plants Under Physiological and Adverse Environmental Conditions: Current View. In: Cánovas, F., Lüttge, U., Matyssek, R. (eds) Progress in Botany Vol. 78. Progress in Botany, vol 78. Springer, Cham. https://doi.org/10.1007/124_2016_3
Download citation
DOI: https://doi.org/10.1007/124_2016_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-49489-0
Online ISBN: 978-3-319-49490-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)