REVIEW

Nitric oxide as a key component in hormone-regulated processes

Marcela Simontacchi • Carlos Garcı́a-Mata •

Carlos G. Bartoli • Guillermo E. Santa-Marı́a •

Lorenzo Lamattina

Received: 29 December 2012 / Revised: 21 March 2013 / Accepted: 21 March 2013 / Published online: 13 April 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract Nitric oxide (NO) is a small gaseous molecule,

with a free radical nature that allows it to participate in a

wide spectrum of biologically important reactions. NO is

an endogenous product in plants, where different biosyn-

thetic pathways have been proposed. First known in ani-

mals as a signaling molecule in cardiovascular and nervous

systems, it has turned up to be an essential component for a

wide variety of hormone-regulated processes in plants.

Adaptation of plants to a changing environment involves a

panoply of processes, which include the control of CO2

fixation and water loss through stomatal closure, rear-

rangements of root architecture as well as growth restric-

tion. The regulation of these processes requires the

concerted action of several phytohormones, as well as the

participation of the ubiquitous molecule NO. This review

analyzes the role of NO in relation to the signaling

pathways involved in stomatal movement, plant growth

and senescence, in the frame of its interaction with abscisic

acid, auxins, gibberellins, and ethylene.

Keywords Abscisic acid � Auxins � Ethylene �
Gibberellins � Nitric oxide

Introduction

For many years, nitric oxide (NO) was identified as a

component of polluted air and blamed for exerting toxic

effects over photosynthesis and plant growth (Clyde Hill

and Bennett 1970). Plants can itself produce NO, in addi-

tion to respond to that offered by the environment, as it was

first observed in soybean (Klepper 1979).

Two centuries after its discovery in 1772, NO burst onto

the scene associated with important functions in vascula-

ture and nervous system in animals (Culotta and Koshland

1992). The identification of biological targets and functions

of NO in mammals led to investigate whether or not NO

was implicated in physiological processes that take place in

plants. It was soon described that NO participates in mat-

uration and senescence, in addition to being an essential

component in plant responses against biotic stress

(Delledonne et al. 1998; Durner et al. 1998; Leshem et al.

1998). Since then, it has become evident that reactive

intermediates and free radicals, formerly considered toxic

compounds, constitute in fact important endogenous sig-

nals in cellular metabolism (Delledonne et al. 1998; Durner

et al. 1998; Crawford 2006; Foyer and Noctor 2009), and

that they participate in the modulation of hormonal

responses (Lamattina et al. 2003; Wendehenne et al. 2004;

Bartoli et al. 2012) regulating plant growth and develp-

mental processes (Correa-Aragunde et al. 2007).

Communicated by P. Kumar.

A contribution to the Special Issue: Plant Hormone Signaling.

M. Simontacchi (&) � C. G. Bartoli

Instituto de Fisiologı́a Vegetal (INFIVE) CC327, Universidad

Nacional de La Plata-CONICET, Diagonal 113 y calle 61 N�495,

CP 1900 La Plata, Buenos Aires, Argentina

e-mail: marcelasimontacchi@agro.unlp.edu.ar

C. Garcı́a-Mata � L. Lamattina

Instituto de Investigaciones Biológicas,

Universidad Nacional de Mar del Plata-CONICET,

7600 Mar del Plata, Buenos Aires, Argentina

G. E. Santa-Marı́a

Instituto Tecnológico Chascomús (IIB-INTECH), CONICET,

Camino Circunvalación Laguna Km 8.5, 7130 Chascomús,

Buenos Aires, Argentina

123

Plant Cell Rep (2013) 32:853–866

DOI 10.1007/s00299-013-1434-1



NO in a biological environment: target molecules

and effects

NO is a small, uncharged, scarcely polar molecule, thus

freely diffuses across membranes from one compartment to

the other. From a chemical point of view it is a free radical,

with an unpaired electron which makes it paramagnetic and

allows its detection by employing electron paramagnetic

resonance (Puntarulo et al. 2010).

In biological systems, NO has a low steady state con-

centration determined by the rates of synthesis and decay

reactions. In hydrophobic environments, such as biomem-

branes, NO reacts with radical species, acting as antioxi-

dant and breaking lipid peroxidation processes (Rubbo

et al. 2000; O’Donnell and Freeman 2001).

Biologically important reactions of NO involve those

with, (a) transition metal ions, including those found in

metalloproteins, (b) free radicals, such as superoxide anion

(O2
-) and intermediates in lipid peroxidation, and (c) thiols

groups present in proteins and peptides (Fig. 1).

Regarding the reactions between NO and transition

metals, they constitute an important mechanism to modu-

late the activity of proteins, being the activation of soluble

guanylate cyclase (sGC) the most studied example (Ignarro

et al. 1984). Research performed in plants showed that NO

induces a transient increase in endogenous cGMP con-

centrations (Durner et al. 1998; Neill et al. 2003). In

addition, inhibitors of sGC block the NO-induced activa-

tion of both the expression of phenylalanine ammonia-

lyase (PAL) genes and enzyme activity (Durner et al.

1998). Auxin responses during the adventitious root for-

mation include NO/cGMP signaling as it is discussed later.

Other regulatory properties of NO which involve post-

translational modification of proteins are exerted through

S-nitrosylation (also named as S-nitrosation) of thiol groups

and nitration of tyrosine residues (Table 1). As a whole,

NO-mediated protein modifications constitute the basis for

NO signaling.

The reaction between NO and O2
-, is among the fastest

biological reactions (k = 4–16 9 109 M-1 s-1, Huie and

Padmaja 1993), and leads to the formation of a short-lived

strong oxidant, peroxynitrite (Ischiropoulos et al. 1992).

This reaction establishes a link between reactive oxygen

and nitrogen species metabolism (Wink and Mitchell

1998). In plants, the simultaneous generation of O2
- and

NO has a synergistically function in defense responses

(Asai et al. 2008), as well as in plants exposed to abiotic

stress (Tanou et al. 2009).

Nitration, consisting in the addition of a nitro group

(–NO2) into a protein tyrosine residue, can alter protein

function and is considered a molecular footprint of per-

oxynitrite presence in cells (Radi 2004). Detection of

nitrated proteins has been reported in several species under

physiological or stress conditions (Morot-Gaudry-Talar-

main et al. 2002; Saito et al. 2006; Romero-Puertas et al.

2007; Bechtold et al. 2009; Chaki et al. 2009; Jasid et al.

2009). Among the proteins prone to be modified by nitra-

tion Rubisco activase, ATP synthase subunit a, and glu-

tamine synthetase 2 in pathogen-challenged Arabidopsis

have been described (Cecconi et al. 2009; Lozano-Juste

et al. 2011). In chloroplasts, tyrosine nitration sites have

been also identified, mainly in PSI, PSII, cytochrome b6/f

and ATP synthase complex (Galetskiy et al. 2011).

As mentioned above, other important mechanism

through which NO exerts its effects is by means of S-nit-

rosylation of sulfhydryl centers (Lamotte et al. 2006). The

NO carrier S-nitrosoglutathione (GSNO) is an excellent

nitrosating agent, which can transfer the NO? group to a

variety of nucleophiles (Hughes 1999; Stamler et al. 2001).

The level of GSNO in vivo depends on both NO synthesis

Fig. 1 NO metabolism and targets. NO steady state concentration in

cells is determined by its production (diffusion from external sources,

synthesis and release from storage compounds) and consumption

(chemical reactions, GSNOR activity, diffusion). The broader chem-

istry of NO involves two interrelated redox forms, apart from NO

radical: nitrosonium cation (NO?) and nitroxyl anion (NO-), which

can be found in living systems (Hughes 1999). Low molecular iron-

nitrosyl complexes and S-nitrosothiols are proposed as NO? carriers

and donors in biological systems (Ramirez et al. 2011) buffering the

concentration of free NO (Stamler et al. 1992). The enzyme GSNOR

metabolizes GSNO to glutathione sulphinamide as main product

(Jensen et al. 1998). Regulatory effects of NO are mediated by

reversible Cys-nitrosylation of proteins (e.g., auxin receptor TIR1,

and ion channel proteins), metal nitrosylation of enzymes (e.g.,

activation of sGC), and Tyr-nitration of proteins (e.g., cytochrome c,

and Mn-SOD). A signaling role for nitroalkenes and nitroalkene thiol

adducts on transcription factors has been proposed in animals (Rubbo

and Radi 2008)

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and GSNO turnover, which is performed by the activity of

the enzyme nitrosoglutathione reductase (GSNOR) (Barr-

oso et al. 2006). Thus, GSNOR activity regulates the global

level of S-nitrosylation in plants (Feechan et al. 2005;

Malik et al. 2011).

Studies on S-nitrosylated proteins in Arabidopsis thali-

ana leaves and tobacco cells suggested that S-nitrosylation

is a specific and regulated event (Lyndermayr et al. 2005;

Lyndermayr and Durner 2009; Astier et al. 2011; 2012).

S-nitrosylation of the auxin receptor TIR1 imposed by

NO constitute a relevant example of post-translational

modification with high impact in biological functions

(Terrile et al. 2012).

Some effects of NO in plant cells are exerted through

the second messenger Ca2? (Gould et al. 2003). Changes in

free cytosolic Ca2?, and its release from specific intracel-

lular stores, induced by NO have been described in dif-

ferent plant species exposed to elicitors or treated with

exogenous NO (Lecourieux et al. 2002). In tobacco cells,

treatment with cryptogein or the NO donor diethylamine

NONOate promoted an increase in cytosolic free Ca2?

concentration, involving phosphorylation events (Lamotte

Table 1 Examples of NO-related post-translational modification in plant proteins

Protein Description References

Glyceraldehyde-3-phosphate dehydrogenase S-nitrosylation

A. thaliana

Reversible inhibition

Lyndermayr et al. (2005)

Methionine adenosyltransferase (MAT) S-nitrosylation

A. thaliana

Inhibition of activity

Lyndermayr et al. (2006)

Ribulose 1,5 bisphophate carboxylase/oxygenase RUBISCO S-nitrosylation

B. juncea and K. pinnata

Inhibition of activity

Abat and Deswal (2009);

Abat et al. (2008)

Auxin receptor TIR1/AFB S-nitrosylation

A. thaliana

Enhances TIR1-Aux/IAA interaction

Terrile et al. (2012)

Salicylic acid-binding protein AtSABP3 S-nitrosylation

A. thaliana

Inhibition of activity and SA binding

Wang et al. (2009)

Glycolate oxidase S-nitrosylation

P. sativum

Peroxisomes exposed to abiotic stress

Ortega-Galisteo et al. (2012)

Dehydroascorbate reductase S-nitrosylation

Solanum tuberosum

Inhibition of activity

Kato et al. (2012)

Ferredoxin–NADP reductase Tyr-nitration

Helianthus annuus

Inhibition of activity

Chaki et al. (2011)

Methionine synthase Tyr-nitration

Arabidopsis

Inhibition of activity

Lozano-Juste et al. (2011)

Glyceraldehyde-3-phosphate dehydrogenase Tyr-nitration

A. thaliana

Inhibition of activity

Lozano-Juste et al. (2011)

NADP-isocitrate dehydrogenase Tyr-nitration

P. sativum

Inhibition of activity

Begara-Morales et al. (2013)

PSI and PSII proteins Tyr-nitration

A. thaliana

Regulate the stability and turnover

Galetski et al. (2011)

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et al. 2004). In this line of evidence, it was also observed in

N. plumbaginifolia that NO induces an increase of Ca2?

through the activation of protein kinases (Lamotte et al.

2006). Interestingly, Calcium and calcium-dependent pro-

tein kinases (CDPKs) are involved in the auxin-NO cross-

talk regulation of adventitious root formation (Lanteri et al.

2006). In addition, ABA-mediated stomatal closure

includes NO-dependent Ca2? mobilization as it is dis-

cussed later.

Finally, the pattern of gene expression can be affected

by NO level in plants (Grün et al. 2006). In A. thaliana,

changes in the expression profiles were analyzed following

infiltration with the NO donor sodium nitroprusside (SNP).

More than 100 genes showed altered expression patterns

with SNP treatment, which belong to the functional cate-

gories of signal transduction, defense or cell death, reactive

oxygen species (ROS) generation and removal, photosyn-

thetic processes, cellular trafficking, and basic metabolism

(Polverari et al. 2003). Other studies disclosed that NO-

regulated genes in plants include enzymes involved in

jasmonic acid (JA) and ethylene synthesis, enzymes of

phenylpropanoid synthesis, auxin-responsive proteins as

well as enzymes involved in glutathione synthesis

(Wendehenne et al. 2004; Innocenti et al. 2007). Interest-

ingly, a microarray analysis performed for Arabidopsis

plants exposed to the NO donor SNP indicated that 10 % of

genes that respond to NO treatment are transcription fac-

tors (Parani et al. 2004). As mentioned above, NO likely

exerts its effects on gene expression imposing post-trasla-

tional modifications of transcription factors, regulatory

proteins or nuclear proteins through S-nitrosylation of

cysteine residues, tyrosine nitration, and metal nitrosyla-

tion (Lyndermayr et al. 2005; Grün et al. 2006; Serpa et al.

2007; Corpas et al. 2010).

A new biochemical pathway for NO catabolism was

described based on the reaction with the plant hormone

cytokinin. In addition, this finding represents a novel

mechanism for NO-hormone interaction (Liu et al. 2013).

In the following sections, we describe some examples

highlighting the role of NO as a mediator in hormone-

regulated processes in plants (Fig. 2). Likely they represent

only a small portion of the processes that take place in

higher plants, particularly when they are exposed to envi-

ronmental challenges, involving a cross-talk between NO

and hormones. The selected examples describe events with

great biological importance.

ABA says NO to stomatal opening and plant water loss

Stomata are pores formed by two differentiated cells

named guard cells located in the epidermis of terrestrial

plants. The opening of the stomatal pore is finely regulated

to facilitate CO2 uptake, for CO2 fixation during photo-

synthesis and to avoid transpirational water loss.

Therefore, optimal photosynthesis and water manage-

ment by plants rely on an exquisite integration of several

inputs linking signaling molecules and second messengers

coming from different, circumstantial, and dynamical plant

requirements.

Environmental parameters such as light, CO2 levels,

humidity, soil water status and biotic stresses regulate

stomatal aperture (Assmann 1993; Hetherington and

ABA ↑ [Ca2+]

GC/cGMP

PP2C

PLC/PLD 

GAs Ethylene

Auxins

NO

NO

NONO

Stomatal
closure

DELLAs

Growth Senescence

respiration

ROS generation

Changes in 
root

morphology

↑ [Ca2+]

cADPR

CDPKs

GC/cGMP

MAPK

PLD

↑ auxin-

dependent

gene 

expression

↑ Fe adquisition

genes

Fig. 2 NO and hormone-regulated processes. Schematic represen-

tation of NO acting as a regulatory molecule in ABA, GAs, ethylene

and auxin-mediated processes. ABA increases NO level in guard cells

and several targets or effectors downstream NO were identified in

ABA-mediated stomatal closure. An interplay between NO and GAs

through DELLAs pathway is currently suggested. Ethylene and NO

exert opposite effects over senescence, as well as postharvest

conservation of plant products. In roots auxins presence led to an

increase in NO levels, and both NR and NOS-like activities were

described as NO sources (Abu-Abied et al. 2012; Jin et al. 2011).

Several effectors acting downstream NO were identified mediating

changes in root architecture. ABA abscisic acid, cADRP cyclic ADP-

ribose, CDPKs calcium-dependent protein kinases, cGMP cyclic

guanosine monophosphate, GAs, gibberellins, MAPK mitogen-acti-

vated protein kinase, NO nitric oxide, NOS nitric oxide synthase, NR
nitrate reductase, PLC phospholipase C, PLD phospholipase D, PP2C
protein phosphatase 2C, ROS reactive oxygen species, sGC soluble

guanylate cyclase

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Woodward 2003; Schroeder et al. 2001). In addition,

endogenous stimuli under the control of plant hormones

influence the stomatal aperture. The size of the stomatal

pore depends on variations of the turgor that results in

volume changes of the guard cells (Blatt 2000). Guard cells

lack plasmodesmata; therefore, transport across plasma

membrane and the modulation of ion channel activity play

key roles determining the entrance and sorting of osmoti-

cally active solutes (Blatt 2000; Schroeder et al. 2001).

Stomatal guard cells are acknowledged as a model

system for the study of signal transduction in plants. The

best-characterized response is that generated by the phy-

tohormone ABA. When ABA molecules reach guard cell,

the surface is internalized by the ABC transporter At

ABCG40 (Kang et al. 2010). Once sensed by the PYR/

PYL/RCAR receptor, ABA triggers a complex signaling

network that results in a reduction of the guard cell turgor

pressure and the closure of the stomatal pore (Blatt 2000;

Schroeder et al. 2001). Some of the key steps in this net-

work are: (a) the inactivation of plasma membrante H?-

ATPase, (b) cytoplasmatic Ca2? increases, and (c) plasma

membrane anion channel activation (both rapid and slow

anion channels) (Kim et al. 2010). Anion efflux generates

and maintains a depolarization of the guard cell plasma

membrane which in turn promotes K? efflux through the

activation of the outward rectifying K? channels and

reduces K? influx through the deactivation of inward-rec-

tifying K? channels, resulting in a net loss of solutes and

the concomitant reduction of turgor pressure and stomatal

closure (Kim et al. 2010; Dreyer and Uozumi 2011).

The first report on NO regulation of stomatal movement

showed that the NO donor SNP-induced stomatal closure in

three different plant species Vicia faba, Salpichroa or-

ganifolia, and Tradescantia spp. (Garcı́a-Mata and La-

mattina 2001). Soon after, NO was linked to guard cells

ABA-dependent signaling network. Two independent

works used the NO-detection fluorescent probe DAF-2 DA

to show that ABA induces endogenous NO production in

Pisum sativum and Vicia faba (Garcı́a-Mata and Lamattina

2002; Neill et al. 2002). It was also demonstrated that the

NO scavenger cPTIO blocks ABA-dependent stomatal

closure, supporting that NO is required for the ABA-reg-

ulated signaling pathway leading to stomatal closure

(Garcı́a-Mata and Lamattina 2002; Neill et al. 2002).

Further studies showed that AtrboHD and AtrboHF-medi-

ated ROS production, recognized as an early event in

ABA-signaling networks, are required for endogenous NO

production (Bright et al. 2006) indicating that ROS are

upstream of NO in ABA-dependent stomatal closure.

Several targets of NO have been identified within ABA-

regulated guard cell signaling. It has been reported that NO

deactivates inward-rectifying K? channels and activates

anion channels, contributing to the loss of the turgor

pressure that precedes stomatal closure (Garcı́a-Mata et al.

2003). Both of these ion channels are Ca2? dependent. In

this context, it has been also demonstrated that NO

increases guard cell cytoplasmic Ca2? concentration, in a

GC/cGMP-dependent manner via Ca2? release from

intracellular Ca2? stores (Garcı́a-Mata et al. 2003). Later it

was shown that the Ca2? insensitive outward rectifying

Ca2? channel GORK was also regulated by NO, possible

via the nitrosylation of the channel protein (Sokolovski and

Blatt 2004).

Another effector pointed out to interact with NO is the

protein phosphatase 2C (PPC2), which binds and stabilizes

the ABA-PYL/PYR/RCAR complex (Fujii et al. 2009; Ma

et al. 2009; Park et al. 2009; Santiago et al. 2009). It was

shown that, even though PP2C mutants abi1-1 and abi2-1

produced NO in response to ABA, they do not close the

stomata in response to NO, indicating that PP2C might be

downstream of NO (Desikan et al. 2002). It was recently

reported that NO interaction with ABI1 was also mediated

by the GC/cGMP pathway (Dubovskaya et al. 2011).

Another component reported to bind to and regulate

ABI1 is the phospholipid signal phosphatidic acid (PA)

(Jacob et al. 1999). PA is rapidly formed in response to

drought stress and it can be synthesized through two

independent ways: (a) from the hydrolysis of phosphati-

dylinositol 4,5-biphosphate (PIP2) in a reaction catalyzed

by phospholipase C (PLC), or (b) by phospholipase D

(PLD) which hydrolyzes structural phospholipids, such as

phosphatidilcholyne to PA and cholyne (Distéfano et al.

2008). ABA activates both PLC and PLD (Jacob et al.

1999; Staxen et al. 1999). In Arabidopsis guard cells, NO

induces the activity of both PLC and PLD, and the

inhibition of both enzymes resulted in a reduction of

ABA-dependent stomatal closure (Distéfano et al. 2008;

2012).

As was reported, ABA induces stomatal closure and

inhibits light-induced stomatal opening via two separate

signaling processes (Schroeder et al. 2001). Interestingly, it

was demonstrated that NO is required in ABA signaling

both for stomatal closure induction and for inhibition of

light-induced stomatal opening (Garcı́a-Mata and Lamat-

tina 2007; Zhang et al. 2007).

Despite the responses generated by ABA are the most

studied processes in guard cells, other hormones have been

reported to regulate stomatal movement under different

physiological conditions. Such is the case of ethylene (Liu

et al. 2010), methyl jasmonate (MeJA) (Saito et al. 2009),

cytokinins (Xiao-Ping and Xi-Gui 2006), auxins (Xiao-

Ping and Xi-Gui 2006), and salicylic acid (Hao et al. 2010).

Interestingly, NO seems to be a common second messenger

participating in all hormone-regulated signaling pathways

controlling stomatal aperture processes and plant gas

exchange with the environment.

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Interactions between NO and gibberellins: the DELLAs

pathway

A main role of plant hormones is to contribute to the

integration of the multiple exogenous and endogenous

signals perceived by plants. Integration of those signals

into a common pathway allows a coordinated growth and

developmental response, which is particularly relevant

when plants are exposed to environmental stresses and it

was undoubtedly a key element for the evolutionary suc-

cess of vascular plants in early land colonization. Research

performed over the last 15 years disclosed a pivotal role of

DELLA proteins, a subfamily of likely nuclear transcrip-

tional regulators, in the integration of hormonal responses

(Harberd et al. 2009; Sun 2011). Some mutant versions of

these proteins display an altered function that confer dwarf

or semidwarf phenotypes, being the later critical to

increase grain production during the green revolution

(Hedden 2003). In turn, plants carrying disruptions in

DELLA coding genes display a slender phenotype.

Detailed studies performed with Arabidopsis and crop

plants indicate that these proteins have the capacity to

repress plant growth. The growth restriction imposed by

them is commonly relieved by the action of gibberellins

(GAs) which, by interacting with GID1 receptors, bind

DELLAs and allow the recruitment of the GA-GID1-

DELLA module to the E3 ubiquitin ligase SLY1, thus

favoring DELLAs degradation at the proteasome and

subsequently promoting growth (Peng et al. 1999; Fu et al.

2002; Ueguchi-Tanaka et al. 2005).

Several lines of evidence suggest a possible interplay

between GAs and NO. Both regulators are known to

influence to a large list of common processes, among them:

hypocotyl elongation and plant responses to light (Peng

et al. 1999; Beligni and Lamattina 2000; Fu et al. 2004),

primary root growth (Correa-Aragunde et al. 2004; Fu and

Harberd 2003; Negi et al. 2010; Fernández-Marcos et al.

2011) as well as responses to several stresses, particularly

salinity (Achard et al. 2006; Bai et al. 2011). Some of these

responses also involve the interaction with other hormones,

which is clearly shown with auxins in the control of pri-

mary root growth (Fu and Harberd, 2003). Both DELLAs

and NO modulate the antioxidant response of plants

(Achard et al. 2008; Bai et al. 2011; Moriconi et al. 2012).

Interestingly, NO and GAs exert opposite effects in several,

but not all, of the physiological processes in which they

participate, suggesting that there is some degree of antag-

onism between them. Indirect evidence suggesting that

such antagonism could involve a differential effect of NO

and GAs on the DELLAs pathway was obtained early for

Hordeum vulgare aleurone layers. In this tissue, GAs-

induced programmed cell death (PCD) was delayed by the

addition of the NO donors SNP and S-nitroso-N-acetyl-DL-

penicillamine (SNAP) (Beligni et al. 2002). It was also

showed that in this plant species the expression of GAM-

YB, a GA-regulated transcriptional activator of a-amylase

expression was induced by GAs through the release of the

repression imposed by SLN1, the barley DELLAs homol-

ogous protein (Gubler et al. 2002). Since alternative

explanations could be advanced to explain those observa-

tions, it remains to be determined at what level NO inter-

feres with GA-induced signaling pathways including PCD

activation. A direct dissection of the interaction between

NO and the GA-GID1-DELLA module for a specific

physiological process has been only recently offered. As a

result of studies performed with nia1,2noa1-2 Arabidopsis

plants, which are deficient in NO accumulation, an ‘‘slen-

der-like’’ phenotype was observed when plants were grown

in white or red light but not in darkness, blue or far red

light (Lozano-Juste and León 2011). In turn, exogenously

applied NO led to an increase in the accumulation of

DELLAs proteins and shortened the hypocotyls as

observed in altered function phenotypes. These data are

consistent with the idea that endogenous NO levels regu-

late DELLAs accumulation and contribute to determine

hypocotyl length. The interaction between NO and DEL-

LAs in this particular phenomenon could be explained

because of an effect of NO on the steps that lead to

DELLAs turnover and activity. In this regard, it was

observed that NO promoted DELLAs accumulation

through negative modulation of SLY1, but also that NO

could eventually reduce the synthesis of GAs in a specific

pool by down regulating the GA20ox3 gene (Lozano-Juste

and León 2011). In addition, those authors observed that

NO generation was down regulated by GAs (Lozano-Juste

and León 2011), indicating the existence of a reciprocal

interaction between both regulators. It seems now evident

that NO and GAs could probably interact in other processes

where the GA-GID1-DELLA module is involved. In this

regard, recent studies indicated that the inhibitory effect of

SNP on Arabidopsis root elongation is partially reverted by

the addition of GAs being moderately diminished in plants

carrying a disruption in four of the five DELLA genes

(Fernández-Marcos et al. 2012). Interestingly, evidence for

a potentially opposite regulation has been reported in wheat

plants exposed to high aluminum concentrations. In this

case, the addition of SNP stimulates GAs accumulation and

subsequently apical root growth (He et al. 2012). These

apparently conflicting reports could be explained by dif-

ferences between Arabidopsis and wheat in the regulation

of root growth or by an interaction between NO and GAs

superimposed to the GA-GID1-DELLA module.

The usual pathway of DELLAs degradation involves the

contribution of GAs. However, evidence of GAs-indepen-

dent DELLAs degradation has been obtained. From the

three Arabidopsis GID1 proteins, it is thought that

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AtGID1B has the capacity to bind DELLAs in a GA-

independent mode (Sun 2011). Interestingly it has been

reported that transcript levels of AtGID1B are diminished

in the nia1,2noa1-2 mutant (Lozano-Juste and León 2011),

suggesting the possibility that NO could eventually mod-

ulate DELLAs stability through both GAs-dependent and

GAs-independent pathways.

These recent findings open an exciting perspective,

while posing important questions. One of them is to what

extent the antagonism between GAs and NO observed in

other processes also involves the GA-GID1-DELLA

module. Besides, it should be noted that while there is now

some knowledge about the way by which NO exerts its

effects on GAs signaling during the transition from dark-

ness to white light, the precise mode by which GAs mod-

ulate NO generation deserves to be further examined. In

this context, an additional question refers to the timing of

the evolutionary coalescence of NO signaling and the

DELLA-GID system. The last one probably became

functional during the early steps of vascular plant evolution

(Sun 2011; Depuydt and Hardtke 2011). As mentioned

above, there is some controversy on the identity and rela-

tive contribution of the pathways that participate in NO

synthesis in plants, being their evolutionary trend essen-

tially unknown. Further research on this subject could help

to understand how those two regulatory pathways became

under reciprocal control giving additional complexity and

flexibility to plant responses to multiple environmental

stimuli.

Role of NO in auxin-mediated processes

Among the broad spectrum of auxin-mediated effects in

plants, this section is focused on the role of auxins in root

morphology (Muday and Haworth 1994; Klerk et al. 1999)

and in plant responses to iron deficiency (Li and Li 2004).

The principal auxin receptors have been identified as

F-box protein components of an SCF ubiquitin E3 ligase

complex, belonging to the TIR1/AFB family (Dharmasiri

et al. 2005; Kepinski and Leyser 2005). Auxins stabilize

the formation of a heterodimer between TIR1/AFB and the

Aux/IAA repressor proteins, stimulating the degradation of

the transcriptional repressors Aux/IAA proteins through the

covalent addition of ubiquitin molecules (Tan et al. 2007).

Auxin-regulated processes mediated by NO have been

described in roots from different species and include root tip

elongation, adventitious root formation, primary root

growth inhibition, gravitropic response, cell cycle activa-

tion and root hair development (reviewed in Correa-Arag-

unde et al. 2007; Fernandez-Marcos et al. 2011). The first

report for NO participation in an auxin-dependent process

was performed in maize root segments exposed to NO

donors (Gouvêa et al. 1997), where it was found that NO

and auxins elicited the same plant response, in this case the

root tip elongation. The application of NO donors mimics

the effect of auxins (Chen et al. 2012), even in promoting

rooting of juvenile and mature cuttings of woody plants

(Abu-Abied et al. 2012). Moreover, the presence of NO was

described as a necessary requirement for crown roots pri-

mordia initiation in rice seedlings (Xiong et al. 2009).

Transient increase in NO levels in tissues were observed

during adventitious root development in cucumber explants

and in lateral root formation in tomato, in both cases

induced by auxins (Pagnussat et al. 2002; Correa-Aragunde

et al. 2004). Accordingly, application of exogenous indole-

3-butyric-acid (IBA) induces both lateral root initiation and

NO raises in primordia of A. thaliana roots (Kolbert et al.

2008). Auxin-induced adventitious roots, lateral roots, and

radical hair formation as well as root gravitropic response

were prevented by the application of the specific NO scav-

enger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-

1-oxyl-3-oxide potassium salt (cPTIO) pointing out a key

role for endogenous NO in mediating these processes

(Pagnussat et al. 2002; Correa-Aragunde et al. 2004; Hu

et al. 2005; Lombardo et al. 2006). Moreover, when polar

auxin transport is blocked employing 1-napthylphlamic

acid, the accumulation of NO in the interfascicular cells is

completely avoided (Yadav et al. 2011).

From these reports it is clear that NO is an important

molecule operating downstream of auxin through signaling

pathways during root growth and development.

One possible interaction between NO levels and auxins

has been proposed in cadmium-stressed plants where

application of NO reduced auxin degradation through the

inhibition of IAA oxidase activity, thus improving cad-

mium tolerance (Xu et al. 2010).

Evidence for a NO/cGMP signaling has been described

in auxin-dependent adventitious root formation in explants

of mung bean (Bai et al. 2012), supporting previous find-

ings demonstrating that NO and cGMP are involved in the

auxin response during the adventitious rooting process in

cucumber (Pagnussat et al. 2002; Pagnussat et al. 2003).

The involvement of a MAPK signal cascade in adventitious

root formation induced by auxins and NO was also

reported (Pagnussat et al. 2004).

These results led to proposing a model for auxin and NO

signaling consisted of auxin-induced NO accumulation in

tissues, which triggers a cascade involving cGMP, cADPR,

increases in cytosolic [Ca2?], and CDPKs or an alternative

cGMP-independent pathway involving MAPKs cascade

(Pagnussat et al. 2002; 2003; 2004; Xiong et al. 2009; Bai

et al. 2012). In addition, phosphatidic acid accumulation

was pointed out as an early signaling component during the

adventitious root formation induced by auxins and NO in

cucumber (Lanteri et al. 2008).

Plant Cell Rep (2013) 32:853–866 859

123



A mechanism explaining NO participation in auxin-

mediated processes has been recently developed for Ara-

bidopsis roots based on NO molecular targets (Terrile et al.

2012). As it was stated, adequate auxins concentration

leads to a transient increase in NO levels, which in turn

produces the S-nitrosylation of the auxin receptor TIR1.

This post-translational modification stimulates TIR1/AFB-

Aux/IAA interaction, which eventually leads to a modu-

lation of auxin-dependent gene expression (Terrile et al.

2012).

There are different aspects of iron metabolism that can

be affected by NO (Wink and Mitchell 1998). In plants,

NO reverts the symptoms of iron deficiency probably by

increasing the availability of internal iron or facilitating the

delivery of iron through the formation of mono- and dini-

trosyl iron complexes (Graziano et al. 2002; Graziano and

Lamattina 2007b; Ramirez et al. 2011). In addition, NO

acts as a signaling molecule mediating iron deficiency

responses through the upregulation of the expression of

iron uptake-related genes and the nuclear encoded ferritin

genes (Murgia et al. 2002).

Iron deficiency leads to an increase in NO level in root

epidermis, which is necessary for the expression of genes

associated with iron uptake in tomato roots, the basic helix-

loop-helix transcription factor LeFER, the ferric-chelate

reductase LeFRO1, and the Fe(II) transporter LeIRT1

(Graziano and Lamattina 2007a).

Strategy I plants (nongraminaceous monocots and

dicots) develop a range of responses against Fe-deficiency

stress, among them the activation of a plasmalemma ferric-

chelate reductase (Robinson et al. 1999) is a key compo-

nent, since it allows the enzymatic reduction of Fe(III) to

Fe(II), required for iron uptake. It has been described that

auxins are able to stimulate root ferric reductase activity in

Fe-sufficient cucumber, bean, and Plantago lanceolata

plants (Schmidt and Bartels 1996; Li and Li 2004). The use

of different auxin and NO-related Arabidopsis mutants

(aux1-7, axr1-3, noa1, and nia1 nia2) led to the conclusion

that NO acts as a signal downstream of auxins leading to

ferric-chelate reductase induction under Fe scarcity (Chen

et al. 2010). The authors developed a model in which Fe

deficiency leads to an increase in auxin levels, with the

subsequent enhance of NO concentration. NO would in

turn act as a signal activating ferric-chelate reductase

activity through a FIT-mediated transcriptional regulation

of FRO2 (Chen et al. 2010). The basic helix-loop-helix

transcription factor FIT (FER-LIKE FE DEFICIENCY-

INDUCED TRANSCRIPTION FACTOR) is a key tran-

scription factor in the Fe deficiency response required for

high-level expression of FRO2 and IRT in Arabidopsis

(Bauer et al. 2007). Moreover, NO and ethylene increase

the accumulation of FIT counteracting its proteasomal

degradation (Meiser et al. 2011; Lingam et al. 2011).

Another morphological response in plants exposed to Fe

scarcity is root branching, where both auxins and NO have

demonstrated to be involved (Benková and Bielach 2010).

Root branching was inhibited in Fe-deficient plants treated

with the NO scavenger cPTIO or the auxin transport

inhibitor NPA (Jin et al. 2011). It was suggested that NO

should act as a downstream signal of IAA in mediating Fe-

deficiency-induced root branching (Jin et al. 2011).

Probably, NO and auxins are implicated in a general

response against nutrient deficiency in plants, as it was

described for the development of lateral roots and cluster

roots in phosphorus-deficient plants (Nacry et al. 2005;

Wang et al. 2010; Meng et al. 2012).

Interplay between NO and ethylene in plant senescence

The senescence of plant organs is the last stage in their

development consisting in the degradation and remobili-

zation of molecules to other growing tissues (Nooden et al.

1997). Degradation of chlorophyll, proteins, antioxidants

and water imbalance are processes involved in the senes-

cence of plant organs highly regulated by hormones. Eth-

ylene is largely known as a key hormone that accelerates

leaf, flower and fruit senescence. In contrast, NO has been

observed participating in active growth and delaying the

development of the senescence syndrome in plants (La-

mattina et al. 2003; Guo and Crawford 2005). Young plant

organs present high NO rate emission, but it decreases

during maturation showing ethylene formation an opposite

trend (Leshem et al. 1998). This implies that NO and

ethylene productions are inversely affected during plant

development.

A specific association between these two signaling

molecules has been established in some studies. NO is able

to decrease ethylene emission through the downregulation

of its synthesis (Zhu and Zhou 2007; Manjunatha et al.

2012). All the elements of the ethylene synthesis pathway

affected are not clearly established. However, it is consis-

tently observed in several reports that the final step in

ethylene synthesis catalyzed by 1-aminocyclopropane car-

boxylic acid oxidase is down regulated by NO (Zaharah

and Singh 2011; Zhu et al. 2006). Furthermore, the S-nit-

rosylation by NO inhibits the activity of enzymes involved

in ethylene synthesis (Kaur and Deswal 2010). This work

shows that ethylene synthesis is highly controlled by NO.

Besides, NO may affect the response of different plant

organs to ethylene. It is well known that the sensitivity of

the tissues to a hormone depends on the active participation

of specific receptors and downstream components of hor-

mone signaling. NO might have an influence on ethylene

signaling pathway, but this interrelationship has not been

deeply studied yet. Information about the cross-talk

860 Plant Cell Rep (2013) 32:853–866

123



between these two physiological players is scarce and

remains to be further studied in detail.

The antagonistic effect of NO on ethylene-associated

senescence disorders has been used for the manipulation of

the development of undesirable biochemical modifications

of edible plant organs. Exogenous NO treatment was suc-

cessfully used for the extension of postharvest life of many

fruits (Cheng et al. 2009; Wills et al. 2000; Zhu et al.

2006). NO treatment delays the climacteric peak of ethyl-

ene production and the progress of fruit ripening of several

species. Associated with ethylene, there is a raise in the

respiratory activity and in ROS generation that are

involved in the acceleration of deteriorative processes

during ripening. Respiration activity is proportional to the

product deterioration, since many organic compounds are

metabolized (Kader 2002). It was also observed that NO

decreases respiration through the inhibition of cytochrome

c oxidase (Millar and Day 1996).

Another beneficial aspect observed during postharvest is

the improvement of fruit quality. Ascorbic acid or vitamin

C is an important nutritional metabolite that declines dur-

ing ripening (Kader 2002). While ethylene decreases

ascorbic acid concentrations (Gergoff-Grozeff et al. 2013)

NO stimulates its accumulation (Jin et al. 2009). Mito-

chondrial activity, which is affected by both NO and eth-

ylene, regulates ascorbate synthesis (Millar and Day 1996;

Bartoli et al. 2006). The precise mechanism linking NO,

ethylene, ascorbic acid, and respiration during plant edible

organ storage remains to be studied. It is worth noting that

other nutritional attributes were also improved by NO

treatment on several fruits (Manjunatha et al. 2012 and

references therein).

Similarly, flower vase conservation of a climacteric

species is improved by NO (Leshem et al. 1998; Bowyer

et al. 2003). NO extended the postharvest life of carnation

flowers, increasing the flower fresh weight and the anti-

oxidant activity and reducing the oxidative damage (Zeng

et al. 2011). The mechanism of action of NO on ethylene

metabolism and sensitivity in cut flowers is not known.

All this evidence shows that NO might affect different

metabolic traits leading to the improvement of extension

and quality of plant products for human consumption.

Concluding remarks

Undoubtedly, NO has a key role in signal transduction

network in plants influencing the action of hormones. In

addition to the mentioned interactions with ABA, auxins,

ethylene, and gibberellins, other research suggests that NO

is involved in jasmonic acid (Huang et al. 2004), salicylic

acid (Zottini et al. 2007), and brassinosteroids (Hayat et al.

2010) actions. Temporally and spatially controlled changes

in NO steady state concentration have an impact on second

messengers, enzymatic activities or activation of tran-

scription factors. Even though important molecular targets

of NO have begun to be discovered, and many others are

likely in the way to be identified in the near future, one

important question is how plants regulate cellular NO

steady state concentrations. Different pathways contribute

to the consumption, among them the enzyme nitrosoglu-

tathione reductase (GSNOR) (Lee et al. 2008) and the

molecular targets mentioned along the text. However, the

sources of NO, which probably rely on local substrates

availability such as L-arg, O2, or nitrite concentrations, as

well as changes in pH, remain unclear (Fröhlich and Dur-

ner 2011).

One of the main drawbacks in research involving NO is

the difficulty inherent in its detection. Detection is not a

simple issue due to both the low concentrations and the

relative high chemical reactivity of NO. The detection

method employing the commonly used diaminofluorescein

(DAF) derivatives is indirect, and actually relies in the

reaction of a product of NO oxidation with the fluorophore,

thus it could be affected by the presence of oxidants

(Jourd0heuil 2002). Detection of NO in a complex biolog-

ical system by this method should be confirmed, so far as

possible, by the use of alternative methodologies (Besson-

Bard et al. 2008).

An additional difficulty issue is related to the way in

which NO levels are manipulated in experimental condi-

tions. Research on NO participation in biological processes

is mainly based on the use of NO scavengers, NO donors,

and inhibitors of endogenous NO synthesis. Reinforcing the

idea of using different methodological approaches, it was

observed under certain conditions, that the presence of the

NO scavenger cPTIO could result in an unexpectedly

increase in the observed DAF fluorescence (Arita et al.

2006), which could be likely attributed to the indirect mode

of this detection as it was pointed out. Regarding the NO

donors, it is important to bear in mind that each compound

may have a different kinetic of NO release, and can differ

from other in the chemical form of NO generated (NO� or

NO?) (Floryszak-Wieczorek et al. 2006). This could help to

explain contradictory observations depending on the NO

donor employed (Murgia et al. 2004). Compounds may also

vary in their capacity for acting as nitrosylating agents, and

sometimes there are other active compounds that are being

released together with NO (Bethke et al. 2006). Finally, the

use of inhibitors of endogenous NO synthesis needs a note

of caution. Despite the fact that at least seven different

pathways have been proposed to produce NO in plants

(Gupta et al. 2011), there is a lack of knowledge regarding

the relevance of the different sources under physiological

conditions. Nitrate reductase (NR) is the unique enzymatic

activity identified in plants with the ability to reduce nitrite

Plant Cell Rep (2013) 32:853–866 861

123



to NO. This enzymatic activity is frequently inhibited

in vivo employing tungstate, which is an inhibitor of

molybdate-containing enzymes. Thus, tungstate has shown

to exert other effects unrelated with the inhibition of NR

activity (Xiong et al. 2012). Other important pathway for

NO production is related with the oxidation of the amino-

acid L-arg. Nitric oxide synthases (NOS) are present in

almost all known organisms except in higher plants, where

no NOS genes or enzymes have been identified yet. Just in

2010 was described the first cannonical NOS gene in a

photosynthetic organism, the microalgae Ostreococcus

tauri (Foresi et al. 2010). The use of L-arg analogs that are

inhibitors of classical mammalian NOS activities have

shown to be active in plant research, often in high con-

centrations (Gupta et al. 2011). In this regard, genetic

approaches involving the use of mutant plants with altered

endogenous NO levels constitute a valuable tool for

research supporting pharmacological studies.

Acknowledgments We are grateful to Agencia Nacional de Pro-

moción Cientı́fica y Tecnológica (ANPCyT) and Consejo Nacional de

Investigaciones Cientı́ficas y Técnicas (CONICET) for financial

support. MS, CG-M, CGB, GS-M, and LL are career investigators

from CONICET.

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866 Plant Cell Rep (2013) 32:853–866

123


	Nitric oxide as a key component in hormone-regulated processes
	Abstract
	Introduction
	NO in a biological environment: target molecules and effects
	ABA says NO to stomatal opening and plant water loss
	Interactions between NO and gibberellins: the DELLAs pathway
	Role of NO in auxin-mediated processes
	Interplay between NO and ethylene in plant senescence
	Concluding remarks
	Acknowledgments
	References