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Review

Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens Srinivas Agurla, Gunja Gayatri, Agepati S. Raghavendra * Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad 500046, India

A R T I C L E

I N F O

Article history: Received 16 April 2014 Received in revised form 12 July 2014 Available online Keywords: Defense response in plants Nitric oxide Nitrosylation Reactive oxygen species Stomatal closure

A B S T R A C T

Stomata facilitate the loss of water, as well as CO2 uptake for photosynthesis. In addition, stomatal closure restricts the entry of pathogens into leaves and forms a part of plant defense response. Plants have evolved ways to modulate stomata by plant hormones as well as microbial elicitors, including pathogen/ microbe associated molecular patterns. Stomatal closure initiated by signals of either abiotic or biotic factors results from the loss of guard cell turgor due mainly to K+/anion efflux. Nitric oxide (NO) is a key element among the signaling elements leading to stomatal closure, hypersensitive response and programmed cell death. Due to the growing importance of NO as signaling molecule in plants, and the strong relation between stomata and pathogen resistance, we attempted to present a critical overview of plant innate immunity, in relation to stomatal closure. The parallel role of NO during plant innate immunity and stomatal closure is highlighted. The cross-talk between NO and other signaling components, such as reactive oxygen species (ROS) is discussed. The possible sources of NO and mechanisms of NO action, through post-translational modification of proteins are discussed. The mini-review is concluded with remarks on the existing gaps in our knowledge and suggestions for future research. © 2014 Elsevier Inc. All rights reserved.

1. Introduction Stomata are minute pores present on the surface of leaves of terrestrial plants, which facilitate transpiration and CO2 uptake. Stomata also act as gateways for the entry of pathogens. When plants are exposed to drought/water stress, stomata are closed and this response is mediated by mobilization of plant hormones, such as abscisic acid (ABA). Similarly, whenever challenged by plant pathogens, stomatal closure restricts the entry of pathogenic microorganisms and helps in plant innate immunity [1–3]. In view of this emerging concept, several recent reviews summarized the crucial step of stomatal closure as one of the effective components of plant defense responses [4–6]. Many signaling components are common in stomatal closure or defense response, and one of such compound is nitric oxide (NO). NO, a reactive nitrogen species, plays an important physiological role as a signaling component during plant–pathogen interactions, plant resistance, hypersensitive response (HR) and expression of related genes [7–9]. During defense responses, NO interacts with various other signaling molecules upstream and downstream including mitogen activated protein kinase (MAPK’s), reactive oxygen species (ROS), cyclic nucleotides and free Ca2+ [10]. Apart

* Correspondence author. Fax: +91 40 23010120. E-mail address: [email protected], [email protected] (A.S. Raghavendra).

from its effective role in plant defense, NO also plays a major role in stomatal closure induced by ABA as well as the elicitors/pathogen associated molecular patterns (PAMPs) [11]. Studies using NO donors, NO-modulators and mutant plants confirm the role of NO in stomatal signaling cascade [12,13]. There are excellent reviews which appeared in the last 4 years, on the role of NO during stomatal closure [14–16] as well as the importance of NO during the innate immunity responses in plants [8,10,17,18]. However, it is not clear if the regulation by NO of defense responses and stomatal closure is a closely integrated process or NO exerts its effect parallely. Readers interested in the earlier work, may refer to some of the reviews, which appeared before 2009 [7,12,13,19–24]. This article is an overview of the importance of NO during stomatal closure in relation to defense responses against pathogens. The interdependence and interaction of NO and ROS are pointed out. The continuing ambiguity on the enzymatic sources of NO is discussed. The growing interest in molecular mechanisms (Snitrosylation, tyrosine nitration and metal nitrosylation) of NO action is pointed out. 2. Significance of stomatal closure in plant defense response The stomatal aperture is modulated due to dynamic changes in ionic status of guard cells. During stomatal opening, guard cells accumulate osmotically active molecules such as potassium, anions and malate leading to water uptake, increase in the turgor of guard

http://dx.doi.org/10.1016/j.niox.2014.07.004 1089-8603/© 2014 Elsevier Inc. All rights reserved.

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Table 1 Elicitor induced NO production and associated defense responses against pathogens in cell suspensions cultures. Elicitor

Source

Plant system

Rise in NO (fold)

Hypersensitive response

PCD

Reference

Cerebroside

Fusarium sp. IFB-121

Cell suspensions: Taxus yunnanensis

8

Fungal cell wall Phytophthora cryptogea

Cell cultures; tomato Cell suspension: N. tabacum cv Xanthi

~3 7.5

Dead cells shown by Evans Blue staining – Dead cells (Evans Blue staining)

[32]

Chitosan Cryptogein

Fungal elicitor

Pencillium citrinum

Cell cultures: Taxus, Catharanthus, Pueraria

2 to 4

–

[35–37]

Fungal elicitor

Aspergillum niger

>7

–

[38]

Fungal elicitor

Not quantified

Phytoalexin accumulation

–

[39]

Fungal elicitor

Diaporthe phaseolorum f. sp. Meridionalis Fusarium oxysporum

Cell cultures: Hypericum perforatum Cotyledons: Soybean

H2O2 production, activation of PAL and accumulation of taxol PA production Ca2+ mobilization, transcript accumulation of heat shock protein TLSH-1, ethylene forming enzyme cEFE-26 Catharanthine synthesis, activation of PAL, biosynthesis of taxol, puerarin Hypericin production

Cells: Taxus chinensis

15

H2O2 production

[40]

INF1

Phytophthora infestans

Cells: tobacco BY-2

4 to 6

Lipopolysaccharide

Outer membrane of Gram negative bacteria Enzymatic preperation of chitosan

A. thaliana suspension cells

2500

–

[43]

Cell suspension: tobacco

Not quantified

–

[44]

Oligogalacturonic acid Oligosaccharide

Degradation product of plant cell wall Fusarium oxysporum

Cell cultures: Panax ginseng

Not quantified

Activation of protein kinase, expression of HSR genes Defense gene (PR gene) induction Resistance to TMV, activation and elevation of mRNA of PAL Saponin synthesis

Dead cells (Evans Blue staining) Dead cells (Evans Blue staining)

–

[45]

18

Artemisinin accumulation

–

[46]

Xylanase Yeast elicitor

Trichoderma viride Yeast extract

Hairy roots: Artemisia annua Cell cultures: tomato Cells: Cupressus lusitanica

4.5 11

PA and ROS production Phytoalexin biosynthesis

– Dead cells (Evans Blue staining)

[47] [48]

Oligochitosan

[33] [34]

[41,42]

Abbreviations: BY-2, bright yellow-2; cEFE-26, ethylene forming enzyme; HSR, hypersensitive related; INF1, inverted formin 1; PA, phosphatidic acid; PAL, phenylalanine ammonia-lyase; PR genes, pathogenesis related genes; PCD, programmed cell death; ROS, reactive oxygen species; TMV, tobacco mosaic virus; TLSH, heat shock protein.

cells and stretch the aperture to open [3]. The opposite events of stomatal closure, namely the efflux of potassium/anions and movement of H2O from guard cells and flaccid guard cells, cause stomatal closure [25,26]. Several environmental signals, such as high CO2, drought, light, humidity, internal signals such as phytohormones, for example ABA, methyl jasmonate (MJ), ethylene and even elicitors cause stomatal closure. Auxins and cytokinins induce stomatal opening [27–30]. Most of the pathogens, including fungi and bacteria try to enter the plants through natural openings like stomata or wounds. Stomatal closure restricts further entry of pathogens into leaves and is a typical component of plant immune response against pathogenic microbes. Cross-defense responses can also occur during plant–pathogen interactions. For example when Arabidopsis plants are challenged by Pseudomonas syringae DC 3000 (a virulent plant pathogen), stomatal closure is induced, as an initial response, to restrict the entry. After 3 hours of incubation, the pathogen Pseudomonas syringae DC 3000 causes re-opening of the stomata by producing a polyketide toxin, coronatine [1,2]. 3. Elicitors/microbe associated molecular patterns (MAMPs) mediate plant defense responses and stomatal closure Plants initiate basal defense response, soon after sensing the attack by pathogens. The early recognition of the microbial presence is often mediated by elicitors, which are either digested products from the microbial cell walls or produced by the plant cell. There is a cross-talk between host plants and pathogens, mediated by elicitors or molecular patterns. PAMPs are evolutionarily conserved molecular signatures present on both pathogen and nonpathogenic microorganisms, so these are later re-named as MAMPs

[2,31]. Several MAMPs were discovered, such as, flg22 and lipopolysaccharides (LPS) from bacteria; xylanase, chitin, chitosan (a deacylated derivative of chitin) and ergosterol from fungi; and glucan, pep13, elicitin from oomycetes. Effector triggered defense response often culminate in the hypersensitive response and programmed cell death (PCD) (Table 1). Most of these elicitors/PAMPs, e.g. flg22 or oligochitosan, induced stomatal closure in wide spectrum of plants like L. esculentum, C. communis, P. sativum, A. thaliana, N. benthamiana, B. napus (Table 2). Each MAMP is perceived by its cognate receptor present on plasma membrane, and when bound the complex initiates signaling cascade, leading to stomatal closure. For example flg22 is perceived by its cognate receptor FLS2, and chitin by chitin elicitor receptor kinase 1 [56]. Upon perception of the elicitors by their respective patternrecognition receptors on stomatal guard cells, elicitors or PAMPs induce stomatal closure in plants. There is misconception that HR is equivalent to PCD but HR is a subset of PCD and may involve multiple components. For example, elicitor activation causes elevation of ROS, cytosolic free Ca 2+ levels, phytoalexin accumulation, phenyalanine ammonia-lyase (PAL) gene expression and hypericine accumulation [32,34,38,40,48]. 4. Role of nitric oxide in plant innate immunity and stomatal closure Multiple approaches have been used to demonstrate the importance of NO during plant defense responses and stomatal closure. These include (i) modulation of NO by donors or scavengers or inhibitors of NO-synthesizing enzymes: (ii) monitoring NO by fluorescent probes, and finally (iii) validation of the NO role by suit-

Please cite this article in press as: Srinivas Agurla, Gunja Gayatri, Agepati S. Raghavendra, Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens, Nitric Oxide (2014), doi: 10.1016/j.niox.2014.07.004

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Table 2 Effects of elicitors on stomatal movement and increase in levels of NO or ROS in guard cells of different plant species. Elicitor

Stomatal closure and increase in NO or ROS

Plant

Reference

Boehmerin, Harpin and Nep1 Boehmerin, Harpin and INF1 Chitosan Flg22 Oligogalacturonic acid

Closure, NO and ROS Closure, NO and ROS Closure, NO and ROS Closure, NO Closure, ROS

[49] [50] [51,52] [1] [53]

Oligochitosan Yeast elicitor

Closure, NO and ROS Closure, NO and ROS

Nicotiana benthamiana N. benthamiana Pisum sativum A. thaliana Lycopersicon esculentum, Commelina communis Brassica napus L. A. thaliana

[54] [55]

Abbreviations: Flg22, 22 amino acid flagellin peptide; INF1, inverted formin 1; Nep1, necrosis- and ethylene-inducing peptide; NO, nitric oxide; ROS, reactive oxygen species.

able mutants deficient in up-stream and down-stream steps of NO action. The levels of NO in plant tissues, can be increased by NO donors, such as sodium nitroprusside (SNP) or S-nitroso-Nacetylpenicillamine (SNAP) [57]. The levels of NO can be lowered by scavengers like 2-phenyl-4,4,5,5-tetramethyl imidazoline-1oxyl 3-oxide (cPTIO). Examples of inhibitors of NO synthesizing enzymes are N-nitro-L-Arg-methyl ester (L-NAME, inhibitor of NOS like enzyme) and tungstate (NR inhibitor) [58]. These inhibitors decrease NO production, and restrict stomatal closure by ABA, MJ or elicitors [1,27,51,59–63]. The levels of NO can be monitored and related to the extent of defense responses or stomatal closure. Fluorescent dyes, like DAF-2DA are used for monitoring NO in plant cells, but are being questioned for their target-specificity [64]. Studies using DAF-2DA indicated that NO production occurs prior to the ROS [51]. High NO can in turn elevate other signaling components, such as PLDα1, PLD, PA, during stomatal closure [65–68]. Since the use of pharmacological compounds is only of limited use, the role of signaling elements is validated by using Arabidopsis mutants, deficient in a given signaling component. The ABAinsensitive mutants (ABI1 and ABI2) indicated that protein phosphatases could act up-stream of NO in the ABA signaltransduction cascade [22]. Impaired NO production and closure in atrbohD/F, NtbrbohA and NtbrbohB single and double silenced plants in response to ABA or elicitors, demonstrated that ROS production was essential for NO production and subsequent signaling steps [27,50]. Similarly, the use of Arabidopsis mutants (nia1,nia2,nia1/ 2) revealed the role of NR as a possible source of NO [59,69]. The first indications related to the role of NO in defense mechanism came from the studies on potato tuber tissues, treated with l-hydroxy-2-oxo-3,3-bis(2-aminoethyl)-1-triazene (NOC-18, a NO donor), during induction of rishitin (a phytoalexin) accumulation. Such accumulation was restricted by the addition of cPTIO. Pearl millet (Pennisetum glaucum L.) seeds, pre-treated with SNP (NO donor), were able to improve their resistance against downy mildew. Conversely, treatment with cPTIO rendered the plants susceptible for pathogen infection [70]. Lipopolysaccharide (LPS) treated Arabidopsis mesophyll cells showed enhanced NO production, which was restricted by incubating the protoplasts with a mammalian NOS

inhibitor, L-NAME, or cPTIO [71]. Administration of NO donors or recombinant mammalian NOS to tobacco plants (or suspension cells) triggered expression of the defense-related genes such as pathogenesis-related 1 (PR1) protein and PAL. The importance of NO in guard cells during stomatal closure has been extensively studied with reference to ABA. In guard cells, NO production is induced by not only ABA, but also other compounds such as salicylic acid (SA), MJ, chitosan and even ethylene [22,52,60,72,73]. A detailed account of NO in stomatal closure is described in detail recently by Gayatri et al. [15]. 5. Cross talk of NO and ROS during stomatal closure and defense mechanism in plants Enhanced production of ROS and NO, known as radical burst, activates the processes involved in the defense mechanism of the plants. Besides their role in plant defense responses, NO and ROS play a prominent role in stomatal closure, induced by ABA, MJ or elicitors like chitosan [52,74,75]. Thus, there seems to be a strong interaction between NO and ROS [76]. Besides with ROS, NO can interact with several other signaling components (Table 3). However, it is not clear, if ROS induces a rise in NO or vice versa, as the cryptogein induced NO production was only partly regulated by RBOHD (a subunit of NADPH oxidase enzyme) [81]. Real time kinetics of ROS and NO production induced by chitosan in Pisum sativum guard cells demonstrated the probable involvement of ROS in the NO production [51]. The elevated NO levels in guard cells of atrbohD/F mutants of Arabidopsis thaliana by SNP (a NO-donor) also indicated the importance of ROS upstream of NO during stomatal closure [75]. In contrast, oligogalacturonides (OGs) triggered fast and prolonged NO production, along with ROS production by RBOHD, in Arabidopsis leaf discs. A detailed description of cross-talk between NO and other signaling components during plant innate immunity is given by Trapet et al. [8]. There seems to be a feedback effect of NO on ROS levels, due to protein modifications by NO. For example S-nitrosylation decreased the activity of ROS scavengers like ascorbate peroxidase and catalase, indicating a regulation by NO of ROS accumulation [82]. Further, NO on reaction with superoxide leads to the formation of

Table 3 Interaction of NO with other signaling components during stomatal closure and elicitor induced defense response in different plant species. Interacting component

Response

Elicitor

Plant

Reference

Ca2+

Resistance to Botrytis cinerea

OGs VBcPG1

Cytosolic pH ROS CNGC MAPK NADPH oxidase

Cytosolic alkalinization precedes ROS and NO production during stomatal closure NO production occurs downstream of ROS during chitosan induced stomatal closure Enhanced Ca2+ transport into the cell and induced resistance to LPS Radical burst via MAPK signaling cascade Production of NO regulated by NADPH oxidase

Chitosan Chitosan LPS INF1 Cryptogein

Arabidopsis thaliana Vitis vinifera cv. Gamay Pisum sativum P. sativum A. thaliana Nicotiana benthamiana Nicotiana tabacum

[77] [78] [52] [51] [79] [80] [81]

Abbreviations: Ca2+, calcium; CNGC, cyclic nucleotide gated channel; INF1, inverted formin 1; LPS, lipopolysaccharides; MAPK, mitogen-activated protein kinases; OGs, oligogalacturonides; VBcPG1, Botrytis cinerea endo-polygalacturonase 1.

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peroxynitrite (ONOO−), a tyrosine nitrating agent, which can mediate cell death during defense responses [83]. Yun et al. [84], reported that S-nitrosylation of conserved cysteine-890 residue of NADPH oxidase inhibited its ability of ROS production. 6. Possible role of other gasotransmitters in stomatal closure and defense response Besides NO, gasotransmitters like hydrogen sulphide (H2S) and carbon monoxide (CO) could modulate stomatal movement. In plants, NO can interact with H2S, ethylene or CO, but convincing studies are scanty. H2S donors, such as sodium hydrosulfide (NaSH) promoted stomatal opening and reduced the NO levels [85,86]. On the other hand, García-Mata and Lamattina [87] found that exogenous NaSH and GYY4137 induced stomatal closure in Vicia faba, Arabidopsis thaliana and Impatiens walleriana. Further work is necessary to confirm the role of H2S in stomatal movement and its relationship to NO production. In contrast to conflicting reports on stomatal movement, the literature on H2S role in defense response is convincing. Sulfur deficient plants were quite susceptible to pathogen attack [88]. The helpful role of H 2 S in plant defense may be due to glutathione and glucosinolate production [89,90]. Recently, Li et al. [91] showed that H2S increased ROS production by modulating NADPH oxidase and glucose-6-phosphate activity in Arabidopsis thaliana roots and a similar situation in leaves may relevant for stomatal closure under pathogen attack. In plants, CO is released during conversion of heme to biliverdine IX by heme oxygenase (HO) [92]. Treatment with ABA increased the expression of HO and raised the CO levels. Further, ABA induced stomatal closure was inhibited by the CO inhibitor zinc protoporphyrin (ZnPP) or hemoglobin (Hb), a CO/NO scavenger. These observations point out that NO may be a downstream component in CO induced stomatal closure [93]. Hematin (a CO donor) induced stomatal closure in Vicia faba. The mechanism of CO action during stomatal closure and plant defense needs further study. 7. Sources and mechanism of action of NO The availability of NO in the cell depends on not only its synthesis by various mechanisms, but also the removal. Though the production of NO in plants is beyond doubt, the mechanisms of NO synthesis and contribution of each source for physiological responses are quite uncertain. Plants seem to have multiple sources of NO, including enzymatic and non-enzymatic pathways. Two enzymes that appear to be major sources for NO in plants are nitric oxide synthase (NOS-like) like enzyme and nitrate reductase (NR). However, the roles of NOS-like (or NOA) and NR are yet to be established clearly. 8. Nitric oxide synthase (NOS) Only in animal systems, the NOS induced NO production is well characterized. In plants, the existence of animal NOS homologue is unclear, due to the absence of cognate nucleotide sequence in the plant genome. The ability of L-arginine analogs e.g. L-NMMA (NGMonomethyl-L-arginine) and L-NAME to inhibit NO production suggested that NOS like enzyme was involved in physiological and developmental processes [94]. Polyamines also act as a source of NO in root growth of Arabidopsis thaliana seedlings [95]. But the actual enzymes in these processes are yet to be characterized. 9. Nitrate reductase (NR) A major source of NO in plants appear to be NR [96], although the ability of NR to form NO is less than that 1% of its normal nitrate reduction capacity [97]. There are two types of enzymes in plant

cells capable of producing NO: cytosolic NR and root-specific plasma membrane bound nitrite-NO reductase (Ni-NOR) [98]. The main function of NR is the conversion of nitrate to nitrite, but under unfavorable conditions, such as low oxygen tension or high nitrite concentration, NR can reduce nitrite to NO by using NADP(H) as an electron source [99]. The role of NR in guard cell, as a source of NO is yet to be critically assessed. Desikan et al. [59] reported that NRdeficient nia1nia2 Arabidopsis double mutant guard cells were unable to induce NO production or stomatal closure in response to ABA. Out of these two NR isoforms, NIA1 was mainly responsible for ABA induced NO production and NR induced NO was also involved in cold acclimatization and freezing tolerance in Arabidopsis [27,100]. Nitrite dependent NO formation has been suggested to be involved in the resistance against to the Pseudomonas syringae. 10. Other enzymatic and non-enzymatic sources The Ni-NOR found in purified plasma membranes of tobacco (Nicotiana tabacum) roots, may be involved in the reduction of apoplastic nitrite to NO [101]. Such Ni-NOR may be also involved in various physiological processes including root development and symbiosis, but its role in NO production is not yet convincing. Further, the molecular identity of Ni-NOR enzyme is not clear [102]. Xanthine oxidoreductase (XOR) is a peroxisomal enzyme, normally catalyzing the oxidation of hypoxanthine to uric acid with the concomitant production of either NADH or superoxide radical (O2−) [103]. Purified XOD from bovine milk reduces nitrite to NO under anaerobic conditions, using NADH or xanthine as reductant [104]. But the role of XOR in NO production in plants needs further investigations. Non-enzymatic reactions can lead to NO production under extreme physiological conditions, and are considered to be a minor source of NO in plants. The evidence in favor of non-enzymatic NO production in various plant tissues is lacking. The reduction of nitrite into NO occurred under the acidic or highly reduced conditions and was not blocked by NOS inhibitors [105]. Similarly rapid NO production occurred, in Hordeum vulgare (barley) aleurone layers, when nitrite is added to the incubation medium [106]. Again, the significance of such non-enzymatic NO production in plants and particularly in guard cells is uncertain. 11. Direct and indirect actions of NO The action of NO can be direct through post-translational protein modifications or indirect through down-stream components, such as cytosolic Ca2+ mobilization. The interaction of NO with other downstream signaling components play a major role in signal transduction during both stomatal closure and plant defense. The elevated NO down regulates K+ and Cl− influx, promotes K+/Cl− efflux and Ca2+ release during stomatal closure and such NO induced free Ca2+ release occurs via guanylate cyclase and cyclic ADP ribose [11,107]. NO can react with superoxide to form peroxynitrite (ONOO−), another highly reactive molecule [10,17,24,108–112]. Due to its reactivity, NO can modify the proteins through S-nitrosylation, tyrosine nitration, metal nitrosylation leading to the alteration of the protein function [19,113]. In plant cells, nitrosylation occurs widely. For example S-nitrosylation of glutathione (GSH) forms S-nitrosoglutathione (GSNO) which can act as a physiological NO source [114,115]. Post-translational modification of proteins, by the reversible covalent addition of NO to the cysteine residue is involved in many physiological/developmental processes, and defense responses. Two such proteins undergoing S-nitrosylation are; NPR1 (non-expressor of PR1), a transcription factor [115,116], and salicylic acid binding protein 3 (SABP3). The topic of nitrosylation as the basis of NO modulation by NO has been described in detail by Astier et al. [117,118] and Yu et al. [115].

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Fig. 1. Signaling network that operates during ABA or PAMP/MAMP induced stomatal closure. The signaling events triggered by either ABA or PAMP/MAMP lead to the production of NO and ROS and subsequent induction of defense responses, including hypersensitive response (HR) and/or programmed cell death (PCD). The steps of stimulation are represented by forward arrows, while the cross-talks are shown by reversible arrows. Solid arrows indicate events supported by experimental evidence and the broken arrows represent the possible events. In the first step, the elicitor/PAMP/MAMP or ABA, binds to a membrane bound receptor like PRR and ABI, and restricts the activity of protein phosphatase. This leads to activation of OST1 kinase, which in turn phosphorylates the plasma-membrane bound NADPH oxidase (RBOH), to promote the production of H2O2. The increased ROS levels induce NO production. Both ROS and NO can either individually or cooperatively initiate responses like HR and PCD. Parallely, NO can promote stomatal closure, with the help of secondary messengers like cGMP, cADPR and Ca2+, which all regulate the ion channels and promote stomatal closure. The possible sources of NO in stomatal guard cells are NR and NOS like enzymes. Further, PAMP/MAMP can raise the levels of hormones such as ABA, SA and MJ, which further interact to enhance defense responses. Detailed description of these events during stomatal closure and defense response can be found in recent reviews [8,10,14–17,115].

12. Concluding remarks Stomata have long been known to be the entry/exit points for H2O, CO2 and even microbes. The stomatal closure to restrict the entry of pathogenic bacteria, is a part of plants’ innate immunity response. Based on biochemical, pharmacological and mutantsbased evidences, NO and ROS have emerged as major signaling components during stomatal closure induced by plant hormones as well as elicitors [76]. A possible scheme of signaling events occurring stomatal closure by elicitors/ABA is depicted in Fig. 1. Despite the undoubted role of NO and ROS in mediating stomatal closure as well as hypersensitive responses, there is ambiguity on several issues. Plant cells are capable of producing NO, when challenged by biotic or abiotic stresses, but the source of NO in plants is debatable. NR and NOS-like enzymes are the most likely candidates, yet there could be other unidentified enzyme sources. The interactions of NO with ROS are of great physiological significance during not only growth/development but also the responses to biotic/abiotic stress factors which include plant pathogens [115]. The presence of NO and ROS together exert a synergistic action during signal transduction. However, the temporal status of NOrise, in relation to ROS is not clear, as there are claims that NO acts upstream of ROS or downstream of ROS or both. Some of the present

approaches involving the use of fluorescent dyes, NO donors or inhibitors of NO-production are questionable. It is therefore important to develop convincing methodology to monitor/modulate NO in plants. In this regard, stomatal guard cells offer an easy and ideal system to study the signaling components, including NO. The observations made with guard cells are quite relevant to other plant tissues as well.

Acknowledgments The work is supported by a J C Bose National Fellowship (No. SR/ S2/JCB-06/2006) to Agepati S. Raghavendra, from the Department of Science and Technology, New Delhi; and University Grants Commission-Junior Research Fellowship to Srinivas Agurla and Gunja Gayatri We also thank DBT-CREBB, DST-FIST and UGC-SAP-CAS, for support of infrastructure in Department/School.

References [1] M. Melotto, W. Underwood, J. Koczan, S.Y. Nomura, S.Y. He, Plant stomata function in innate immunity against bacterial invasion, Cell 126 (2006) 969–980.

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[2] M. Melotto, W. Underwood, S.Y. He, Role of stomata in plant innate immunity and foliar bacterial diseases, Annu. Rev. Phytopathol. 46 (2008) 101–122. [3] W. Underwood, M. Melotto, S.Y. He, Role of plant stomata in bacterial invasion, Cell. Microbiol. 9 (2007) 1621–1629. [4] V. Nicaise, M. Roux, C. Zipfel, Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm, Plant Physiol. 150 (2009) 1638–1647. [5] C.M. Baker, R. Chitrakar, N. Obulareddy, S. Panchal, P. Williams, M. Melotto, Molecular battles between plant and pathogenic bacteria in the phyllosphere, Braz. J. Med. Biol. Res. 43 (2010) 698–704. [6] W. Zeng, M. Melotto, S.Y. He, Plant stomata: a checkpoint of host immunity and pathogen virulence, Curr. Opin. Biotechnol. 21 (2010) 599–603. [7] L. Lamattina, C. Garcia-Mata, M. Graziano, G. Pagnussat, Nitric oxide: the versatility of an extensive signal molecule, Annu. Rev. Plant Biol. 54 (2003) 109–136. [8] P. Trapet, A. Kulik, O. Lamotte, S. Jeandroz, S. Bourque, V. Nicolas-Francès, et al., NO signaling in plant immunity: a tale of messengers, Phytochemistry (2014) . [9] E. Baudouin, The language of nitric oxide signaling, Plant Biol. 13 (2011) 233–242. [10] F. Gaupels, G.T. Kuruthukulangarakoola, J. Durner, Upstream and downstream signals of nitric oxide in pathogen defense, Curr. Opin. Plant Biol. 14 (2011) 707–714. [11] C. García-Mata, R. Gay, S. Sokolovski, A. Hills, L. Lamattina, M.R. Blatt, Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways, Proc. Natl Acad. Sci. U.S.A. 100 (2003) 11116–11121. [12] S. Neill, R. Barros, J. Bright, R. Desikan, R. Hancock, J. Harrison, et al., Nitric oxide, stomatal closure, and abiotic stress, J. Exp. Bot. 59 (2008) 165–176. [13] I.D. Wilson, D.M. Ribeiro, J. Bright, A. Confraria, J. Harrison, R.S. Barros, et al., Role of nitric oxide in regulating stomatal apertures, Plant Signal. Behav. 4 (2009) 467–469. [14] J.T. Hancock, S.J. Neill, I.D. Wilson, Nitric oxide and ABA in the control of plant function, Plant Sci. 181 (2011) 555–559. [15] G. Gayatri, S. Agurla, A.S. Raghavendra, Nitric oxide in guard cell as an important second messenger during stomatal closure, Front, Plant Sci. 4 (2013) 1–11. [16] C. García-Mata, L. Lamattina, Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange, Plant Sci. 201–202 (2013) 66–73. [17] H. Yoshioka, K. Mase, M. Yoshioka, M. Kobayashi, S. Asai, Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity, Nitric Oxide 25 (2011) 216–222. [18] M. Simontacchi, C. García-Mata, C.G. Bartoli, G.E. Santa-María, L. Lamattina, Nitric oxide as a key component in hormone-regulated processes, Plant Cell Rep. 32 (2013) 853–866. [19] M. Leitner, E. Vandelle, F. Gaupels, D. Bellin, M. Delledonne, NO signals in the haze: nitric oxide signalling in plant defense, Curr. Opin. Plant Biol. 12 (2009) 451–458. [20] J. Durner, D.F. Klessig, Nitric oxide as a signal in plants, Curr. Opin. Plant Biol. 2 (1999) 369–374. [21] C. García-Mata, L. Lamattina, Nitric oxide and abscisic acid cross talk in guard cells, Plant Physiol. 128 (2002) 790–792. [22] R. Desikan, M.K. Cheung, J. Bright, D. Henson, J.T. Hancock, S.J. Neill, ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells, J. Exp. Bot. 55 (2004) 205–212. [23] I.D. Wilson, S.J. Neill, J.T. Hancock, Nitric oxide synthesis and signaling in plants, Plant Cell Environ. 31 (2008) 622–631. [24] D. Wendehenne, J. Durner, D.F. Klessig, Nitric oxide: a new player in plant signaling and defense responses, Curr. Opin. Plant Biol. 7 (2004) 449–455. [25] L.D. Talbott, E. Zeiger, Central role for potassium and sucrose in guard-cell osmoregulation, Plant Physiol. 111 (1996) 1051–1057. [26] A. Vavasseur, A.S. Raghavendra, Guard cell metabolism and CO2 sensing, New Phytol. 165 (2005) 665–682. [27] J. Bright, R. Desikan, J.T. Hancock, I.S. Weir, S.J. Neill, ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis, Plant J. 45 (2006) 113–122. [28] W. Ye, M.A. Hossain, S. Munemasa, Y. Nakamura, I.C. Mori, Y. Murata, Endogenous abscisic acid is involved in methyl jasmonate-induced reactive oxygen species and nitric oxide production but not in cytosolic alkalization in Arabidopsis guard cells, J. Plant Physiol. 170 (2013) 1212–1215. [29] J. Liu, Z. Hou, G. Liu, L. Hou, X. Liu, Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L, J. Integr. Agric. 11 (2012) 1644–1653. [30] R. Alcázar, J.C. Cuevas, M. Patron, T. Altabella, A.F. Tiburcio, Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana, Physiol. Plant. 128 (2006) 448–455. [31] T. Boller, G.A. Felix, Renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors, Annu. Rev. Plant Biol. 60 (2009) 379–406. [32] J.W. Wang, L.P. Zheng, R.X. Tan, Involvement of nitric oxide in cerebrosideinduced defense responses and taxol production in Taxus yunnanensis suspension cells, Appl. Microbiol. Biotechnol. 75 (2007) 1183–1190. [33] N. Raho, L. Ramirez, M.L. Lanteri, G. Gonorazky, L. Lamattina, A. tenHave, et al., Phosphatidic acid production in chitosan-elicited tomato cells, via both

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43]

[44]

[45] [46]

[47] [48]

[49]

[50]

[51]

[52]

[53]

[54]

[55]

[56] [57]

[58]

[59]

[60]

phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide, J. Plant Physiol. 168 (2011) 534–539. O. Lamotte, K. Gould, D. Lecourieux, A. Sequeira-Legrand, A. Lebrun-Garcia, J. Durner, et al., Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein, Plant Physiol. 135 (2004) 516–529. M.J. Xu, J.F. Dong, M.Y. Zhu, Involvement of NO in fungal elicitor-induced activation of PAL and stimulation of taxol synthesis in Taxus chinensis suspension cells, Chin. Sci. Bull. 49 (2004) 1038–1043. M.J. Xu, J.F. Dong, M.Y. Zhu, Nitric oxide mediates the fungal elicitor-induced puerarin biosynthesis in Pueraria thomsonii Benth. suspension cells through a salicylic acid (SA)-dependent and a jasmonic acid (JA)-dependent signal pathway, Sci. China C. Life Sci. 49 (2006) 379–389. M. Xu, J. Dong, Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells, Appl. Microbiol. Biotechnol. 67 (2005) 40–44. M.J. Xu, J.F. Dong, M.Y. Zhu, Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid dependent signal pathway, Plant Physiol. 139 (2005) 991–998. L.V. Modolo, F.Q. Cunha, M.R. Braga, I. Salgado, Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f. sp. meridionalis elicitor, Plant Physiol. 130 (2002) 1289–1297. J.W. Wang, J.Y. Wu, Involvement of nitric oxide in elicitor-induced defense responses and secondary metabolism of Taxus chinensis cells, Nitric Oxide 11 (2004) 298–306. A. Yamamoto, S. Katou, H. Yoshioka, N. Doke, K. Kawakita, Involvement of nitric oxide generation in hypersensitive cell death induced by elicitin in tobacco cell suspension culture, J. Gen. Plant Pathol. 70 (2004) 85–92. S. Saito, A. Yamamoto-Katou, H. Yoshioka, N. Doke, K. Kawakita, Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells, Plant Cell Physiol. 47 (2006) 689–697. D. Zeidler, U. Zähringer, I. Gerber, I. Dubery, T. Hartung, W. Bors, et al., Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes, Proc. Natl Acad. Sci. U.S.A. 101 (2004) 15811–15816. X.M. Zhao, X.P. She, W. Yu, X.M. Liang, Y.G. Du, Effects of oligochitosans on tobacco cells and role of endogenous nitric oxide burst in the resistance of tobacco to tobacco mosaic virus, J. Plant Pathol. 89 (2007) 55–65. X. Hu, S.J. Neill, W. Cai, Z. Tang, Nitric oxide mediates elicitor-induced saponin synthesis in cell cultures of Panax ginseng, Funct. Plant Biol. 30 (2003) 901–907. L.P. Zheng, B. Zhang, T. Zou, Z.H. Chen, J.W. Wang, Nitric oxide interacts with reactive oxygen species to regulate oligosaccharide-induced artemisinin biosynthesis in Artemisia annua hairy roots, J. Med. Plant Res. 4 (2010) 758–765. M.L. Lanteri, L. Lamattina, Mechanisms of xylanase-induced nitric oxide and phosphatidic acid production in tomato cells, Planta 234 (2011) 845–855. J. Zhao, K. Fujita, K. Sakai, Reactive oxygen species, nitric oxide, and their interactions play different roles in Cupressus lusitanica cell death and phytoalexin biosynthesis, New Phytol. 175 (2007) 215–229. H. Zhang, M. Wang, W. Wang, D. Li, Q. Huang, Y. Wang, et al., Silencing of G proteins uncovers diversified plant responses when challenged by three elicitors in Nicotiana benthamiana, Plant Cell Environ. 35 (2012) 72–85. H. Zhang, Q. Fang, Z. Zhang, Y. Wang, X. Zheng, The role of respiratory burst oxidase homologues in elicitor-induced stomatal closure and hypersensitive response in Nicotiana benthamiana, J. Exp. Bot. 60 (2009) 3109–3122. N. Srivastava, V.K. Gonugunta, M.R. Puli, A.S. Raghavendra, Nitric oxide production occurs downstream of reactive oxygen species in guard cells during stomatal closure induced by chitosan in abaxial epidermis of Pisum sativum, Planta 229 (2009) 757–765. V.K. Gonugunta, N. Srivastava, A.S. Raghavendra, Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan, Plant Signal. Behav. 4 (2009) 561–564. S. Lee, H. Choi, S. Suh, I.S. Doo, K.Y. Oh, E.J. Choi, et al., Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis, Plant Physiol. 121 (1999) 147–152. Y. Li, H. Yin, Q. Wang, X. Zhao, Y. Du, F. Li, Oligochitosan induced Brassica napus L. production of NO and H2O2 and their physiological function, Carbohydr. Polym. 75 (2009) 612–617. M.A.R. Khokon, M.A. Hossain, S. Munemasa, M. Uraji, Y. Nakamura, I.C. Mori, et al., Yeast elicitor-induced stomatal closure and peroxidase-mediated ROS production in Arabidopsis, Plant Cell Physiol. 51 (2010) 1915–1921. S. Hou, C. Zhang, Y. Yang, D. Wu, Recent advances in plant immunity: recognition, signaling, response, and evolution, Biol. Plant. 57 (2013) 11–25. C. García-Mata, L. Lamattina, Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress, Plant Physiol. 126 (2001) 1196–1204. J. Xiong, G. Fu, Y. Yang, C. Zhu, L. Tao, Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research?, J. Exp. Bot. 63 (2012) 33– 41. R. Desikan, R. Griffiths, J. Hancock, S. Neill, A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana, Proc. Natl Acad. Sci. U.S.A. 99 (2002) 16314–16318. V.K. Gonugunta, N. Srivastava, M.R. Puli, A.S. Raghavendra, Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid, Plant Cell Environ. 31 (2008) 1717–1724.

Please cite this article in press as: Srinivas Agurla, Gunja Gayatri, Agepati S. Raghavendra, Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens, Nitric Oxide (2014), doi: 10.1016/j.niox.2014.07.004

ARTICLE IN PRESS S. Agurla et al./Nitric Oxide ■■ (2014) ■■–■■

[61] X. Liu, W. Shi, S. Zhang, C. Lou, Involvement of nitric oxide in the signal transduction of salicylic acid regulating stomatal movement, Chin. Sci. Bull. 48 (2003) 449–452. [62] X. Liu, W. Shi, S. Zhang, C. Lou, Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L, Chin. Sci. Bull. 50 (2005) 520–525. [63] S.J. Neill, R. Desikan, A. Clarke, J.T. Hancock, Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells, Plant Physiol. 128 (2002) 13–16. [64] E. Planchet, W.M. Kaiser, Nitric oxide (NO) detection by DAF fluorescence and chemiluminescence: a comparison using abiotic and biotic NO sources, J. Exp. Bot. 57 (2006) 3043–3055. [65] A.M. Distéfano, C. García-Mata, L. Lamattina, A.M. Laxalt, Nitric oxide-induced phos phatidic acid accumulation: a role for phospholipases C and D in stomatal closure, Plant Cell Environ. 31 (2008) 187–194. [66] A.M. Distéfano, M.L. Lanteri, A. tenHave, C. García-Mata, L. Lamattina, A.M. Laxalt, Nitric oxide and phosphatidic acid signaling in plants, Plant Cell Monogr. 16 (2010) 223–242. [67] Y. Zhang, H. Zhu, Q. Zhang, M. Li, M. Yan, R. Wang, et al., Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis, Plant Cell 21 (2009) 2357–2377. [68] M. Uraji, T. Katagiri, E. Okuma, W. Ye, M.A. Hossain, C. Masuda, et al., Cooperative function of PLDδ and PLDα1 in abscisic acid induced stomatal closure in Arabidopsis, Plant Physiol. 159 (2012) 450–460. [69] F. Hao, S. Zhao, H. Dong, H. Zhang, L. Sun, C. Miao, Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis, J. Integr. Plant Biol. 52 (2010) 298–307. [70] G. Manjunatha, S.N. Raj, S. Nandini, H.S. Shetty, Nitric oxide donor seed priming enhances defense responses and induces resistance against pearl millet downy mildew disease, Pestic. Biochem. Physiol. 91 (2008) 1–11. [71] A. Sun, S. Nie, D. Xing, Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides, Plant Physiol. 160 (2012) 1081–1096. [72] L.R. Sun, F.S. Hao, B.S. Lu, L.Y. Ma, AtNOA1 modulates nitric oxide accumulation and stomatal closure induced by salicylic acid in Arabidopsis, Plant Signal. Behav. 5 (2010) 1022–1024. [73] J. Liu, L.X. Hou, G.H. Liu, X. Liu, X.C. Wang, Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana, Chin. Sci. Bull. 56 (2011) 3547–3553. [74] S. Munemasa, I.C. Mori, Y. Murata, Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells, Plant Signal. Behav. 6 (2011) 939–941. [75] M.A.R. Khokon, M. Uraji, S. Munemasa, E. Okuma, Y. Nakamura, I.C. Mori, et al., Chitosan-induced stomatal closure accompanied by peroxidase-mediated reactive oxygen species production in Arabidopsis, Biosci. Biotechnol. Biochem. 74 (2010) 2313–2315. [76] Y. Wang, G.J. Loake, C. Chu, Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death, Front. Plant Sci. 4 (2013) 1–7. [77] S. Rasul, C. Dubreuil-Maurizi, O. Lamotte, E. Koen, B. Poinssot, G. Alcaraz, et al., Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana, Plant Cell Environ. 35 (2012) 1483–1499. [78] E. Vandelle, B. Poinssot, D. Wendehenne, M. Bentejac, A. Pugin, Integrated signalling network involving calcium, nitric oxide, and active oxygen species but not mitogen activated protein kinases in BcPG1-elicited grapevine defenses, Mol. Plant Microbe Interact. 19 (2006) 429–440. [79] R. Ali, W. Ma, F. Lemtiri-Chlieh, D. Tsaltas, Q. Leng, S. von Bodman, et al., Death don’t have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel2 and innate immunity, Plant Cell 19 (2007) 1081–1095. [80] S. Asai, K. Ohta, H. Yoshioka, MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana, Plant Cell 20 (2008) 1390–1406. [81] A. Kulik, E. Noirot, V. Grandperret, S. Bourque, J. Fromentin, P. Salloignon, et al., Interplays between nitric oxide and reactive oxygen species in cryptogein signaling, Plant Cell Environ. (2014) . [82] A.P. Ortega-Galisteo, M. Rodríguez-Serrano, D.M. Pazmiño, D.K. Gupta, L.M. Sandalio, M.C. Romero-Puertas, S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress, J. Exp. Bot. 63 (2012) 2089–2103. [83] E. Vandelle, M. Delledonne, Peroxynitrite formation and function in plants, Plant Sci. 181 (2011) 534–539. [84] B.W. Yun, A. Feechan, M. Yin, N.B. Saidi, T.L. Bihan, M. Yu, et al., S-nitrosylation of NADPH oxidase regulates cell death in plant immunity, Nature 478 (2011) 264–268. [85] M. Lisjak, N. Srivastava, T. Teklic, L. Civale, K. Lewandowski, I. Wilson, et al., A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation, Plant Physiol. Biochem. 48 (2010) 931–935. [86] M. Lisjak, T. Teklic, I.D. Wilson, M. Wood, M. Whiteman, J.T. Hancock, Hydrogen sulfide effects on stomatal apertures, Plant Signal. Behav. 6 (2011) 1–3. [87] C. García-Mata, L. Lamattina, Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling, New Phytol. 188 (2010) 977–984. [88] E. Bloem, S. Haneklaus, I. Salac, P. Wickenhauser, E. Schnug, Facts and fiction about sulfur metabolism in relation to plant-pathogen interactions, Plant Biol. 9 (2007) 596–607.

7

[89] A. Calderwood, S. Kopriva, Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule, Nitric Oxide (2014) . [90] B.A. Halkier, J. Gershenzon, Biology and biochemistry of glucosinolates, Annu. Rev. Plant Biol. 57 (2006) 303–333. [91] J. Li, H. Jia, J. Wang, Q. Cao, Z. Wen, Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root, Protoplasma 251 (2013) 899–912. doi:10.1007/ s00709-013-0592-x. [92] E. Baudouin, P. Frendo, M.L. Gleuher, A. Puppo, A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules, J. Exp. Bot. 55 (2004) 43–47. [93] C.Z. Yu, H.B. Kai, W.Q. Ya, X. Wei, L.T. Fang, Z. Bo, et al., Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway, Chin. Sci. Bull. 52 (2007) 2365–2373. [94] K.J. Gupta, A.U. Igamberdiev, G. Manjunatha, S. Segu, J.F. Moran, B. Neelawarne, et al., The emerging roles of nitric oxide (NO) in plant mitochondria, Plant Sci. 181 (2011) 520–526. [95] N.N. Tun, C. Santa-Catarina, T. Begum, V. Silveira, W. Handro, E.I.S. Floh, et al., Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings, Plant Cell Physiol. 47 (2006) 346–354. [96] D. Lu, J. Dong, H. Jin, L. Sun, X. Xu, T. Zhou, et al., Nitrate reductase-mediated nitric oxide generation is essential for fungal elicitor induced camptothecin accumulation of Camptotheca acuminata suspension cell cultures, Appl. Microbiol. Biotechnol. 90 (2011) 1073–1081. [97] E. Planchet, K.J. Gupta, M. Sonoda, W.M. Kaiser, Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport, Plant J. 41 (2005) 732– 743. [98] A. Besson-Bard, A. Pugin, D. Wendehenne, New insights into nitric oxide signaling in plants, Annu. Rev. Plant Biol. 59 (2008) 21–39. [99] P. Rockel, F. Strube, A. Rockel, J. Wildt, W.M. Kaiser, Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro, J. Exp. Bot. 53 (2002) 103–110. [100] M.G. Zhao, L. Chen, L.L. Zhang, W.H. Zhang, Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis, Plant Physiol. 151 (2009) 755–767. [101] C. Stöhr, F. Strube, G. Marx, W.R. Ullrich, P. Rockel, A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite, Planta 212 (2001) 835–841. [102] C. Stöhr, S. Stremlau, Formation and possible roles of nitric oxide in plant roots, J. Exp. Bot. 57 (2006) 463–470. [103] R. Harrison, Structure and function of xanthine oxidoreductase: where are we now?, Free Radic. Biol. Med. 33 (2002) 774–797. [104] B.L.J. Godber, J.J. Doel, G.P. Sapkota, D.R. Blake, C.R. Stevens, R. Eisenthal, et al., Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase, J. Biol. Chem. 275 (2000) 783–792. [105] J.L. Zweier, A. Samouilove, P. Kuppusamy, Non-enzymatic nitric oxide synthesis in biological systems, Biochim. Biophys. Acta 1411 (1999) 250–262. [106] P.C. Bethke, M.R. Badger, R.L. Jones, Apoplastic synthesis of nitric oxide by plant tissues, Plant Cell 16 (2004) 332–341. [107] S. Sokolovski, M.R. Blatt, Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells, Plant Physiol. 136 (2004) 4275–4284. [108] M.C. Romero-Puertas, M. Perazzolli, E.D. Zago, M. Delledonne, Nitric oxide signaling functions in plant-pathogen interactions, Cell. Microbiol. 6 (2004) 795–803. [109] J.T. Hancock, R. Desikan, A. Clarke, R.D. Hurst, S.J. Neill, Cell signalling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species, Plant Physiol. Biochem. 40 (2002) 611–617. [110] M.P. Murphy, Nitric oxide and cell death, Biochim. Biophys. Acta 1411 (1999) 401–414. [111] G.P. Bolwell, Role of active oxygen species and NO in plant defense responses, Curr. Opin. Plant Biol. 2 (1999) 287–294. [112] M. Delledonne, I. Murgia, D. Ederle, P.F. Sbicego, A. Biondani, A. Polverari, et al., Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease-resistance response, Plant Physiol. Biochem. 40 (2002) 605–610. [113] D. Bellin, S. Asai, M. Delledonne, H. Yoshioka, Nitric oxide as a mediator for defense responses, Mol. Plant Microbe Interact. 26 (2013) 271–277. [114] A. Feechan, E. Kwon, B.W. Yun, Y. Wang, J.A. Pallas, G.J. Loake, A central role for S-nitrosothiols in plant disease resistance, Proc. Natl Acad. Sci. U.S.A. 102 (2005) 8054–8059. [115] M. Yu, L. Lamattina, S.H. Spoel, G.J. Loake, Nitric oxide function in plant biology: a redox cue in deconvolution, New Phytol. 202 (2014) 1142–1156. [116] Z. Mou, W. Fan, X. Dong, Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes, Cell 113 (2003) 935–944. [117] J. Astier, S. Rasul, E. Koen, H. Manzoor, A. Besson-Bard, O. Lamotte, et al., S-nitrosylation: an emerging post-translational protein modification in plants, Plant Sci. 181 (2011) 527–533. [118] J. Astier, A. Kulik, E. Koen, A. Besson-Bard, S. Bourque, S. Jeandro, et al., Protein S-nitrosylation: what’s going on in plants?, Free Radic. Biol. Med. 53 (2012) 1101–1110.

Please cite this article in press as: Srinivas Agurla, Gunja Gayatri, Agepati S. Raghavendra, Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens, Nitric Oxide (2014), doi: 10.1016/j.niox.2014.07.004