Climate Change and Plant Abiotic Stress Tolerance || Role of Nitrosative Signaling in Response to Changing Climates

6

Role of Nitrosative Signaling in Response to Changing Climates

Panagiota Filippou, Chrystalla Antoniou, and Vasileios Fotopoulos

Abstract

The increased frequency and extent of global climatic changes and associatedextreme environmental events remarkably influence plant growth and develop-ment, ultimately affecting crop productivity throughout the world. In addition tothe well-documented enhanced accumulation of reactive oxygen species followingabiotic stress factors, a large amount of research carried out during the last decadeimplicates the participation of nitric oxide and other reactive nitrogen species(RNS) leading to nitrosative stress in the plant’s responses to environmentalstimuli. The imposition of abiotic stresses is known to cause overproduction ofRNS, which ultimately inflicts a secondary oxidative and nitrosative stress, leadingto various signaling responses. However, our understanding of nitrosativesignaling remains poorly understood. The present chapter represents an up-to-dateoverview of the literature in terms of the important role played by nitrosativesignaling in model as well as crop plants in response to increasingly changingclimates.

6.1

Introduction

Environmental stress resulting from constantly changing climates has a significantnegative effect on crop productivity worldwide [1]. Over the past years reactivenitrogen species (RNS) have emerged as signal molecules involved in a number ofimportant physiological processes in plants in a similar fashion to reactive oxygenspecies (ROS) [2–4], although knowledge on the outcomes of oxidative andnitrosative signaling is still unclear [5]. It is also established that RNS, along withROS, are key players in the plant’s response to a multitude of environmentalstimuli such as salinity, drought, heavy metals, and high light intensity [6,7].Interestingly, the existence of a cross-talk between ROS and nitric oxide (NO) has

137

Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill.� 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

been recently documented [5], and there is increasing evidence that NO may beinvolved in the phenomenon of priming, in which transient pre-exposure to NOcan induce tolerance against subsequent stress waves (reviewed in [8]), thushighlighting the important role of NO and RNS in general in abiotic stressresponses as signaling molecules.The term “RNS” has been formulated to designate NO and the NO-derived

molecules such as nitrogen dioxide (�NO2), peroxynitrite (ONOO�), S-nitrosothiols

(RSNOs), and S-nitrosoglutathione (GSNO) [9]. Nitrosative stress is induced bypathophysiological levels of NO and S-nitrosothiols, resulting from thenitrosylation of critical protein cysteine (Cys) thiols (S-nitrosylation) and metalcofactors [10]. NO-triggered defense responses are now widely recognized[11,12]. NO can also have a direct, protective effect against abiotic stressfactors, as it alleviates the deleterious effects of ROS in establishing stressresistance responses [11], partly by increasing the activity of antioxidantenzymes [13]. Research is currently focusing on the understanding anddeciphering of the mechanism of cellular nitrosative status induction, with theultimate aim to aid in the clarification of the plant’s global stress response andthe identification of potential targets for genetic manipulation and cropimprovement. The present chapter provides an up-to-date description offindings (key studies summarized in Table 6.1) focusing on the role ofnitrosative signaling in response to major abiotic stress factors.

6.2

Salinity

High salt (salinity) is a critical environmental factor that affects plant productivitydue to its negative effects on plant growth, ionic balance, and water relations,including several key metabolic processes [14–16]. Nowadays, salinity affectsapproximately 830Mha worldwide and is becoming an increasing problem inregions where saline water is used for irrigation [17].During salinity stress, Naþ enters the cells, and its over-accumulation induces

ionic and osmotic stress in plants [18], modifies plant cell plasma membrane lipidand protein composition, and eventually disturbs normal growth and development[19,20]. In many plant species, it has been shown that NaCl provokes oxidativestress due to ROS accumulation [21,22]. Consequently, plants appear to possess awide array of defense mechanisms to protect themselves from the deleteriouseffects of salinity stress. NO is one of the signaling molecules important in defenseresponses against salinity stress in plants [23–25].Although the role of NO as a sole molecule or as part of RNS has been reported

in abiotic stresses of different plant species (for a review, see [4,26]), the dataavailable for salinity stress can sometimes be contradictory, depending on the plantspecies and the variety of the salinity treatment.Several studies have demonstrated that NO production in certain plants is

increased by a wide range of stresses, although the specific source of NO has not

138 6 Role of Nitrosative Signaling in Response to Changing Climates

Table 6.1 Summary of up-to-date research focusing on the role of nitrosative signaling in

response to key abiotic stress factors (representative examples shown).

Abiotic stress Plant Reference(s)

Salinity Olive [35,36]Sunflower [42]Arabidopsis [37,52]Poplar [41]Citrus [33,34]Red kidney bean [43]Rice [46]Cucumber [24,48]Reed [53]Maize [50]

Drought Barrel medic [7]Tobacco [27]Pea [73]Wheat [73,80]Cucumber [75]Arabidopsis [78,79,102]Maize [74]Broad bean [83]Reed [84]Rice [99]

Heavy metals Pea [105,110]Soybean [108,124]Arabidopsis [109,112]Mustard [110]Barrel medic [114]Rice [123]Wheat [127]Tomato [126]

Heat Tobacco [27]Pea [6]Arabidopsis [130,131]Reed [133,134]Rice [46]Chrysanthemum [138]

Chilling/freezing Loquat [142,143]Arabidopsis [144,145]Pea [6]Mustard [147]Kiwifruit [148]Tomato [140]Mango [150]Cucumber [151]

Anoxia/hypoxia Alfalfa [156]Arabidopsis [64]Barley [158]Tobacco [164]Apple [168]

6.2 Salinity 139

been determined [27–29], while many of the available data have been obtained byindirect studies using exogenous NO donors dependent on the type of NO donorsemployed [30,31].The important aspect of NO signaling regulation upon salinity stress is NO

production, which is tightly linked with the NO mobility and communicationbetween different cellular compartments. NO was detected using the specific NO-sensing fluorochrome DAF-2 DA in vascular bundles of olive and citrus leavesexposed to high salinity [32–35]. In olive plants grown under in vitro conditions, saltstress (200mM NaCl) induces nitrosative stress, while the general increase in theseRNS taking place mainly in vascular tissues could play an important role in theredistribution of NO-derived molecules throughout the different organs ofthe plants [35,36]. In Arabidopsis, peroxisomes have been shown to be required forthe accumulation of NO in the cytosol during salinity stress [37]. Furthermore,attempts to enhance salinity tolerance are currently being applied in cell-type-specific manipulation of transport processes in commercially important plantssuch as rice and barley [38,39].Salt stress sensitivity during germination was observed in Arabidopsis mutant

Atnoa1 plants with an impaired NO biosynthesis [40], while calluses from Populuseuphratica with enhanced nitric oxide synthase (NOS)-like activity displayed salttolerance [41]. It has also been demonstrated that the endogenous generation of NOin sunflower seedlings appears to be mediated by NOS activity-provokedbiochemical adaptation during seedling growth under salinity conditions [42]. Inaddition, Liu et al. [43] showed that the enzyme glucose-6-phosphate dehydrogen-ase played a vital role in nitrate reductase-dependent NO production and inestablishing salt stress tolerance in red kidney bean roots.The clarification of the signaling function of NO in plant responses to salinity

was further studied by exogenous NO applications. Treatment with various NOdonors was shown to improve salt stress tolerance in several plant species [11,12].When exposed to NO donors, NO-associated salt priming action was evident in

the succulent shrub Suaeda salsa, a halophyte, demonstrating that NO stimulatesseed germination more efficiently than nitrate under salt stress [44]. Pretreatmentof NO effectively increased the total soluble protein, and enhanced the activities ofendopeptidase and carboxypeptidase in plants under salt stress [45]. Moreover, rootapplied pretreatments with a NO donor induced salt-specific responses in leaves ofcitrus plants [33,34]. Furthermore, the commonly used NO donor sodiumnitroprusside (SNP) was found to significantly alleviate the oxidative damage ofsalinity to seedlings of rice [46], lupin [47], and cucumber [48], enhance seedlinggrowth [49], and increase the dry weight of maize and Kosteletzkya virginicaseedlings [50,51] under salt stress.For instance, Arabidopsis mutant Atnoa1, with reduced endogenous NO levels

and salt stress sensitivity [40,52], when treated with exogenous NO (SNP), alleviatedthe oxidative damage caused by NaCl stress while inhibition of NO accumulation inthe wild-type plants resulted in the opposite effects. Atnoa1 mutants displayed agreater Naþ/Kþ ratio in shoots than the wild-type plants when exposed to NaCl, butSNP treatment attenuated this elevation of the Naþ/Kþ ratio [11,40]. Furthermore,


following imposition of 200mM NaCl stress in the calluses of reed (Phragmitescommunis), the addition of SNP stimulated the expression of the plasma membraneHþ-ATPase, indicating that NO serves as a signal inducing salt resistance byincreasing the Kþ/Naþ ratio [53].NO is typically applied to salt-treated experimental plants through various NO

donors that may not mimic physiological situations. Therefore, it is possible thatthe signal transduction pathway activated by exogenously applied NO donors forproducing NO may differ from the endogenous pathway induced by salt stress-driven NO generation [54,55].A number of mechanisms have been described for achieving NO-mediated salt

stress tolerance in different plant species. A transient increase in NO was shown toact as a signaling molecule in achieving enhanced salt tolerance in maize leaves byincreasing the activities of vacuolar Hþ-ATPase and Hþ-PPase, which provide thedriving force for Naþ/Hþ exchange [50]. Exogenously applied NO is also known toinduce antioxidant enzymatic activity in response to high salt conditions [55]. NOin all these situations does not act in isolation, but in concert with other signals,such as ROS and hormones, in order to control the development of salt tolerancemechanisms [55].Overlapping functions of H2O2 and NO in salt tolerance are described in citrus

plants [33,34]. It is possible that cell-to-cell and/or tissue-to-tissue NO signaling canbe mediated by the various RNS generated during the strong interaction of NOwith ROS, particularly evidenced under salt-derived oxidative/nitrosative stresssituations [35]. For instance, in 5-month-old bitter orange (Citrus aurantium L.)trees, root pretreatment with H2O2 or SNP induced major antioxidant defense(superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), andglutathione reductase) responses in the leaves of citrus plants grown both in theabsence or presence of 150mM NaCl for 16 days [34].Additionally, the defense mechanism of NO action against salinity involves the

reduction of membrane permeability, rate of ROS production, malondialdehyde(MDA), H2O2, and intercellular CO2 concentration (Ci) under salt stress byinducing ROS scavenging enzyme activities of CAT, POD, SOD, APX [56], andproline accumulation [47,48,51]. Enhanced ROS scavenging enzyme activitiesfollowed by expression of several stress-responsive genes were detected in NOdonor SNP-treated salt-stressed rice seedlings [25,46]. NO was shown to induce theexpression of transcripts for stress-related genes such as sucrose-phosphatesynthase and D0-pyrroline-5-carboxylate synthase [46]. Moreover, NO participates inthe enhancement of photosynthesis by inducing photosynthetic pigments undersalt stress [48,57], ATP synthesis, and two respiratory electron transport pathwaysin mitochondria [58,59].Protein post-translational modifications like S-nitrosylation could also contribute

to NO signaling during salt stress [25,33]. NO accumulation under in vivo salinitystress conditions [37] participates in the generation of peroxynitrite and inenhancing protein tyrosine nitration, as a marker of nitrosative stress [39]. Onemode of NO action in the phloem could be, therefore, the tyrosine nitration ofphloem proteins, found upon salt exposure [4,35,60,61].

6.2 Salinity 141

The effect of NO on major protein kinases, such as mitogen-activated proteinkinases (MAPKs), in plant responses to salt stress has also been investigated [62].The NO-induced osmotic stress-activated protein kinase (designated as NtOSAK)activation in salt-stressed tobacco cell suspensions occurred possibly via thephosphorylation of two residues rather than S -nitrosylation [63]. It was also shownthat NO can exert its modulating function on MAPK activity through the wholeplant, as exposure of Arabidopsis thaliana roots to SNP-driven nitrosative stresscan induce a rapid activation of protein kinases with MAPK-like properties inshoots [64].Moreover, it is possible that NO does not act alone, but interacts with other salt-

depended signaling to establish the salt stress response. For example, phytohor-mones (e.g., auxin, abscisic acid (ABA), ethylene, jasmonic acid) may betransported from salt-treated roots to leaves to induce NO synthesis and/or triggerNO transport [55]. Another important issue of NO signaling during salt stress is thegeneration of S -nitrosoglutathione, which is a transporting glutathione-bound NOmolecule [35].Hydrogen sulfide (H2S), another gaseous messenger molecule, promotes

germination and alleviates salinity damage involving the NO pathway, partially dueto the induction of antioxidant metabolism as well as the re-establishment of ionhomeostasis [65].Another possibility is that NO systemic signaling function may be mediated by

arginine-dependent NO production. In fact, de novo arginine biosynthesis in leaveshas been described as a response of plants to salinity [66], whereas an enzymaticL-arginine-dependent production of NO (NOS-like activity) has been demonstratedin leaf extracts from salt-stressed plants [35].Polyamine levels correlate with NO via L-arginine, a common precursor in

polyamine biosynthesis [24,67], whereas the importance of polyamines in saltstress tolerance has been reported in several plants [25,68,69]. Exogenous SNPapplication regulated the high (triamine spermidine þ tetraamine spermine)/putrescine value and the accumulation of spermine, thus enhancing the salttolerance of cucumber seedlings [24]. Furthermore, considering the function ofpolyamines, polyamine catabolism enzymes (diamine oxidase, polyamine oxidase),and NO in salt stress, one could speculate that polyamine-induced NO generationmight be an intermediate candidate involved in salt stress tolerance [25].

6.3

Drought

Water is crucial for plant growth and development. The constant reduction of watersupply in many areas around the world could affect global climate change scenarios[70]. Around 64% of the global land area is affected by drought (FAO World SoilResources Report 2000, ftp://ftp.fao.org/agl/agll/docs/wsr.pdf ). It has been knownfor many years now that drought, in combination with high temperature andradiation, poses the most important environmental limitation to plant survival and


ftp://ftp.fao.org/agl/agll/docs/wsr.pdf

crop productivity [71]. However, many plants possess the ability of acclimation andadaptation to water deficit by triggering several physiological, biochemical, andmolecular procedures [72]. Many molecules have a role in the plant response towater stress, but some of those orchestrate vital processes for the cell. NO is one ofthose signaling molecules, participating in several signaling pathways andmetabolic procedures.In the last decade, numerous studies have been carried out in order to reveal the

multifunctional nature of NO in regulating the plant response to dehydration. Themajority of them illustrate that drought promotes endogenous NO production indifferent plants, such as pea, wheat, tobacco, and barrel medic [7,27,73]. Theprotective role of exogenous and endogenous NO in water deficit is highlighted inseveral reports (e.g., [74]). Recently, Arasimowicz-Jelonek et al. [75] reported thatsevere drought led to a remarkable NO accumulation in cucumber roots incomparison with roots treated to mild (5–10 h) water deficit, which showed slightlyincreased NO synthesis in root tips. Moreover, exogenous application of NO donordecreased the level of lipid peroxidation in water-stressed cucumber roots byreducing the activity of lipoxygenase [75].Several defense responses are activated under drought conditions. The main

mechanism to limit the effect of low water accessibility is stomatal closure as a wayto conserve water [36]. NO was proved to enhance the adaptive plant response byregulating stomatal closure that was induced by the redistribution and synthesis ofABA and low respiration rate [13]. Although the stomatal apparatus is regulatedinitially by ABA, it is also affected by a variety of other molecular intracellularsignaling molecules, such as NO and H2O2. NO synthesis is essentially enhancedin guard cells and accumulation was observed in several stressed plant species as aresult of ABA-induced stomatal closure [11,13,76–78]. A variety of NO donorsinduce stomatal closure in a dose- and time-depended manner. In this context theireffect can be reversed following exposure to different NO scavengers such as2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (PTIO) and carboxy-2-phe-nyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (cPTIO) [79]. Exogenous NOapplication in wheat plants limited water loss by enhancing stomatal closure andreducing the transpiration rate [76].There are several possible mechanisms that could be involved in the generation

of NO in guard cells in response to ABA or other compounds [13,80]. It was shownthat NOS-like activity contributed in the response of water-stressed wheat plants[13,80]. An accumulation of NO and a remarkable induction of NOS-like enzyme incytosolic and microsomal fractions was observed in maize exposed to 10% poly(ethylene glycol) (PEG), which simulates water stress conditions [74]. Many studiesobserved that potential NOS-like activity was inhibited by chemical inhibitors suchas NG-nitro-L-arginine methyl ester; thus the accumulation of NO in guard cells andABA-induced stomatal closure are simultaneously blocked [52,79]. Additionally,further studies in Arabidopsis guard cells suggested that nitrate reductase is theenzyme implicated in ABA-induced NO synthesis [78].Among others, NO is shown to affect the movement of Ca2þ in order to maintain

stomatal closure by modulating the Ca2þ channels in guard cells. Other authors

6.3 Drought 143

[81–83] supported the involvement of NO as a signaling molecule in the regulationof stomatal closure by showing that NO leads to induction of Ca2þ production,which regulates Kþ and Cl� intracellular channels in Vicia faba through the cGMP/cADPR-dependent signaling pathway.The protective effect of NO in osmotic stress was shown in reed suspension

cultures sensitive and tolerant to drought. Treatment with PEG induced theproduction of NO in stress-tolerant, but not in sensitive ecotypes, protecting reedsagainst oxidative damage [84]. Similarly, exposure of wheat seedlings to mannitolresulted in the accumulation of ABA in leaves in parallel with reduced water loss.Not surprisingly, these results were reversed in the presence of NO scavenger andinhibitors of NOS-like activity [28].Cross-talk between NO and ROS in water-stressed plants has also been reported

([7,25]; e.g., see Figure 6.1). Experimental evidence supported that H2O2 and NO

Figure 6.1 Effect of drought and rewatering on

the phenotype and nitrosative status of

Jemalong A17M. truncatula plants. (Adapted

from Filippou et al. [7].) (I) “A” represents

healthy, control plant, “B” showsaplant 11days

after drought imposition, while “C”

demonstratesaplant rewateredfor2daysafter9

days of drought. (II) NO content in leaves (D)

and roots (E) of Jemalong A17M. truncatula

followingdroughtandrewatering.Datadenoted

with different letters are statistically different

according to Tukey’s pairwise comparison test

(p< 0.05).


function synergistically as essential signals for coordinated stomatal function inABA-induced stomatal closure [82]. It has been reported that the presence of NOdonor and ROS induces a higher production of ABA in wheat roots as a response todrought, whereas in the presence of inhibitors of NO and ROS, ABA synthesis wassignificantly lower [85]. Similarly, the observed interaction between NO and ROSduring water stress in wheat seedlings was induced by ABA signaling [28].Moreover, the important role of the MAPK signaling pathway, which is activated byABA, and the synergistic action of NO and H2O2 has also been reported [82,85,86].NO has a dual role, protective or deleterious to the cellular status depending on

its concentration [87,88]. A variety of NO donors induce stomatal closure in a dose-and time-dependent manner. Exogenous application of high-dose NO provokesstress as a consequence of uncontrolled oxidative stress and the inability ofantioxidant systems to scavenge the ROS [89]. In contrast, lower concentrations ofSNP (NO donor) alleviated ROS, accelerated protein synthesis, enhanced thephotosynthesis rate, and induced the production of H2O2 scavenging enzymes(CAT and SOD), leading to water loss of leaves that were treated with PEG [90].Although the dual role of NO depending on its concentration and on the situationis well established, the NO-triggered response mechanisms during environmentalstimuli such as drought need to be further elucidated [91].Taking into account the observation of exogenous and endogenous NO-induced

stomatal closure in guard cells, a possible mechanism by which NO regulates themembrane ion transporter and water movement was further investigated. NO, as ahighly diffusible and reactive molecule, is able to directly or indirectly interact withseveral cellular proteins [92]. Consequently, NO is able to modify soluble guanylylcyclase, which generates the second messenger cGMP, and the reversiblemodulation activity of S-nitrosylation proteins. These molecules constitute themajor components of the signaling function of NO [23,93]. Several studies supportthat cGMP is a NO signaling intermediate. In pea epidermis and Arabidopsis guardcells, an increase of cGMP levels was observed after treatment with ABA or SNP.These results were reversed by coincubation of plant tissue with PTIO. In addition,pharmacological work using cell-permeable cGMP and inhibitors of NO-sensitivesoluble guanylyl cyclase showed that, although an elevated level of cGMP isessential for effective ABA-induced stomatal closure, the synergistic effects of otherABA-stimulated signaling pathways are still necessary [94].There is remarkable evidence that indicates that NO is a critical factor in the

activation of antioxidant enzymes that should be necessarily present in water stressas a result of the high concentration of ROS [12]. As already mentioned, ABA wasshown to induce the synthesis of NO and H2O2 during drought, subsequentlyactivating potential signal transduction pathways. However, the accumulation ofROS caused by water stress can have deleterious effects, including ion leakage,DNA fragmentation, and even cell death [11]. Consequently, the antioxidant role ofNO is crucial to control the level of ROS, thus preventing oxidative stress in plantssubjected to drought conditions. Sang et al. [74] demonstrated that the rapidproduction of NO in water-stressed wheat was accompanied by an induction ofantioxidant enzymes such as SOD, APX, and glutathione reductase. Exogenous

6.3 Drought 145

application of NO in Dendrobium huoshanense treated with 10% PEG triggered theantioxidant mechanism by inducing several enzyme, such as SOD, POD, and CAT,and reducing the content of MDA, 7 days after the exposure to SNP [95]. To confirmthe effect of SNP treatment, NO scavenger cPTIO was added simultaneously withSNP [95]. Investigation of the effect of drought and rewatering in Medicagotruncatula plants showed a parallel generation of NO and induction of transcripts ofantioxidant enzymes in a differential spatiotemporal regulation. Although severalROS scavenger enzymes were synthesized to reduce the drought-induced oxidativedamage, rewatering restored the expression levels of most genes, mainly in leaves[7]. Likewise, in Zea mays leaves, the NO-dependent antioxidant response wasdecreased by NO scavengers and NOS-like inhibitors [85].Another frequent response of plants to drought stress is the accumulation of

compatible osmoprotectants including proline, sugars, betaine, and glycine [96], aswell as other metabolites such as polyamines. Proline synthesis is essential not onlyfor its osmoprotectant role, but it might also act as a free radical scavenger,stabilizing the protein structure and decreasing cell activity [97,98]. Exogenousapplication of SNP under water stress increased the content of proline in wheat andrice [90,99], while drought-stressed M. truncatula plants also increased prolinecontent in correlation with an increase NO production [7]. With reference topolyamines, these small aliphatic amines have a substantial role in a variety ofdevelopmental and physiological processes, as well in environmental stresses[100,101]. Considering the common functions of NO and polyamines, a linkbetween NO synthesis and polyamine production under water deficit wasestablished [25]. Exogenous application of two main polyamines (spermidine andspermine) resulted in increased NO generation in Arabidopsis plants [102].Exogenous polyamine application in cucumber seedlings showed a remarkableproduction of NO during drought stress. Furthermore, early and periodicalbiosynthesis of NO and direct response to stress deficit may be caused byspermidine and spermine application [25].

6.4

Heavy Metals

Heavy metal contamination affects the biosphere in many places worldwide [103].Various studies have been conducted in order to evaluate the effects of differentheavy metal concentrations in plants. For instance, soil acidity (pH 5.0), acharacteristic of over half of the world’s arable land, poses a serious limitation tocrop production worldwide, principally through the effect of promoting Altoxicity [104].The vital role of NO in heavy metal stress tolerance is mainly carried out through

the enhancement of antioxidant enzyme activities, thus alleviating the toxicity ofheavy metals [12]. NO-mediated detoxification and antioxidation function wasfound in soybean cells exposed to Cd and Cu, and inHibiscus moscheutos exposed totoxic Al3þ levels [11]. In addition, cross-talk between ROS, NO, and Ca2þ has been


proposed for the defense responses of pea plants exposed to Cd [105]. The signalingmode of NO action at the molecular level includes protein modification by bindingto critical Cys residues, heme or iron–sulfur centers, and Tyr residue nitration viaperoxynitrite formation [106].The effects of different heavy metals on endogenous NO content in different

plant species and tissues is a matter of continuous research and controversy,depending on the different heavy metal concentrations, the ages of the plants, andthe duration of the treatment used [107].Soybean cells treated with 4 or 7 mM Cd2þ for 72 h exhibit a dose-dependent and

rapid production of NO, which may suggest that NO functions as a signalingmolecule involved in alleviation of the heavy metal stress [108]. Recently, Cd-induced increases of NO have been reported in Arabidopsis cell suspension cultures[109]. Furthermore, Bartha et al. [110] demonstrated an increase in NO content inCd-, Cu-, or Zn-exposed roots of Brassica juncea L. and Pisum sativum L., indicatingdifferent NO levels with these heavy metal loads. Tewari et al. [111] alsodemonstrated that NO increases in the adventitious roots of Panax ginseng exposedto 50mM Cu for 24 h.In contrast, Ille9s et al. [112] reported that treatment with 90 mM Al reduces NOS-

like activity and NO production in Arabidopsis roots. Tian et al. [113] also discoveredthat treatment with 100 mM Al for 20min induces a rapid decrease of NO in theroots of 4-day-old H. moscheutos seedlings. In addition, a recent report showed thatNO significantly decreases after treatment with 50mM Cd for 48 h in M. truncatularoots [114]. Therefore, the conflicting results on the relationships between NO andheavy metal toxicity are attributed to the impacts of heavy metals on NO contentand the different sources of NO production in plants [115].NO is known to be engaged in auxin (indole acetic acid (IAA))-mediated

signaling pathways under physiological conditions [116]. Recently, Xu et al. [114]demonstrated that NO may participate in maintaining the auxin equilibrium byreducing IAA oxidase activity in roots of M. truncatula subjected to Cd stress, thusalleviating the negative effect of Cd on root growth inhibition.In the past decade, experimental designs revealed that exogenously applied NO

can provide protection against heavy metal toxicity (i) due to its ability to indirectlyscavenge heavy metal-induced ROS and increase the antioxidant enzyme activity inplants [117], (ii) by affecting root cell wall components (NO might increase heavymetal accumulation in root cell walls and decrease heavy metal accumulation in thesoluble fraction of leaves in plants) [118], and (iii) NO could function as a signalingmolecule in the cascade of events leading to changes in gene expression underheavy metal stresses [86,119,120]. Although many authors have reported the effectsof exogenous NO in alleviating heavy metal toxicity in plants, some authors havedemonstrated that the amelioration effects depend on the concentration ofexogenous NO used in the experiments [105,113,114,118].Interestingly, exogenous NO application in Cd-stressed plants is another example of

controversy, since although the first pharmacological approaches revealed thatexogenous NO can alleviate Cd toxicity in plants, recent reports have indicated thatNO contributes to Cd toxicity by promoting Cd uptake and subsequent metal-induced

6.4 Heavy Metals 147

reduction of root growth [121]. An additional analysis indicated that the accumulationof NO in Arabidopsis root cells contributes to Cd toxicity also by favoring Cd2þ versusCa2þ uptake and/or Ca2þ extrusion, partly by modulating the activity of Ca2þ-permeable channels and/or Ca2þ transporters [121,122].Moreover, there are many reports indicating the importance of exogenous NO in

protecting against the deleterious effects of heavy metals. For instance, it wasdocumented that exogenous NO alleviated Cd toxicity in rice by increasing pectinand hemicellulose content in root cell walls, increasing Cd deposition in root cellwalls, and decreasing Cd accumulation in soluble fractions of leaves [118].More specifically, exogenous SNP application reduced Cu toxicity and NH4

þ

accumulation in rice leaves reversed by cPTIO [123] and decreased the Al3þ toxicity

in root elongation of Hibiscus moschetuos [113]. The detoxification and antioxidativeproperties of NO have also been found in soybean cell cultures under Cd and Custress [124]. In addition, the exogenous application of NO donor to Artemisia annuaplants counteracts the toxicity of B or Al, while inducing the biosynthesis ofartemisinin (the most promising antimalarial drug) in the presence of excess of Band/or Al in the soil [125].Regarding the mechanisms of SNP-induced alleviation of heavy metal toxicity,

SNP treatment alleviated the growth inhibition induced by CuCl2 in tomato plantsvia ROS-scavenging enzymes, reduction of H2O2 accumulation, and Hþ-ATPaseand Hþ-PPase induction activity [126]. Additionally, Hu et al. [127] also found thatpretreatment with NO improved wheat seed germination, and alleviated oxidativestress against Cu toxicity by enhancing SOD and CAT activity and by decreasinglipoxygenase activity and MDA synthesis [127,128]. Pretreatment with SNPincreased proline accumulation in Cu-treated algal cells by about 1.5-fold, while thiseffect could be blocked by the addition of cPTIO [127,128]. Cu and NO were able tostimulate D0-pyrroline-5-carboxylate synthetase (P5CS) activity, the key enzyme ofproline biosynthesis, and upregulate the expression of P5CS in Cu-treated algae.

6.5

Heat Stress

As every plant has an optimum temperature for growth and development,temperatures out of the optimal range (higher or lower) could potentially beharmful for plants. The most evident consequence of global climate changes is theincrease of temperature in several agro-climate zones. High temperature cangenerate heat stress to plants. This phenomenon negatively affects agriculturalproductivity. It has been proved that exposure to high temperatures reduces cropyield owing to a shorten life cycle and accelerated senescence [129].Plants have the ability to respond to heat stress by inducing several and diverse

mechanisms. The most common adaptive response to heat is the production ofprimary and secondary metabolites as well as heat shock proteins. The role of NOin heat-stressed plants is to react with proteins, activating different signaltransduction pathways, mainly by inducing the production of antioxidant enzymes.


Furthermore, some studies note the enhanced ability of NO in other biologicalprocedures, including photosynthesis, and the induction of other heat stress factors[46,130].Several studies have shown remarkable NO generation under high temperature,

depending on plant species as well as the duration and degree of exposure [36]. Forinstance, heat treatment in tobacco plants at 40 �C for 7min led to a direct andsignificant increase of NO in adaxial epidermal cells [27]. In contrast, pea plantexposure at 38 �C for 4 h presented a decline in NO content without a remarkableinfluence in NOS-like activity. However, a 3-fold increase of S-nitrosothiol wasreported, demonstrating that NO acts directly with proteins to produce othersignaling molecules [6]. Different Arabidopsis mutants sensitive to heat stressshowed that S-nitrosogluthathione reductase (GSNOR) regulates the intracellularcontent of S-nitrosothiols, thus offering thermotolerance as well as the enhance-ment of plant growth and development [131]. Additionally, suspension culture heat-stressed cells of tobacco Bright Yellow-2 demonstrated low NO production underexposure at 35 �C compared with 55 �C heat-shocked cells, which were reported tohave rapid NO accumulation [132].Since it is well established that NO production occurs under heat stress, a major

goal of the scientific research was to determine the role of NO in the alleviation ofheat stress. The most common function of NO during extreme temperature mightbe the decrease of free radicals – mainly ROS [2]. High temperature can causeoxidative damage by accumulating ROS into the cell, leading to protein denatura-tion, enzyme activation, generation of lipid peroxide, and substantial inhibition ofphotosynthesis and plant growth [133]. As a result, NO involvement is potentiallyuseful for cell viability by inducing the synthesis of antioxidant enzymes.Application of two NO donors, SNP and S-nitroso-N-acetylpenicillamine, in twoecotypes of reed calluses dramatically decreased oxidative damage and growthsuppression by elevating the activity of SOD, APX, CAT, and POD [134]. NOactivated the antioxidant mechanism and elevated heat resistance of heat-stressedwheat coleoptiles of seedlings that were pretreated with 500 mM SNP depending onthe Ca2þ concentration and ROS [135].A wide range of key signaling molecules acting as second messengers, including

Ca2þ, salicyclic acid, and H2O2, are implicated in response signaling to heatstresses [136,137]. A great deal of evidence suggests that ABA and NO, the twomajor signaling molecules, cross-talk in different abiotic stresses, including heatstress. More specifically, results by Song et al. indicated that NO could represent thekey intermediate molecule for ABA-induced heat stress thermotolerance, implyingthat NO inhibition blocked the protective effect of exogenous ABA in reed calluses,whereas the opposite effect was not observed [133].Other important biological and physiological mechanisms in which NO may be

implicated as a response to high temperatures are the activation of heat shockfactors and regulation of photosynthesis [12,46]. It was observed that heat-stressedrice seedlings exposed to low levels of H2O2 and NO, compared with non-treatedcontrols, survived as a result of higher quantum yield for Photosystem II [12,46]. Bycomparison, proteomic analysis in sunflower seedlings that were exposed to 38 �C

6.5 Heat Stress 149

for 4 h showed that nitration of some specific factors caused inhibition of theactivity of proteins implicated in the photosynthetic apparatus, such as carbonicanhydrase and ferredoxin-NADP reductase, although the effect of NO onphotosynthesis under heat stress needs to be further elucidated. Exogenousapplication of NO also partially alleviated heat stress by preventing the decrease ofphotosynthetic pigment content and photosynthetic rate in Chrysanthemummorifolium [138]. Experimental evidence in Arabidopsis transgenic lines thatoverexpress AtCaM3, a key heat-stress factor, present NO as an enhancer of theDNA-binding ability of heat stress transcription factors, also stimulating heat shockprotein 18.2 (HSP 18.2) expression [130].

6.6

Chilling/Freezing/Low Temperature

Low temperature is considered to be one of the major abiotic stresses that negativelyaffect both vegetative and reproductive plant growth [36]. Low temperature, as animportant environmental stress factor, has been shown to regulate the expression ofmany genes, as well as the level of certain proteins andmetabolites [139].Contrarily, one of the main postharvest problems affecting tropical and subtropical

commodities is their sensitivity to low temperature, resulting in chilling injury [140].Crops sown in the fall may experience subfreezing temperatures at the vegetativestage during winter. Freezing damage arises from dehydration and membranedamage caused by the growth of ice crystals. Full expression of frost tolerance at thevegetative stage typically requires a prior period of acclimation during which plantsare exposed to low, non-freezing temperatures [141].Low temperature (cold stress) causes many changes in biochemical and

physiological processes and ROS homeostasis in plants [142–144]. In many studies,researchers tried to determine the role of NO in the alleviation of cold/freezingstress [12,106].The effects of low temperature on endogenous NO generation and the role of

endogenous NO in chilling tolerance have been thoroughly investigated. Lowtemperature at 1 �C triggered a marked increase in endogenous NO levels in loquatfruit, triggering antioxidant enzyme activities, removing ROS, and reducing lipidperoxidation and cellular membrane damage, thus conferring tolerance of the fruit tochilling stress by controlling endogenous NO generation [142,143]. Furthermore, incold-exposedArabidopsis plants, a rapid increase in NO content and the importance ofthe subsequent lipid-based signaling in cold tolerance was observed [145].Similarly, freeze tolerance was shown to be achieved by nitrate reductase-

dependent NO production by modulating proline accumulation in Arabidopsisplants. Cold acclimation up- and downregulated expression of P5CS1 and ProDHgenes, respectively, resulting in enhanced accumulation of proline in wild-typeplants [144]. In addition, the authors reported that the low endogenous NO level innia1 nia2 (nitrate reductase-defective double mutant) leaves resulted in lesstolerance to freezing during cold acclimation plants than wild-type. Further studies


using a nitrate reductase inhibitor, NO scavenger, and NO donor confirmed thatthe nitrate reductase-dependent NO level was positively correlated with freezingtolerance [12].Low temperature was the stress that affected several key components of the

metabolism of RNS, including the production of the highest increase of L-arginine-dependent NOS and GSNOR activities, accompanied by an increase in the contentof total NO and S-nitrosothiols, and an intensification of the immunoreactivity withan antibody against NO2-Tyr [6]. Considering that protein tyrosine nitration is apotential marker of nitrosative stress, the results obtained suggested that lowtemperature can induce nitrosative stress in pea plants [6].Moreover, in leaves of pepper plants, low temperature (8 �C for 24 h) caused cold

stress, characterized by a general imbalance of ROS and RNS metabolism,triggering a rise in lipid oxidation and protein tyrosine nitration, thereby indicatingan induction of oxidative and nitrosative stress promoted by low temperature [146].Similar behavior has been observed in A. thaliana exposed to 4 �C for 1–4 h [145] orduring cold acclimation [144], where the NO content increased. In the case of B.juncea seedlings, low-temperature stress (4 �C for 1–48 h) provoked a rise ofS-nitrosothiols. Moreover, proteomic analysis indicated that low temperatureinduced differentially nitrosylated proteins involved in photosynthesis, plantdefense, glycolysis, and signaling processes [147]. For instance, low temperatureinactivated RuBisCO carboxylase by a process of S-nitrosylation, which is wellcorrelated with the photosynthetic inhibition detected under this type of stress [147].Exogenous NO application has been found to mediate cold resistance in a wide

variety of plant species, such as tomato, wheat, and corn [3]. It is possible that thiseffect was related to the antioxidative action of NO, subjected to cold stress [2].There is evidence to support a role of exogenously applied NO in protectingkiwifruit against oxidative damage caused by ROS during storage [148].Postharvest NO fumigation has also been reported to alleviate chilling injury

during cold storage of Japanese plums (Prunus salicina Lindell), “Kensington Pride”mangoes, and cucumbers [149–151]. The alleviation of chilling injury by NO mightbe related to suppression of ethylene production and respiration [149,150] or bytriggering antioxidant defense mechanisms in the fruit [151].In view of the correlations between polyamines, NO, and proline in plant

tolerance to chilling/cold stress [25,152], together with the potential role of arginaseas a metabolic control point for Arg homeostasis in higher plants, the role ofarginase was also investigated, by applying Arg (the most specific substrate forarginase) or Nv-hydroxy-nor-L-arginine (an ideal inhibitor to study the role ofarginase) to mature green cherry tomato fruit of “Messina” cultivar [140].

6.7

Anoxia/Hypoxia

Low-oxygen environmental conditions that occur in flooded or poorly drained soilscan limit plant growth and development, affecting the distribution of many woody

6.7 Anoxia/Hypoxia 151

plants [153]. The reduction of oxygen below optimal levels, termed hypoxia, is themost common form of stress in wet soils and occurs during short-term flooding,while the complete lack of oxygen, termed anoxia, occurs in soils that experiencelong-term flooding [154,155], both representing serious problems that affect cropgrowth and yield in low-lying rain-fed areas.Plant tolerance to low oxygen availability differs considerably among species, but

despite the wide range of behaviors observed in hypoxia- and anoxia-treated plants,some common responses are present [153].NO levels increase in response to hypoxia in plants [156,157], thus rendering NO

as a potential signaling molecule in response to this stress. Under hypoxicconditions, NO can be formed by anaerobic reduction of nitrite by a portion of themitochondrial electron transport chain. The overall reaction sequence, referred toas the hemoglobin/NO cycle [158], consumes NADH and maintains ATP levels viaan as-yet unknown mechanism [159].NO increase appears to be modulated by levels of plant class I non-symbiotic

hemoglobins, which also increase in abundance in response to hypoxia. It wasshown that NO accumulation in alfalfa root cultures reached 120 nmol g�1 of freshweight after 24 h incubation – 50% lower in the hemoglobin overexpressing lineand 1.5 times higher in the hemoglobin downregulated line [156,160]. Conse-quently, hemoglobins play a central role in the detoxification of excess NO [154],acting as a NO scavenger, by catalyzing the conversion of NO to nitrate in an NAD(P)H-dependent reaction [161].While NO is only formed in oxygenated plant tissues in quantities sufficient for a

signaling function, it becomes a major metabolite in oxygen-deprived tissues,formed primarily by mitochondria and playing a pivotal role in the bioenergetics ofthe hypoxic cell [162].The mechanism of NO scavenging by hemoglobins has been investigated in

plants exposed to anoxic conditions, and was shown to have an importantphysiological role in the maintenance of redox and energy balance [158,161,163],while the opposite process leading to NO formation during anoxia has beendemonstrated in plants [156,164].While NO is formed only in sufficient quantities for a signaling function in

oxygenated tissues, it becomes a major metabolite in hypoxic tissues, playing a rolein the bioenergetics of the hypoxic cell. The net effect is to keep NAD(P)H/NAD(P)þ ratios low while maintaining energy charge and ATP/ADP ratios sufficientlyhigh for short-term plant survival [165].The shift to anaerobic metabolism leads, among others [166], to oxidative stress

by producing ROS. Therefore, an efficient enzymatic antioxidant system mightprovide a defense against the cytotoxic effects of ROS and anoxic stress tolerance[167,168]. Moreover, although gene expression is repressed in response to oxygendeficit, an important subset of genes is induced depending on the extent of oxygendepletion [169].Interestingly, both NO and H2O2 have been found to function as localized and

long-range root-derived signals capable of indirectly activating MAPK-like activityin A. thaliana shoots [64]. Whether the observed increases in NO evolution under


flooding condition from roots or soils act as a positive message in root-to-shootcommunication remains to be elucidated [155].

6.8

Conclusions

In view of the global climatic changes taking place, plants have adapted by quicklyaltering their physiology and metabolism in response to external stimuli. RNSrepresent a group of small but important molecules that can act in a protective orcytotoxic manner depending on intracellular concentrations and are involved in awide array of cellular responses in plants. Fully deciphering the mechanism bywhich a plant identifies and responds to RNS and the induced cellular nitrosativestatus could prove to be remarkably helpful towards the clarification of the plant’sglobal stress response.

Acknowledgments

V.F. would like to acknowledge financial support from Cyprus University ofTechnology internal grant EX032 and Grants-in-Aid from COSTAction FA0605.

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