Roles of Nitric Oxide in Conferring Multiple Abiotic Stress Tolerance in Plants and Crosstalk with Other Plant Growth Regulators

Abstract

Nitric oxide (NO) is a free-radical gasotransmitter signaling molecule associated with a varied spectrum of signal trans-duction pathways linked to inducing cross-adaptation against abiotic stresses. It has crucial roles from seed germination to plant maturity, depending upon its cellular concentration. The functional cross-talk of NO among different stress signaling cascades leads to alteration in the expression of developmental genes that regulate biosynthesis and function of plant growth regulators (PGRs). NO-PGRs and secondary signaling compounds cross-talk trigger reprogramming of stress-responsive gene expressions, transcriptional gene modulations, redox regulating machinery, oxidative metabolisms, and multiple regulatory pathways under plant abiotic stress. Recent findings suggest NO as critical components of numerous plant signaling network that interplays with auxin, gibberellins (GA), abscisic acid (ABA), ethylene (ET), jasmonic acid (JA), brassinosteroids (BRs), H 2 O 2 , melatonin, hydrogen sulfide (H 2 S), salicylic acid (SA), and other PGRs to modulate growth and development under multiple stresses. Considering the importance of NO signaling crosstalk under stress adaptation, in this review, we point out the biosynthesis and metabolism of NO and its crosstalk with numerous other signaling compounds. Further, recent cellular and molecular advances in NO signaling cross-talk under abiotic stress adaptations also have been discussed.

Full text

Vol.:(0123456789)
1 3
Journal of Plant Growth Regulation
https://doi.org/10.1007/s00344-021-10446-8
Roles ofNitric Oxide inConferring Multiple Abiotic Stress Tolerance
inPlants andCrosstalk withOther Plant Growth Regulators
RajeshKumarSinghal1· HanumanSinghJatav2 · TariqAftab3· SaurabhPandey4· UditNandanMishra5·
JyotiChauhan6· SubhashChand1· Indu1· DebanjanaSaha5,10· BasantKumarDadarwal7· KailashChandra2·
MudasserAhmedKhan2· VishnuD.Rajput8· TatianaMinkina8· EetelaSathyaNarayana9· ManojKumarSharma2·
ShahidAhmed1
Received: 31 March 2021 / Accepted: 13 July 2021
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021
Abstract
Nitric oxide (NO) is a free-radical gasotransmitter signaling molecule associated with a varied spectrum of signal trans-
duction pathways linked to inducing cross-adaptation against abiotic stresses. It has crucial roles from seed germination to
plant maturity, depending upon its cellular concentration. The functional cross-talk of NO among different stress signaling
cascades leads to alteration in the expression of developmental genes that regulate biosynthesis and function of plant growth
regulators (PGRs). NO-PGRs and secondary signaling compounds cross-talk trigger reprogramming of stress-responsive gene
expressions, transcriptional gene modulations, redox regulating machinery, oxidative metabolisms, and multiple regulatory
pathways under plant abiotic stress. Recent findings suggest NO as critical components of numerous plant signaling network
that interplays with auxin, gibberellins (GA), abscisic acid (ABA), ethylene (ET), jasmonic acid (JA), brassinosteroids (BRs),
H2O2, melatonin, hydrogen sulfide (H2S), salicylic acid (SA), and other PGRs to modulate growth and development under
multiple stresses. Considering the importance of NO signaling crosstalk under stress adaptation, in this review, we point out
the biosynthesis and metabolism of NO and its crosstalk with numerous other signaling compounds. Further, recent cellular
and molecular advances in NO signaling cross-talk under abiotic stress adaptations also have been discussed.
Keywords Abiotic stresses· Cross-talk· Plant growth regulators· Stress tolerance· Signaling network
Introduction
Nitric oxide (NO) is an essential gasotransmitter, which
acts as a signaling molecule during plant stress. NO cross-
talk with other signaling molecules to transduce stress sig-
nals between the cells. These signaling molecules include
Handling Editor: M. Naeem.
* Hanuman Singh Jatav
hanumaniasbhu@gmail.com; hsjatav.soils@sknau.ac.in
1 ICAR-Indian Grassland andFodder Research Institute,
Jhansi, UttarPradesh, India
2 S.K.N Agriculture University, Jobner, Rajasthan, India
3 Department ofBotany, Aligarh Muslim University, Aligarh,
India
4 National Institute ofPlant Genome Research, NewDelhi,
India
5 M.S. Swaminathan School ofAgriculture, Centurion
University ofTechnology andManagement, Gajpati, Odisha,
India
6 Narayan Institute ofAgricultural Sciences, Gopal Narayan
Singh University, Bihar, India
7 Institute ofAgriculture Sciences, Banaras Hindu University,
Varanasi, UttarPradesh, India
8 Southern Federal University, Rostov-on-Don, Russia
9 Agricultural College-Palem, Nagarkurnool, PJTSAU,
Hyderabad, Telangana, India
10 Department ofBiotechnology, Centurion University
ofTechnology andManagement, Bhubaneswar752050, India

Journal of Plant Growth Regulation
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reactive oxygen species (ROS), phytohormones [Auxin
(Aux), gibberellin (GA), cytokinin (CK), ethylene (ET),
and abscisic acid (ABA), jasmonic acid (JA)], plant growth
regulators’ melatonin (MT), and other signaling molecules.
This suggests that two or more biosynthesis pathways share
some common path to regulate signals in better ways, also
known as crosstalk. Several endogenous growth regulators
such as ABA and GA are reported previously for breaking of
seed dormancy/inducing seed germination. In recent years,
nitrate, nitrite, hydroxylamine, azide, NO, and sodium nitro-
prusside (SNP) compounds were also identified to regulate
seed dormancy and germination processes through phyto-
hormonal cross-talk (Krasuska etal. 2017).
For instance, ET and NO crosstalk with ABA during seed
germination and dormancy period counteract the action of
ABA (Arc etal. 2013). Similarly, in canola and maize, exog-
enous application of NO enhances seed germination in a
dose-dependent manner (Fan etal. 2013a, b). Nevertheless,
different mechanisms stimulate seed germination by light
and NO reported (Beligni etal. 2000; Poor etal. 2019). It
remains unclear whether the GA- and NO-promoting ger-
mination mechanism acts synergistically or antagonistically.
CK and NO crosstalk were also reported to regulate the
photo-morphogenesis process observed in Arabidopsis, pars-
ley, or tobacco cell (Tun etal. 2001). Exogenous application
of NO and CKs inhibit hypocotyl elongation in Arabidop-
sis and lettuce dark-grown seedlings (Beligni etal. 2000).
Recently, Wu etal. (2016b) reported that hydrogen peroxide,
NO, and UVR 8 interact with each other and are subjected
to anthocyanin accumulation in reddish sprouts. Likewise,
NO plays a crucial role in inhibiting primary root growth in
Arabidopsis by regulating PHYTOCHROME INTERACT-
ING FACTOR 3 (PIF 3) under light conditions (Bai etal.
2014). There is evidence that IAA and NO regulate the same
responses in plants due to sharing some common steps dur-
ing the signal transduction pathway. For example, growth of
maize root segment influenced by NO in a dose-dependent
manner similar to indole acetic acid (IAA) (Gouvea etal.
1997).
Studies suggested that NO plays a crucial role in stomatal
movement, together with H2O2, abscisic acid (ABA) under
water stress (Garcia-Mata etal. 2002; Desikan etal. 2002;
Garcia-Mata etal. 2003; Desikan etal. 2004). NO regulate
stomatal closure through Ca2 þ–dependent stomatal closure
mechanism (Desikan etal. 2001). Synergistic effects of ABA
and NO on stomatal closure were observed in Pisum sati-
vum and Vicia faba plants (Neill etal. 2003). Some research
also confirmed NO in guard cells (Garcia-Mata etal. 2002),
leading to stomata closure through NR activity. Recently, it
is suggested that UVR8, H2O2, and NO interact with each
other under UV light and close the stomata by regulating
the UVR8 pathway (Tossi etal. 2014). NO also increases
the chlorophyll content in potato, lettuce, and Arabidopsis
(Beligni etal. 2000). NO preserves and increases chlorophyll
content similarly to CKs “chlorophyll retention effect” in pea
and potato (Leshem and Wills 1998).
Rapid synthesis of NO and a parallel accumulation of
ROS are typically observed under biotic and abiotic stresses.
Consequently, these adverse responses activate the senes-
cence process, ultimately leading to the death of plant cells.
Earlier studies suggest that both NO and ROS play impor-
tant roles in regulating programmed cell death (PCD) either
independently or synergistically (Wanget al. 2013). There-
fore, NO plays crucial functions in nutrient homeostasis, ion
transport, plastid development, and alleviation of antioxidant
genes during normal and unfavorable conditions as signaling
compounds. Some of the pivotal roles of NO in plant growth
and development are highlighted in Fig.1.
Abiotic (drought, salinity, heavy metals, extreme temper-
ature, etc.) stresses are a significant concern for low agricul-
tural production worldwide. They are steadily increasing due
to uninvited anthropogenic activities in the natural environ-
ment (Asgher etal. 2017). These stresses adversely affect
plant growth and development (Khan etal. 2015a; Fancy
etal. 2017) by producing ROS (singlet oxygen, hydrogen
peroxide, hydroxyl radicals, superoxide radicals, etc.). These
are needed for the proper functioning of cells under normal
conditions but adversely affect the cell programming sys-
tem under stressful environments (Gupta etal. 2016; Asgher
etal. 2017). The multiple stresses induce modulation of phy-
tohormonal regulation, metabolism, and signaling in plants,
which affects the plant defense system through metabolic
adjustment, stomatal regulation, and behavioral changes in
plant growth and development (Zhang etal. 2006a). The NO
has been considered either a protective mediator or stress-
inducing agent and plays a crucial role in intracellular redox
signaling, ion homeostasis, and activation of antioxidant
defense mechanisms (Asgher etal. 2017). Several studies
suggested NOs’ role in maintaining pigment composition,
stomatal movements, root growth and development, water
relations, membrane stability, hormonal balance, osmotic
adjustments, and ion channels’ activities in plants under dif-
ferent circumstances through cross-talk with other signaling
compounds (Li etal. 2015; Shan etal. 2015; Kaya etal.
2020a, b; Wu etal. 2020; Santos etal. 2020).
On recognizing the importance of NO crosstalk in plants
under multiple abiotic stresses, in this review, we have
explored biosynthesis and metabolism pathways of NO in
different cellular sites and their regulating factors. Then, we
have discussed the NO cross-talk with other signaling com-
pounds, their regulatory roles, and crucial molecular mecha-
nisms of NO crosstalk under multiple abiotic stresses. This
information will help us understand the role of NO crosstalk
as a central hub in regulating plant processes under different
environmental stresses.

Journal of Plant Growth Regulation
1 3
NO Biosynthesis andMetabolism
Nitric Oxide (NO) has multifaceted physiological role in
plants as a bioactive gasotransmitter. Eight different enzy-
matic and non-enzymatic processes that can produce NO in
plants have been identified to date. Nitrite (NO2−) or more
reduced compounds (L-arginine or hydroxylamine) are pro-
duced due to NO generation through oxidation (Mur etal.
2013). Cytoplasm, mitochondria, chloroplast, peroxisome,
and apoplast are themajor cellular sites for NO2−reduction
(Roszer 2012a,b). Reduced NO can be generated through
nitrate reductase activity (NR; EC 1.6.6.1 to EC 171) via
mitochondrial electron transport chain (mETC) or heme-
containing proteins. The oxidative NO can be synthesized
through L-arginine and other compounds. In the acidic
compartments of plant tissues, non-enzymatic reduction
of NO2−/NO can also happen (Roszer 2012a, b; León and
Costa‐Broseta 2020). Mechanism of production or synthesis
of oxidized and reduced, enzymatic, and non-enzymatic NO
are discussed in this section and highlighted in Fig.2.
Mechanisms ofReductive Synthesis
By Nitrate Reductase (NR)
Nitrate reductase can reduce NO2− to NO with low efficacy
through primary nitrate (NO3−) oxidoreductase activities
(Rockel etal. 2002). In cyanobacterium (Anabaena doli-
olum), green algae, and vascular plants, NR catalytic reduc-
tions from NO2− to NO have a crucial role during stress
response (Mur etal. 2013; Floryszak-Wieczorek et al.
2016). It indicates one of the oldest forms of NO produc-
tion mechanisms in plants (Astier etal. 2018). Cytoplasm
and chloroplast association are the main pool of NR activity
(Kolbert etal. 2019). However, using a reduced cytochrome
cas an electron donor, NO2−/NO-reductase (NI-NOR)
reduces NO2− to NO. NO NI-NOR generation is similar to
NO3−-reduced root-specific NR activity, but NO-NOR may
act as a separate protein and needs to be regarded as NR-
generated NO (Mohn etal. 2019).
By Mitochondrial ETC (Electron Transport Chain)
Mitochondria can use NO2− as an alternate electron accep-
tor for ATP synthesis; reduction of NO2− to NO takes place
Fig. 1 Schematic illustration of nitric oxide (NO) pools in the cells
triggered under stress and their subsequent metabolism. The possi-
ble different pathways can lead to the generation of NO pool in the
cytosol (enzymatic and non-enzymatic pathways) and apoplast (non-
enzymatic pathway). Cytoplasmic organelles such as peroxisome,
mitochondria, chloroplast, and acidic vacuoles are the prime com-
partments for NO biosynthesis. Various effectors regulating (up- or
down-regulation) NO pools are phytohormones (ABA, cytokinin,
GA, auxin, brassinosteroids), ambient light, transition metals, phe-
nolics, abiotic stressors, and feedback inhibition (NO pool-mediated
reduction of NO2−to NO).Solid lines ( ) and dotted lines (
) are used to avoid the overcrowding and clarity of the figure; ( )
depicts inhibition/inhibitory effect

Journal of Plant Growth Regulation
1 3
inside complex III (cytochrome bc1) and IV (cytochrome-c
oxidase, CCO) (Gupta and Igamberdiev 2011a; Kolbert etal.
2019). The mechanism creates hypoxia in plant cells which
results in mitochondrial NO generation. Hypoxia increases
NR transcription activities, which converts NO3− to
NO2− and results in a cytoplasmic accumulation of NO2−.
NO2− reduction is limited in the hypoxic cell, and a contin-
ued supply of NO2− for reduced NO synthesis is permitted
(Roszer 2012a, b). Therefore, a specific system of O2 trans-
port in plants reduces NO synthesis/mitochondrial NO2− or
NO. The NO generated within the mitochondria inhibits the
germination of CCO (Gniazdowska etal. 2010a, b), which
enhances the energy status of O2-limited cells (Gupta and
Igamberdiev 2011b). The reduced mitochondrial NO gen-
eration inhibits the photo-respiratory cycle and fermentative
metabolism (Oliveira etal. 2013). NO released from mito-
chondria into the cytosol is oxidized by plant hemoglobin
(NO3−) due to hypoxia (Igamberdiev and Hill 2004). This
leads to NO/NO2− exchange of mitochondria in the cyto-
plasm, maintaining a continuous supply of NO2 for ATP
synthesis under hypoxia (Gupta and Igamberdiev 2011b).
The cytoplasmic conversion NO/ NO3−/NO2 ensures that the
low redox level helps adapt to the hypoxic NADH/NADP+
and NADPH/NADP+ ratios (Igamberdiev etal. 2010).
By Heme‑Containing Proteins
Plant peroxisomes can produce NO under hypoxic or anoxic
conditions by reducing NO2− (Igamberdiev etal. 2010).
NO2−/NO may reduce the capacity of deoxygenated heme-
containing proteins in the peroxisome matrix, which is the
primary production mechanism (Igamberdiev etal. 2010;
Sturms etal. 2011). The plant plasma membrane, cytosol,
and endoplasmic reticulum have shown a similar reductional
NO generation (Igamberdiev etal. 2010). Cyanobacteria
(Sturms etal. 2011) and mammalian tissues have also been
affected by a reduction in the use of heme-proteins from
NO2− to NO (e.g., hemoglobin’s) (Tiso etal. 2011).
Mechanisms ofOxidative NOSynthesis
NOS (EC 1.14.23.29) proteins and NOS encoding genes
(Roszer 2010) have been identified in prokaryotes, unicel-
lular eukaryotes, invertebrates, non-mammalian vertebrates,
and mammals. However, higher plants lack homologous
sequences for known NOS encoding genes (Mur etal. 2013).
Oxidative L-arginine synthesis is also present in plants’
cells, but the responsible enzyme NO synthase (NOS) has
not yet been found. Some of the pathways.
From L‑arginine
The chloroplasts and leaf peroxisomes of the vascular
plants and the green algae have been identified as a site for
enzymatic oxidation of L-arginineto NO and L-citruline
(Roszer 2012b). The chloroplastic oxidation of L-arginine
to NO requires NADPH and in the absence of Ca2+ (Jasid
etal. 2006). In the peroxisomes of leaves, Ca2+, calmodulin,
NO crosstalk functionsinplants
Physiological processes
Molecular
Biochemical
Abiotic stress tolerance
Reproductive
Post-harvest
Early stage
Vegetative stage
Biosynthesis and metabolism
Oxidative defense
Energy metabolism
Plant growthregulators
activity
Post translational modification
Alleviation of antioxidantgenes
Produce heat shockand stress protein
Regulatory gene expression
Redox depend chromatin remodeling
Activate stress crosstalksignalling
S-nitrosylation
Protein carbonylation
Redox homeostasis
Antioxidants elevation
Heavy metals
Water stress
Temperature stress
Salinity stress
High irradiance
stress
Pollen tube
growth
Fertilization
Flowering
Leaf senescence
Photosynthetic partioning
Fruit ripening
Improving fruit quality
Programmed cell death
Dormancy release
Seed germination
Hypocotylelongation and development
Activation of cell cycle
Plastid development
Reprogrammed root system
architecture
Nutrient homeostasis
Photosynthatesformation
Stomatal movement
Waterrelation
Plant metabolism
Photo-morphogenesis
Iontransport Nutrient stress
Fig. 2 Highlights the crucial functions of NO crosstalk in plant growth developments and under stresses. Nitric oxide regulates the crucial func-
tion from germination to post-harvesting and regulates critical processes (physiological, biochemical, and molecular) during multiple stresses

Journal of Plant Growth Regulation
1 3
FAD, FMN, and NADPH are required for L-arginine/L-cit-
rulline conversion (del Rio etal. 2003; del Río 2011). It has
been recently found that L-arginine-oxylated NO synthesis
requires both Ca2+ and NADPH, with tetrahydrobiopterin
(BH4)in Ostreococcus green algae species (Foresi etal.
2010). Plant mitochondria also oxidize L-arginine to NO
with the help of enzymes available in the matrix or inter-
membrane space (Guo and Crawford 2005). It is debatable
whether plant mitochondria contain a specific NO oxidative
synthesis enzyme (Barroso etal. 1999).
Other Forms ofOxidative NOSynthesis
Polyamines and hydroxylamine have recently been shown
to increase the synthesis of oxidative NO in plant cells
(Wimalasekera etal. 2011). The exact mechanism of poly-
amines in increasing NO synthesis remains uncertain (Fröh-
lich and Durner 2011). However, NO cannot mediate the
effect of polyamines on plants. Pathways possibly respon-
sible include an interaction between polyamines and NR-
catalyzed NO (Rosales etal. 2012) and the indirect impact of
polyaminesynthesis on L-arginine metabolism (Zhang etal.
2011). Hydroxylamine is an intermediate in the nitrification
process and can be oxidized to NO in tobacco cell cultures
(Rumer etal. 2009). This mechanism could be a substi-
tute for oxidative NO synthesis via L-arginine. However,
the underlying molecular mechanism is still unknown for
hydroxylamine’s role in NO synthesis (Rumer etal. 2009).
The possible contribution to NO plant synthesis for other
enzymes needs to be explored.
Non‑enzymatic NOGeneration
Non-enzymatic NO generation includesrelease from nitrous
acid (HNO2) after protonation. Acidic environments such
as apoplast of germinating and hypoxic seeds favor this
type of chemical NO release (Yamasaki 2000; Bethke
etal. 2004). Consequently, in the aleuronic layer of bar-
ley, the NO release from NO2− has been shown (Bethke
etal. 2004). Phenolic compounds found in aleuron apoplast
and on seed coat increase this non-enzymatic NO release.
The NO release in germinating seeds may protect them
from soil microorganisms (Bethke etal. 2004). In addition,
seed dormancy is interrupted by NO, which suggests that
proper germination requires NO2− together with an enzy-
matic NO synthesis (Roszer 2012b). Together, NO release
can synergize with the reduction of the enzyme NO2−/NO
to invoke germination NO burst. During germination,NO-
mediated programmed cell death occurs when aleuron cells
are removed (Lombardi etal. 2010). However, the release
of NO from S-nitrosoglutathione (GSNO) (del Río 2011) is
another possible, unexplored mechanism for non-enzymatic
NO generation. This compound is formed in the oxidative
environment of peroxisomes, which allows both GSNO and
GSNO to react with glutathione (Barroso etal. 2006). The
GSNO is a compound NO-donor and could carry reserve NO
distributed in the plant’s tissues. GSNO genesis is facilitated
by environmentally friendly light and metal transition (Flo-
ryszak-Wieczorek etal. 2006). Hydroxylamine is another
possible non-synthesis substrate (Rumer etal. 2009), but
GSNOR would not support hydroxylamine production.
NO Metabolism
NO metabolism includes a redox range, which displays dis-
tinctive properties and reactivity such as nitrosonium (NO+),
NO radical (NO*), and nitroxyl anion (NO−) (Gisone etal.
2004). Nitrosation in aqueous phases in organic molecules
in –S, –N, –O, and –C centers results in NO+. The biological
relevance of NO+ was disputed under slightly acidic or phys-
iologic conditions, but a variety of nitroso-compounds form-
ing effectively under neutral physiological conditions could
be interpreted as NO+ reactions (Stamler etal. 1992).These
compounds include metal-nitrosyl-complexes, thionitrites
(RS-NO), nitrosamines (RNH–NO), alkyl- and aryl-nitrites
(RO–NO), and tri- and tetra-oxides (N2O3 and N2O4) of
dinitrogen. Numerous nuclear centersin biological systems
whose potential nitrosativevulnerability were demonstrated
in invitro studies (Stamler etal. 1992). Dimerization and
dehydration quickly convert NO− to the N2O (Basylinski and
Hollocher 1985) and reacts with Fe (III) heme (Goretski and
Hollocher 1988).
NO* is also reversible in sulfhydryl oxidation, leading
to low molecular weight and protein-associated thiols. The
transmission of electrons and collisions is standard and
generally results in NO radical (NO*) as the main product.
S-nitrosothiols are thought to be a (minor) product of the NO
disulfide reaction (Stamler etal. 1992). The significant NO
reactions are those with O2 and its different redox and transi-
tion ions in biological terms. When discussing the chemical
and physiological effects, NO is a highly diffused second-
ary messenger that may generate relative effects far from
its production site in plants. Hence, the concentration and
the source of NO are the main determinants of its biologi-
cal effects (Wink and Mitchell 1998). The direct effects of
NO are the result of the interaction between NO and metal
complexes. NO form complexes, including those found reg-
ularly in metalloproteins, of transition metal ions. Heme-
containing protein reactions have been studied extensively
for NO-complexes.
NO also forms non-heme transition metal complexes,
and biochemical focus was given to its responses to the
Fe–S center of the proteins, including several mitochon-
drial electron transportations and enzyme proteins (Henry
etal. 1991). NO’s reaction to heme-containing proteins

Journal of Plant Growth Regulation
1 3
includes cytochrome P450 interactions with more consider-
able physiological consequences (Wink etal. 1993). Tyros-
ine nitration is also a directly established effect of NO on
proteins. Tyrosine nitration is selective and reversible and
ONOO− dependent. Invivo nitration pathways were shown
to be ONOO− independent (Davis etal. 2001). NO can also
stop lipid peroxidation (Rubbo etal. 1995). Nitrosating oxi-
dation or nitration is the indirect effect of NO, generated
by the interaction of the NO and O2− (Wink etal. 1993).
None of these substances can undergo autoxidation (i.e.,
reactions to O2) to produce N2O3 in aquatic solutions (Ford
etal. 1993). Since NO and O2 are 6–20 times more soluble
in lipid layers, the auto-oxidation rate in a lipid phase (Ford
etal. 1993) dramatically increases. The primary N2O3 reac-
tions are thought to occur in the membrane fraction.
In its response to O2, NO generates ONOO at a rate near
diffusion, which acts as a nitrating agent as well as a pow-
erful oxidant to modify the proteins (nitrotyrosine forma-
tion), lipids (lipid oxidation, lipid nitration), and nucleic
acids (DNA oxidation and DNA nitration). In short, there are
numerous potential reactions of NO depending on the cell
milieu facilitating biochemical modifications. The produc-
tion site, source, and NO concentration collectively deter-
mine its effects. In addition, a relative equilibrium exists
between oxidative and nitrosating stress. The mechanism
of NO biosynthesis and its metabolism are highlighted in
Fig.1.
NO: Plant Signaling Component Hub
Perceiving the cues within cells and outside the environ-
ment is vital for the plant life cycle. This perception is
accomplished by plant signaling. Plant signaling involves
an exchange of information between plant cells from recep-
tors to effector through signaling molecules. Discoveries of
molecular components related to signaling provided evi-
dence about the signal response as a cumulative effect of
cross-talk between different signaling pathways (Taylor etal.
2004). This cross-talk generally results from pathway inte-
gration with the unique signal response as a combination.
Such cross-talk involved in physiological processes ranged
from development to stress responses (Peck and Mittler
2020). Some of the critical signaling compounds are ROS,
PGRs, and signaling peptides discussed in this section in NO
as a central signaling molecule. NO orchestrate a plethora of
signaling responses in plants. These responses act at inter-
and intra-cellular levels to modulate plant growth and devel-
opment. NO-mediated transcriptional changes or secondary
messenger activation regulates these processes (Falak etal.
2021). These processes include photosynthesis, organelles
motility, hypersensitive response, programmed cell death,
seed germination, cell wall lignification, flowering, pollen
tube growth, fruit ripening as well as legume–rhizobium
symbiosis, and biotic and abiotic stress (Turkan 2017; Sami
etal. 2018; Inmaculada Sánchez-Vicente etal. 2019).
NO signaling operates at various levels, specifically with
ROS of the anti-oxidant system (Ma etal. 2016) and affects
seed dormancy, plant reproduction mechanisms (Jiménez-
Quesada etal. 2016), plant–rhizobia interaction (Damiani
etal. 2016), and plant–pathogen interactions (Thalineau
etal. 2016). Moreover, higher NO/ROS content correlates
with the compromised antioxidant system in plants (Gaupels
etal. 2016). This interplay of NO/ROS homeostasis is also
vital for N nutrition and plant immunity. These processes are
mainly governed by NR activity, which is an essential part
of NO signaling after stress induction. Hormonal control on
NO/ROS homeostasis is a crucial factor in plant develop-
ment and stress response, as reported by Sivakumaran etal.
(2016). Also, mitochondria play a vital role in the modu-
lation of NO and ROS signaling by changing hypoxic or
anoxic conditions (Gupta and Igamberdiev 2016). Other than
the direct involvement of NO in ROS production, post-trans-
lational modification of NO enzymes is essential for NO/
ROS homeostasis, emphasizing the ascorbate–glutathione
cycle (Begara-Morales etal. 2016). NO self-regulation also
affects ROS levels (Romero-Puertas and Sandalio 2016).
This regulation indicates the fine-tuning of NO and ROS as
signaling components.
Another facet of NO signaling operates as a secondary
messenger in conjugation with other signaling molecules as
cytosolic Ca2+ levels, cyclic guanosine 5′-monophosphate
(cGMP), cyclic adenosine diphosphate ribose (cADPR),
phosphatidic acid, H2O2, JA and SA, and Mitogen-Associ-
ated Protein kinases (Santner and Estelle 2009; Foyer and
Noctor 2015; Duszyn etal. 2019; Yang etal. 2019). NO-
cGMP-dependent pathway in plants opens avenues of NO
crosstalk with cGMP signaling (Gross and Durner 2016).
While NO-mediated cGMP signaling is well known in mam-
mals, this system is not well defined in plants. However, the
identification of enzymes of the cGMP pathway in higher
plants supports this hypothesis. This crosstalk provides
the molecular basis of physiological and developmental
responses generated through NO signaling.
Further, downstream target protein studies give cues
about the indirect effect of NO signaling (Simon and Dres-
selhaus 2015). Other than cross-talk in conventional path-
way, NO directly interacts with other molecules to affect
the biological processes in the plant, for example, NO–sul-
fur (Fatma etal. 2016), NO–inositol (Lytvyn etal. 2016),
NO–heme oxidase 1 (Wu etal. 2016a), and NO-H2O2
interactions (Molassiotis etal. 2016). Understanding this
cross-talk in light of NO response and signaling will provide
insights into its mechanism. The NO crosstalk with other
crucial signaling compounds is highlighted in Fig.3 and
discussed in this section.

Journal of Plant Growth Regulation
1 3
Molecular Understanding ofNOCrosstalk
withCrucial Signaling Compounds
In the signaling cascade, phytohormones are instrumental
for orchestrating plant growth, development, and stress
responses (Santner and Estelle 2009). NO is an essential cue
in signaling cascade interactions with all major hormones
and other endogenous molecules (Freschi 2013). Here, NO
acts as a secondary messenger for plant hormones involved
in stress responses (Saito etal. 2009; Liu etal. 2010). The
subsequent section will discuss the NO accumulation in spe-
cific tissues to perform particular functions in routes with
hormonal regulation.
NO–ABA Crosstalk
Abscisic acid (ABA) is referred to as stress hormone cross-
talk with NO during various environmental challenges and
activates the antioxidant system (Hancock etal., 2011; Fre-
schi 2013). The ABA-induced response was reduced after
the decrease in NO synthesis, which suggests that it is acting
downstream of ABA under stress treatments (Tossi etal.
2012; Zhang etal. 2009). On contrary to this, NO coun-
teracts the ABA (Lozano-Juste and Leon 2010a, 2010b).
This mechanism operates at cell, tissue, and organ level
and indicates the specificity of NO–ABA signaling under
specific physiological events. The role of NO–ABA cross-
talk was reported in different physiological processes, for
example, during germination (Liu etal. 2009) as transcrip-
tional inducer and in the maintenance of seed dormancy
(Bethke etal. 2006). Under stress conditions, ROS gen-
eration induces the ABA–NO crosstalk by activating anti-
oxidants and transcription factors (Lu etal. 2009; Zhang
etal. 2007a). Other signaling molecules such as cGMP
MAPK and type 2C protein phosphatases act downstream
of NO–ABA interplay and antioxidant system to modulate
plant stress response (Desikan etal. 2002; Dubovskaya etal.
2011; Mioto etal. 2013). Mutant studies suggested the role
of this cross-talk for salinity stress (Lu etal. 2009; Kong
etal. 2016), heat and drought stress (Zandalinas etal. 2016),
and thermotolerance of plant calluses (Song etal. 2008).
NO–GA Cross‑Talk
Gibberellic acid is a crucial phytohormone associated with
seed germination and plant growth. In the signaling cas-
cade, NO promotes the biosynthesis of GA by transcriptional
regulation of GA biosynthesis genes (Bethke etal. 2007).
NO
ROS
Auxin
H2O2
Ca
Cd toxicity
Cu toxicity, salt
stress
Heat stress
GA
ABA
Salt stress
PAs
Cold stress
ET
Fe deficiency
CO
Fe deficiency
Seed dormancy and
germination
ROS
ET
Fruit ripening
SA
Salt stress
Plastid
development
BRs
Cold stress
H2S
Root system
development
Stomata
closing
Stomatal movement,
activation of MAPK
JA
Senescence,
Defense
Root
development
Triterpenoid
synthesis
MT
Root system
development
Si
Adventitious
root formation
Fe deficiency,
salt stress
Fruitripening
Fe deficiency
Fig. 3 Model highlights the NO crosstalk with PGRs and other sign-
aling compounds in plant growth regulation and stress conditions.
NO crosstalk is very complex in nature; it crosstalk with numerous
signaling compounds such as H2S, H2O2, Ca, melatonin, ethylene,
abscisic acid, and salicylic acid to regulate various homeostasis pro-
cesses under normal and stress conditions

Journal of Plant Growth Regulation
1 3
NO acts as a balance center for ABA-induced dormancy
and GA-stimulated germination. The molecular basis of
this balance lies in the activation of the anti-oxidant system
along with post-translational modification of other enzymes
involved in ethylene synthesis (Gniazdowska etal. 2010a,
b; Hebelstrup etal. 2012). GAs have been reported to con-
trol hypocotyl growth in coordination with DELLA protein
degradation (de Lucas etal. 2008). Interestingly enough,
higher NO levels antagonize hypocotyl growth (Beligni
and Lamattina 2000). Moreover, NO was also reported in
the repression of PIF genes and augmenting DELLA pro-
tein content (Lozano-Juste and León 2011). That led to the
possibility of NO–GAs–light interplay in the regulation of
seed germination events. NO–GAs module also operates at
various stress conditions, for example, aluminum toxicity
in wheat (He etal. 2012), cadmium toxicity in Arabidop-
sis (Zhu etal. 2012), and deprived phosphorous condition
(Asgher etal. 2017).
NO–Auxins Crosstalk
Auxin is an essential phytohormone associated with cell
elongation. NO as a signaling molecule in NO–Auxin cross-
talk modulates auxin degradation enzyme activity (Xu etal.
2010), interferes with auxin transport through PIN1 efflux
carrier (Fernández-Marcos etal. 2011), and activates auxin
signaling by S-nitrosylation of the auxin receptor protein
(Terrile etal. 2012). The role of auxin in plant root archi-
tecture, lateral root growth, and root hairs is well docu-
mented (Overvoorde etal. 2010). Interestingly, most root
architecture phenotypes are also influenced by NO as signal
molecules (Fernández-Marcos etal. 2011). Invitro cultures
suggest that auxin application does not affect NO release
(Tun etal. 2001). This advises downstream action of NO
in auxin signaling response (Chen etal. 2010). NO–Auxin
crosstalk operates from synthesis to perception in response
to environmental and developmental cues. This crosstalk
was also reported in plant stress responses, for example,
iron deficiency (Chen etal. 2010), drought and water stress
conditions (Pagnussat etal. 2002; Liao etal. 2012) due to
extensive involvement with root architecture regulation, and
cadmium toxicity (Yuan etal. 2016; Xu etal. 2010).
NO–Melatonin Crosstalk
Melatonin is the novel amine-derivative hormone class
involved in plant growth, development, aging, and stress
response. Interaction of NO with melatonin regulates the
melatonin synthesis genes and changes the phytohormone
level (Zhu etal. 2019). Further, downstream action of NO
activates MAPK-associated defense responses. Exogenous
application of melatonin induces glycerol, sugar produc-
tion, ultimately increasing NO and salicylic acid levels.
NO–melatonin crosstalk affects several physiological pro-
cesses like root growth, aging, and iron deficiency allevia-
tion (Zhu etal. 2019; Kaya etal. 2020a).
NO–JA Crosstalk
Jasmonic acid is a fatty acid-derivative phytohormone
mainly associated with herbivory and pathogen response.
Abiotic stress, such as drought stress, affects the JA-asso-
ciated signaling genes (Huang etal. 2008). NO treatment
induces JA-biosynthesis genes that indicate interplay of
NO–JA module (Palmieri etal. 2008). CDPKs are induced
by JA, starting the ABA-induced stomatal closure (Mune-
masa etal. 2007). External treatment with MeJA and ABA
increases NO and ROS content in guard cells (Munemasa
etal. 2007). Evidence suggests calcium signaling acting
downstream of NO–ROS crosstalk. Apart from that, JA asso-
ciated with NO synthesis increases ROS scavenging enzyme
as reported for chilling stress tolerance in Cucumis sativus
(Liu etal. 2016).
NO–CK Crosstalk
Cytokinins are a class of phytohormones associated with
plant cell division in plant shoot and root. CK–NO module
of signaling affects the biosynthesis of nitric oxide; how-
ever, peroxynitrite (NO-derived) binds with zeatin to reduce
its activity (Liu etal. 2013). Type-A response regulators
are a crucial component of CK signaling regulated by NO-
mediated S-nitrosylation (Feng etal. 2013). NO–CK cross-
talk also operates in different stress responses, such as water
stress conditions (Shao etal. 2010) and salt stress conditions.
Antagonistic relation of CK on NO levels was also reported
in Vicia faba seedlings grown under dark (Song etal. 2011)
and leaf development in aging leaves. The molecular basis
of this regulation is supposed to be the limitation of phos-
phorelay activity caused due to S-nitrosylation (Fan etal.
2013a, b).
NO–ET Crosstalk
Ethylene also known as ripening/senescence/stress hormone
is important for plant growth regulation. Heavy metal stress
often increases the activity of the 1-aminocyclopropane-
1-carboxylic acid (ACC) synthase (ACS) enzyme that is
associated with ET (Khan etal. 2015b). Understanding the
NO–ET crosstalk provides the operating mechanism of plant
stress adaptation mechanism under these stresses. ET–NO
crosstalk leads to activation of MAPK cascades and poly-
amine synthesis during cadmium stress in soybean and pea
seedlings (Chmielowska-Bąk etal. 2013; Rodríguez-Serrano
etal. 2006). Similarly, treatment of Cd and spermine leads to
NO generation in roots in Triticum aestivum seedlings which

Journal of Plant Growth Regulation
1 3
ultimately inhibits the root growth (Groppa etal. 2008). Fe-
deficiency signaling is affected by NO–ET crosstalk with the
induction of several genes associated with the iron accumu-
lation and transport (Garcia etal. 2010). Other than heavy
metals, NO–ET module works profoundly in salinity stress
(Liu etal. 2015).
NO–SA Crosstalk
Salicylic acid is an important plant hormone essential for
plant growth, development, and pathological processes.
NO–SA interplay regulates plant stress responses; for
example, combination of NO and SA prevents nickel tox-
icity by proline accumulation, reduced lipid peroxidation,
and chlorophyll content enhancement in Brassica napus
(Kazemi etal. 2010). On contrary to this, NO–SA com-
bination increases the Cd concentration in the cell wall of
Arachis hypogaea to prevent organelles from toxic effects
(Xu etal. 2015). In addition, ROS also participates with
NO in SA-induced closure of stomata (Khokon etal. 2011).
Here, SA activates peroxidase enzyme that promotes ROS
accumulation, leading to NO generation in guard cells and
ultimately stomata closure. Similarly, the combination of
NO–SA acts synergistically in alleviating salt stress by
improving divalent cations absorption (Dong etal. 2015).
Again, pretreatment of SA in Spinacia oleracea modulates
the NR activity for improvement in chilling tolerance (Aydin
and Nalbantoğlu 2011). This implicates SA interplay in the
NO generation pathway that can be used for the future gen-
eration of climate-smart crops.
NO–Sulfur Crosstalk
Sulfur (S) is a vital part of essential molecules, such as the
thioredoxin system, reduced glutathione (GSH), methionine,
and coenzyme A. Under salt stress conditions, NO–S cross-
talk changes the ET and ABA levels in guard cells to affect
the photosynthetic and stomatal response. NO interacts with
GSH and forms S-nitrosoglutathione (GSNO) to impart bet-
ter stress tolerance (Wang etal. 2015b). Further, NO–sulfur
crosstalk is essential for S-assimilation, as shown for Cys
synthesis modulation by ET production (Fatma etal. 2016).
Interactions of nitro and sulfhydryl groups are crucial during
nitration (Leterrier etal. 2011). NO also interacts with H2S
to provide salinity stress tolerance by upregulation of salinity
stress-induced genes like HvSOS1 and HvHA1 (Chen etal.
2015). This process is mainly governed by transcriptional
activation of vacuolar transport and compartmentalization
genes where NO acts as a signaling molecule.
NO–BRs Crosstalk
Brassinosteroids (BRs) are the novel class of plant hormones
implicated in plant growth, development, and immunity.
Recently, reports have suggested NO–BRs interplay in
plant root architecture as well as in root development (Tossi
etal. 2013). In addition, alleviation of Copper toxicity was
mediated by NO–BRs crosstalk in conjunction with ABA in
Raphanus sativus seedlings (Choudhary etal. 2012).
These reports suggest precise NO interaction with hor-
mones and other signaling components for fine-tuning the
plant growth, development, and stress response. Further
experiments on targeted NO homeostasis in controlled
induced conditions (Temporal and spatial) will shed light
on components of these cross-talks. Direct target identifica-
tion of NO signaling in biosynthesis, perception, and signal
transduction will be important to decipher the underlying
regulatory mechanisms.
Molecular Understanding ofNOCrosstalk During
Plant Stress
Nitric oxide is an essential gasotransmitter with a regulatory
role during plant growth and development. These regulatory
roles are amplified when NO crosstalk with other signaling
molecules or PGRs. The NO crosstalk with other compounds
regulate various biosynthetic pathways, signaling processes,
and metabolism and ultimately maintains plant growth and
development under multiple stresses. Therefore, the mecha-
nism of NO crosstalk under numerous abiotic stress toler-
ance is highlighted in Fig.4 and discussed in this section.
The NO crosstalk with PGRs and other signaling compounds
under multiple stresses and their improved traits for stress
tolerance are presented in Table1.
Drought Stress
It has been well established that NO is required for ABA-
induced stomatal closure and provides tolerance to plants
under drought stress (Garcia-Mata and Lamattina 2002).
Further, stomatal closure is regulated by ABA-induced NO
production in Arabidopsis guard cells. Although, Desikan
etal. (2002) revealed no stomatal closer in response to
ABA in double-mutant nia1 nia2, which are associated with
reduced NO production. This suggests the role of other inter-
mediaries in NO–ABA crosstalk. Plants accumulate more
ABA in drought stress, leading to activation of NADPH
oxidase enzymes such as RBOHF and RBOHD (respiratory
burst oxidase homolog F and D), resulting in more super-
oxide accumulation. This phenomenon is needed for sto-
matal closure through NO production via NR and activates
MAPK signaling cascade (Desikan etal. 2002; Bright etal.
2006; Fency etal. 2017). Several studies showed that the

Journal of Plant Growth Regulation
1 3
exogenous application of NO could promote the accumula-
tion of ABA in plants under drought stress, which can be
reversed by the application of NO scavenger (Zhao etal.
2001; Fency etal. 2017). Thus, there is ambiguity in NO’s
function in the increased or decreased ABA signaling under
water deficit. The NO-mediated S-nitrosylation could be
crucial for drought tolerance, as reported in several studies.
The central component of ABA signaling is OST1/SnRK2.6
(open stomata 1/sucrose non-fermenting 1-related protein
kinase 2.6) induced by the S-nitrosylation process in plants.
The protein kinase activity of OST1/SnRK2.6 is inhibited
by S-nitrosylation at Cys 137 position. This ABA-induced
S-nitrosylation of SnRK2.6 acts as a negative feedback regu-
lator of ABA signaling in plants (Wang etal. 2015a).
There are reports which emphasize the role of transcrip-
tion factors from MYB family to regulate tolerance mecha-
nism in plants under abiotic stresses. Transcription factor,
AtMYB2, is associated with salt, and drought stress tends
to inhibit its DNA binding activity after the S-nitrosylation
process (Serpa etal. 2007). Another transcription factor,
AtMYBB30, has been found to lose its DNA binding activ-
ity after S-nitrosylation (Tavares etal. 2014; Fency etal.
2017). Thus, protein kinases and transcriptions factors play
a vital role in mitigating plant stress under water deficit. Sev-
eral recent studies suggested that NO crosstalk is a central
player of drought stress tolerance. Wang etal. 2020 reported
that crosstalk between NO and H2S mediates priming-
induced drought tolerance via accumulation of osmolytes
(proline and glycine betaine). Sami etal. (2018) found that
NO crosstalk with phytohormones mediates the alteration in
plant metabolism, and post-translational modification such
as S-nitrosylation confers multiple stress tolerance includ-
ing drought. Likewise, Shan etal. (2015) reported that
NO induced by exogenous application of JA upregulated
the AsA–GSH cycle activity and reduced drought stress in
wheat crops. Moreover, recent studies suggested that NO
crosstalk with other signaling compounds and phytohor-
mones mitigate the drought stress by improving the relative
water contents, photosynthetic capacity, antioxidant defense,
ionic balance, and other plant growth attributes (Shan etal.
2015; Khan etal. 2017; Kaya etal. 2019). However, the
exact mechanism of NO crosstalk under drought tolerance
at the molecular level needed to be explored. These stud-
ies point out that NO crosstalk plays a crucial role dur-
ing drought stress tolerance by antioxidant and osmolytes
regulation.
Temperature Stress
Plant growth and development are severely affected by low
temperature (cold and freezing) and high-temperature stress.
Plants have evolved mechanisms during evolution to combat
Fig. 4 Illustrated the physiological, biochemical, and molecular mechanisms of NO crosstalk under stress conditions. Under abiotic stresses,
plant faces the drastic effects on several physiological, biochemical, and molecular processes, which are balanced by NO crosstalk

Journal of Plant Growth Regulation
1 3
Table 1 Highlights the NO crosstalk with PGRs and other signaling compounds under multiple stresses and their improved traits for stress tolerance
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
Heavy metal stress
NO–H2S Lead stress (2mM Pb+2)Sesamum indicum Improve antioxidants defense
mineral homeostasis, and
restricted uptake and trans-
location of Pb
Improved chlorophyll
and carotenoid content,
enhanced photosynthesis
efficiency, and reduced
proline contents
Amooaghaie and Enteshari
(2017)
NO–H2S Cd stress (20µM) Vigna radiata Improved antioxidant defense
and ascorbate–glutathione
cycle activity, and enhanced
phytochelatins
Enhance photosynthetic rate,
accumulation of carbohy-
drates, chlorophyll content,
stomatal conductance
Khan etal. (2020)
NO–H2S Cd stress (0.10mM) Triticum aestivum L Reducing oxidative stress and
Cd uptake, improved anti-
oxidant capacity, and uptake
of some essential nutrients
Enhanced total plant dry
matter, chlorophyll a and
b contents, photochemical
efficiency, and leaf water
content
Kaya etal. (2020a, b)
ROS–Ca–NO Cd toxicity(50µM) Pisum sativum Expression of pathogen-
related PrP4A, chitinase,
and defense-related HSP71.2
Upregulation of jasmonic
acid, ethylene, antioxidant
enzyme regulation
Rodriguez-Serrano etal. (2009)
Ca–H2O2–NO Copper toxicity (10µM
CuCl2)Ulva compressa Activation of genes of calmo-
dulins, calcium-dependent
protein kinase, oxidation and
nitrosylation of antioxidant
protein
Activation of electron
transport chain, regula-
tion of photosynthesis rate,
activation of Krebs cycle
enzymes, and increased
expression of antioxidant
enzymes
González etal. (2012)
NO–ROS Arsenate stress (100µM) Oryza sativa Diluting the As toxicity by
improving root structure
architecture, redox balancing
of ascorbate and cell cycle
dynamics
New adventitious root
formation, and improved
accumulation of primary
root biomass
Kushwaha etal. (2019)
NO–H2O2Arsenate stress (50µM) Glycine max var. JS 20–29 Regulation of ascorbate–glu-
tathione cycle
Promoting vascular seques-
tration, mitigate oxidative
stress, and increase cell
viability
Singh etal. (2020)
Polyamine–NO Cd toxicity (1.5mM) Vigna radiataL Upregulation of metal
detoxification, antioxidant
defense, and methylglyoxal
detoxification system
Improved plant height, root
length, leaf area, seedling
dry weight, reduce chlo-
rophyll degradation, and
enhanced accumulation of
osmoprotectants
Nahar etal. (2016)

Journal of Plant Growth Regulation
1 3
Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
NO–H2S Al toxicity (50 and 100µM
AlCl3)Glycine maxL Regulate citrate exudation
via GmMATE 13 and
GmMATE 47 transporters
Reduced root inhibition, Al
accumulation by 33.1%,
increase citrate exudation
by 36.5%, and upregulation
of plasma membrane H+—
ATPase
Wang etal. (2019)
NO–H2S Co toxicity (150–300µM) Triticum aestivumL. cv.Ekiz Modulating photosynthesis,
chloroplastic redox, and
antioxidant capacity
Induce relative growth rate,
relative water content
(RWC), ion homeostasis,
Fv/Fm ratio, carbon assimi-
lation rate, stable ascor-
bate–glutathione cycle in
chloroplast, and antioxidant
enzymes
Ozfidan-Konakci etal. (2020)
NO–H2S Cr Toxicity (100µM Cr) Solanum lycopersicumL.
Mill. cv. BL-1076
Enhance GSH metabolism,
antioxidant enzymes, sulfur
assimilation and bosting
immunity
Increase in shoot and root
length, fresh and dry
weight, enhance chl a,
chl b, RuBisCo activity,
photosynthetic rate, cysteine
biosynthesis and osmotic
adjustment by enhancing
glycine betaine and total
soluble sugar contnt
Almari etal. (2020)
Si–NO Cd toxicity (20–50mg/kg) Zea mays Decrease uptake and accumu-
lation of Cd
Improve photosynthesis by
30%, higher number of
grains (17%), decreased
uptake of cd in root, shoot,
and grains by 41, 34, and
51%, respectively,
Liu etal. (2020)
Drought stress
Polyamine–NO 0,5,10, and 15h withdrawal
of water Cucumis sativuscv. Dar Reduced membrane permea-
bility and lipid peroxidation
Improve RWC and antioxidant
enzymes activity
Arasimowicz-Jelonek etal.
(2009)
Cytokinin–NO 18% PEG+Hoagland solution Zea mays L Induced photosynthetic adapt-
ability, reduce ROS-medi-
ated oxidative stress
Enhance nitrate reductase
activity, improve photosyn-
thetic performance index,
and stimulation of more
energy conversion to elec-
tron transfer
Shao etal. (2010)
NO–ET Withdrawal of water for
18days Hordeum vulgarevar. golden
promise
Improve polyamine biosynthe-
sis and proline content
Improve RWC, transpiration
rate, and increase arginine
content
Montilla-Bascón etal. (2017)

Journal of Plant Growth Regulation
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Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
NO–H2S 15% PEG+Ruakura’s nutrient
solution Triticum aestivum L Sustaining antioxidant
enzyme, osmotic adjust-
ment, and cysteine homeo-
stasis
APX, GR, POX, CAT, and
SOD content increased,
reduced ion leakage,
improve RWC, and accumu-
lation of proline and glycine
betaine
Khan etal. (2017)
NO–BRs 80 and 40% field capacity (Capsicum annuumL.) cv.
“Semerkand
Induce antioxidant system,
and aggravated oxidative
stress
Improve shoot fresh weight,
RWC, total chlorophyll,
total soluble sugar, proline,
leaf Ca+2 contents and activ-
ity of SOD, CAT and POD
and maintain ascorbate and
glutathione
Kaya etal. (2019)
NO–JA 15% PEG+Hoagland solution Triticum aestivum L Regulation of ascorbate–glu-
tathione cycle
Elevated the ratio of GSH/
GSSG, redox maintain
by regulating APX, GR,
DHAR, and MDHAR
Shan etal. (2015)
Salt stress
Ca–H2O2–NO Nacl (0, 50, 100, and
200mM) Chenopodium quinoa Improved α-amylase activity
and water soluble sugar
content
Improved germination rate,
germination rate index,
and reduce mean time of
germination
Hajihashemi etal. (2020)
24-Epibrassinolide–SNP 100mM NaCl Brassica juncea L. cv. Varuna Enhance proline, nitrogen
metabolism, and ABA
crosstalk
Improvements in root length,
root fresh and dry weight,
total protein and K+ content
Gupta etal. (2017)
Auxin–GA–NO 0, 50, 100, 150, 200, and
250mM NaCl Arabidopsis thaliana Integration of IAA7 and
RGL-3 proteins
Reduce electrolyte leakage,
stabilization of proteins, and
improve seedling survival
under stress,
Shi etal. (2017)
NO–H2S 100mM NaCl Capsicum annuumL Induced melatonin, and
reduce oxidative stress
Improve 31.04, 33.30, 25.11
total, shoot, and root bio-
mass, respectively, decrease
H2O2, electrolyte leakage
and MDA content, promote
CAT, SOD activity and
enhance mineral nutrition
Kaya etal. (2020a, b)

Journal of Plant Growth Regulation
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Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
NO–Phytohormones 80mM NaCl Lactuca sativa Stable hormonal balance,
reducing Na+ accumula-
tion, and activating defense
mechanisms
Enhance Na+ concentration
5- and 3-folds in leaves and
roots, reduce H2O2 concen-
tration, electrolyte leakage
and cell damage, enhance
antioxidant enzymes activ-
ity and 88% increment in
proline concentration
Compos etal. (2019)
NO–ABA 150mM NaCl Triticum aestivumL.cv. Yang-
mai 158
Enhancing the activity of
Δ-pyrroline-5-caroxylase
synthetase and inhibition of
proline dehydrogenase
Enhance water retention up
to 7.9%, improve seedling
survival and osmotic adjust-
ment
Ruan etal. (2004)
NO–H2S 100mM NaCl Medicago sativa Induce the transcript of
antioxidant enzymes such as
SOD, APX, CAT, and POD
Improve seedling germina-
tion and seedling growth,
and re-establishment of ion
homeostasis such as high K/
Na ratio
Wang etal. (2012)
NO–SA 100mM NaCl Glycine max L. cv.
Union × Elf
Improve antioxidant defense
and ion homeostasis
Balanced the Na/K ratio,
improved germination
percentage, elevate the
concentration of anthocya-
nin, and improve antioxidant
enzymes SOD, PPO, LOX,
and PAL
Simaei etal. (2012)
NO–H2O2150mM NaCl Citrus aurantiumL Alteration of oxidation and
S-nitrosylation pattern of
stress proteins
Reduce MDA content,
improve photosynthesis
and defense/detoxification
proteins
Tanou etal. (2009)
NO–Calcium nitrate 100mM NaCl T. aestivumL. cv. Jimai 22 Maintain ion homeostasis and
antioxidant defense
Improve RWC, chlorophyll
and soluble sugar content,
reduce electrolyte leakage
and lipid peroxidation
Tian etal. (2015)
ABA–NO–Auxin 150mM NaCl Solanum lycopersicumL. cv.
Ailsa Craig
Modulation of plasma mem-
brane H+-ATPase coupling
and antioxidant defense
Increase root dry biomass,
nitrate reductase activity,
ionic and osmotic homeo-
stasis, redox balancing,
and enhance antioxidant
enzymes
Santos etal. (2020)

Journal of Plant Growth Regulation
1 3
Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
NO–JA 200mM NaCl Solanum lycopersicum L Upregulating the antioxidant
metabolism, osmolytes
synthesis, and metabolite
accumulation
Enhance 200 and 250%
shoot and root dry weight,
increase of (208, 100,
162.79, and 7.69%) chl a,
chl b, total chl, and carot-
enoid content, respectively,
increase in SOD, GR, APX,
and CAT activity
Ahmad etal. (2018)
Heat stress
 H2O2–NO 48°C for 18h Medicago truncatula H2O2-induced thermotoler-
ance
Improve maize seedling sur-
vival under heat stress
Li etal. (2015)
NO–H2O245°C for 24h Arabidopsis thaliana Stimulation of DNA binding
capacity to heat shock fac-
tors and accumulation of
heat shock protein
Increase survival rate of
seedlings, overexpression
of AtNIA1&2, and induce
expression of heat shock
proteins
Wang etal. (2014)
NO–ABA 45°C for 2h Phragmites communisTrin Integrate membrane stability,
and reduced ion leakage
Improve relative growth rate,
reduce MDA content and
membrane permeability
Song etal. (2008)
NO–Ca+2 42°C for 4h Solanum lycopersicum Improve antioxidant defense,
osmotic adjustment, and
photosynthetic capacity
Enhanced proline and glycine
betaine content by 69.25
and 81.08%, respectively,
decrease MDA content and
H2O2 by 36.13 and 44.82%,
enhanced chl a and chl b
contents, improve NR, SOD,
POD, GR, and APX activity
Siddiqui etal. (2017)
Ca–NO–H2O246°C for 10min Triticuma estivumL Mediate the signal transduc-
tion for heat tolerance
Increase survival of seedlings,
NR activity, and enhance
antioxidant capacity
Karpets etal. (2016)
Cold stress
NO-MPK1/212°C for 3days and 4 °C for
5days Solanum lycopersicumL. cv.
Condine Red
Induction of S-nitrosylated
glutathione reductase
(GSNOR) and nitrate reduc-
tase activity
Reduced chilling photo-inhi-
bition and lipid-peroxidation
Lv etal. (2017)
Polyamine–ABA–NO–H2O24°C for 0, 12, and 24h Lycopersicon esculentumMill Enhance nitrate reductase,
expression of defense-
related genes
Reduced electrolyte leakage Diao etal. (2017)
NO–Sphingolipid Chilling stress Plants Modified the synthesis of
phytosphingosine phosphate
(PHS-P) and ceramide phos-
phate (Cer-P)
Alters the activity of kinase
and phosphatase enzymes,
and stables integrity of
membranes
Guillas etal. (2011)

Journal of Plant Growth Regulation
1 3
Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
NO–H2O211°C during day time and
7°C during night for 0, 2, 5,
7, 24, and 48h
Cucumis sativusL Improving the efficiency of
Calvin cycle and Ascorbate–
Glutathione cycle
Improve the content of
glucose, fructose, starch,
sucrose, and expression
levels of acid invertase (AI),
sucrose synthase (SS), and
sucrose phosphate synthase
(SPS)
Wu etal. (2020)
NO–PA 14/4°C day/night temperature
for 10days Zingiber officinaleRoscoe Improving antioxidant defense
and reduced chilling-
induced photo-inhibition
Improve photosynthetic
pigments, modulate fatty
acid composition to reduce
lipid peroxidation, improve
antioxidant enzymes SOD,
CAT, APX, and GPX activ-
ity (73, 51, 72, and 77%,
respectively)
Li etal. (2014)
NO–H2O2 − 2°C for 24h Triticum aestivumL. cv.
Yangmai 16
Modification of photosynthe-
sis and antioxidant system
Alleviate Fv/Fm ratio,
maintains the SOD, CAT,
APX, and GR activity, and
elevation of photosynthetic
genes
Si etal. (2017)
Nutrient deficiency
Auxin–ET–NO Fe deficiency non-graminaceous plants Activation of Fe acquisition
genes such as AtFIT and
SIFER
Development of subapical
root hair and transfer cells
Romera etal. (2011)
NO–H2S Fe deficiency Capsicum annuumL Induced melatonin, and
reduce oxidative stress
Improve 35.06, 45.82,37.99
total, shoot, and root bio-
mass, respectively, decrease
H2O2, electrolyte leakage,
and MDA content, promote
CAT, POD activity, and
enhance Fe content
Kaya etal. (2020a, b)
CO–NO–Auxin Fe deficiency Arabidopsis thaliana Increased expression of FIT1
gene and Fe uptake
Enhance root hair develop-
ments, Fe acquisition, and
auxin polar transport
Yang etal. (2016)
NO–ET P deficiency Oryza sativa Improve expression of
phosphorus transporter gene
OsPT2 and pectin content
Improve root attributes, reu-
tilization of cell wall P, and
translocation of P from root
to shoot
Zhu etal. (2017)
NO–SLs N & P deficiency Oryza sativa Induction of seminal root
elongation
Improve 18 and 24% seminal
root elongation under N and
P deficiency, and increase
root meristem activity
Sun etal. (2016)

Journal of Plant Growth Regulation
1 3
temperature stresses. NO cross-talk plays an essential role
in a plant’s battle against temperature fluctuations (Majlath
etal. 2012; Parankusam etal. 2017; Kolbert etal. 2019). For
example, exogenous application of NO induces the expres-
sion of MfSAMS1 and thereby increased S-adenosylmethio-
nine (SAM), polyamines (PAs) concentration, and PA oxida-
tion under cold stress in alfalfa (Medicago sativa) (Guo etal.
2014). In this context, SAMs are acting by up-regulating PA
oxidation and H2O2-induced antioxidant defense (Guo etal.
2014). There is an antagonistic relationship between NO and
ET during fruit ripening in cold stress. For example, Zaharah
etal. (2011) studied the different NO levels for fumigation
on mango fruits and observed a significant reduction in ET
production during fruit ripening. They also found reduced
chilling injury, softening, ripening, and delayed fruit color
development in mango fruits under cold storage conditions.
Thus, cross-talk between NO and ET delays fruit senescence
and thereby fruit quality during cold fruit storage.
The crop productivity is adversely affected by heat stress
due to adverse effects on photosynthesis, respiration, mem-
brane stability, membrane permeability, and water relations
(Kolbert etal. 2019). Heat stress affects cytoskeleton struc-
ture, cell metabolism, and membrane fluidity by increasing
the accumulation of proteins that affect ROS, NO, and other
phytohormones (Wahid etal. 2007). It has been suggested
that NO acts via reduction of ROS level through activating
antioxidant enzymes such as catalase (CAT), superoxide dis-
mutase (SOD), ascorbate peroxidase (APX), and expression
of heat shock factor during heat stress in plants (Neill etal.
2002; Song etal. 2006; Wang etal. 2014; Fency etal. 2017).
Exogenous application of NO (pre-treatment) increased
the survival rate of maize (Zea mays) seedlings and wheat
(Triticum aestivum) leaves and reduced heat stress-induced
loss in rice (Oryza sativa) seedlings (Lamattina etal. 2001;
Uchida etal. 2002). Similarly, crosstalk between NO and
H2S regulates the H2O2-induced thermotolerance in maize
seedlings. It also affects the Ca and calmodulin levels in
tobacco seedlings (Li etal. 2015). These reports suggest
that NO crosstalk needed to be further explored for its role
during thermotolerance in plants.
Salinity
Soil salinity is one of the main factors for reduced crop
production in major food and fodder crops and, by large,
emerged due to extensive use of groundwater for irrigation
across the world (Slinger etal. 2005). The role of NO to
address plant salt tolerance has been extensively studied in
various plant species (Zhang etal. 2007b; Hasanuzzaman
etal. 2018). For example, artificial application of sodium
nitroprusside (SNP, act as NO donor) protects plants against
salt stress by altering growth habit and protects from oxida-
tive damage by maintaining plant ion homeostasis (Zhang
Table 1 (continued)
Type of crosstalk Stress Plant Tolerance mechanism Improved plant traits References
ET–NO Mg deficiency Arabidopsis thaliana Induced root hair morpho-
genesis
Regulate auxin concentration
and ACS and ACO activity
in root
Liu etal. (2018)
Other environmental stresses
NO–Ca+2 500 and 100μmol m−2 s−1
PPFD light in stress and
control (High irradiance
stress)
Festuca arundinacea Synergistically alters the
antioxidant enzymes activi-
ties (SOD, CAT, and MDA)
content
Decrease ion leakage and
increase Ca content
Xu etal. (2016)
NO–ABA Under low light Festuca arundinacea Induce photosynthesis and
antioxidant system
Increase in chlorophyll con-
tent, activation of carboxy-
lation enzymes, enhance
light harvesting capacity,
RuBisCo regeneration
capacity, induce CAT, SOD,
POD, and APX activity
Zhang etal. (2018)

Journal of Plant Growth Regulation
1 3
etal. 2006b). Moreau etal. (2008) studied the effect of NO
using Atnoa1 plants (defective in GTPase activity) and con-
cluded a role of NO under salt stress. The S-nitrosylated
proteins play an essential role under NaCl stress and nega-
tively affect salt concentration (Tanou etal. 2009). However,
exogenous application of NO increased (pre-treatment) the
concentration of NaCl-induced S-nitrosylated protein that
played a protective role under stress conditions (Tanou
etal. 2009). Arora etal. (2016) stated that NO can interact
with different metal proteins such as zinc–sulfur clusters,
heme–iron, copper, and iron–sulfur clusters and form a
stable metal nitrosyl complex that can modify the protein
structure as well as function. They also observed the binding
of thiols to NO and their role in transporting it to the site of
action. Camejo etal. (2013) observed decreased S-nitrosyla-
tion of proteins during short-term and long-term salt concen-
trations. A recent report suggested that pretreatments with
CaCl2, H2O2, and SNP improve β-amylase activity, which
influences starch breakdown and improved seedling estab-
lishments in Chenopodium (Hajihashemi etal. 2020).
Similarly, Singh and Bhatla (2018) reported that NO bind
with ACC oxidase and form a ternary complex (ACC–ACC
oxidase—NO), which lead to a reduction of ethylene biosyn-
thesis and induce LR formation in sunflower under salt stress
conditions. Likewise, Arora and Bhatla (2017) reported that
melatonin and NO crosstalk maintain redox homeostasis
and differential modulations of SOD isoform in sunflower
under salt stress. Moreover, several recent updates on NO
crosstalk with other signaling compounds alleviate salinity
stress (Fatma etal. 2016; Shi etal. 2017; Kaya etal. 2019).
However, there was a significant reduction in S-nitrosylation
under long-term salt treatment. Thus, there were inconsist-
encies between different studies due to differences in plant
genotypes/species, tissue-examined, variable NaCl concen-
tration, and duration of time. Further, NO, S-nitrosylation,
and associated enzyme GSNOR play an essential role in
mitigating salt stress in plants. However, there is a need to
focus more on proteomic approaches to identify salt stress
signaling components directly and indirectly regulated by
redox enzymes and GSNOR.
Heavy Metal Stress
Heavy metals (HMs) such as mercury(Hg), cadmium (Cd),
arsenic (As),chromium(Cr), thallium (Tl), and lead (Pb)
have an unknown biological function and are very harm-
ful for plants in higher concentrations. They tend tobio-
accumulate (accumulation in plant cell with the time) and
non-biodegradable. Plants taking up these HMs through
roots from the soil and hyper-accumulation of these HMs
bring rapid cellular homeostasis changes (Ghori etal. 2019).
Nitric oxide (NO) has a broad spectrum of regulation func-
tions with widespread inter- and intra-cellular messenger
activities (Wei etal. 2020). Many enzymatic reactions
accelerated through NO, including nitrate reductase and
L-Ar-dependent nitric oxide synthase-related reactions, an
essential component for HMs tolerance (Wei etal. 2020).
Like other stresses, NO also plays a vital role in enhancing
antioxidant enzyme activities and alleviates the toxicity of
HMs. Rodriguez-Serrano etal. (2009) studied the cadmium
(Cd) toxicity effect on nitric oxide (NO) metabolism in pea
(Pisum sativum), and results implicated that Cd toxicity
inactivated the NO synthase-dependent NO production. Con-
sequently, it leads to calcium (Ca) deficiency in leaves. This
suggests that the Cd toxicity effect can be counteracted by
calcium (Ca). Exogenous SNP application acts as NO donor
to the rice leaves and reduces the Cu and NH4+ accumulation
(Mazid etal. 2011). Moreover, Wang etal. (2010) report that
NO actions reduce Cu toxicity through antioxidant enzymes,
which accelerates the metallothionein and metallothionein.
There was an increase in total chlorophyll content and fresh
or dry weight of leaves against Cu toxicity in tomato. Also,
reports suggested the cross-protection role of putrescine and
NO toward Cd toxicity in mung bean seedlings (Nahar etal.
2016). Singh etal. (2008) also found the detoxification and
anti-oxidative properties of NO for Cd and Cu toxicity in
wheat. Exogenous application of SNP accelerated the ROS
scavenging enzymes, which reduced the accumulation of
H2O2 and diminished the toxic effect of Cu in tomato (Cui
etal. 2009). Similar results were observed in rice against
Cd toxicity. The exogenous application of NO ameliorates
the tolerance against Cd toxicity by increasing the pectin
and hemicelluloses content in the root cell wall (Xiong etal.
2009). In soybean seedlings, the short-term treatment with
Cd accelerated the geneS expression of encoding the pro-
tein of NO synthesis and ET (Chmielowska-Bak etal. 2013;
Kolbert etal. 2019). Likewise, recent studies on the role of
NO crosstalk on HMs stress tolerance suggest that it acts via
regulating the root growth (biomass, formation, and length),
photosynthetic activity, antioxidant defense, accumulation of
osmoprotectants, and inhibition of HMs transport to grain
and above plant parts (Khan etal. 2020; Kaya etal. 2020a,
b; Singh etal. 2020).
Other Stresses
During the stress condition, NO is generated from L-arg-
dependent NO synthase. This NO can react with superoxide
(O2−) to form ONOO, a powerful oxidant that can lead to
tyrosine nitration of proteins. Tyrosine nitration is an indica-
tor of nitrosative stress in plants which acts as the defense
system for the plants during stress (Nabi etal. 2019). Recent
reports have explained that a wide range of abiotic stresses
is leading to NO synthesis and signaling. It is gaining more
attention mainly due to its properties like small size, no
charge, free radicals, and highly diffusible nature across

Journal of Plant Growth Regulation
1 3
the cell membranes and many plant physiological functions
like growth, development, maturation, and senescence. It
is believed that NO signaling is involved in the respiratory
electron transport system in mitochondria, where it confers
the modulation of ROS and accelerates the antioxidant sign-
aling defense system in the plant, which is exposed to several
abiotic factors (Mazid etal. 2011; Santisree etal. 2020).
The regulatory function of NO crosstalk is not only limited
to drought, cold, heat, cold, and HMs stress but also has a
regulatory role during combined stress, nutrient deficiency,
and high and low light stress. For example, some studies
suggested the NO crosstalk role during the N, P, Mg, and
Fe deficient soil and suggested that it regulates the nutrient
deficiency by improving root attributes, better translocation
of ions, and regulating phytohormones concentration (Yang
etal. 2016; Su etal. 2016; Zhu etal. 2017).
Conclusion andPerspectives
NO has gained attention during the last few decades due to
its substantial role as a gasotransmitter and defense mol-
ecule during numerous environmental stresses. Most of the
NO crosstalk functions are associated with redox, oxida-
tive, ion, and hormonal homeostasis through the modu-
lations of downstream genes in the signaling pathway.
A large body of research has addressed the elementary
mechanism of NO crosstalk regarding plant development
and its role as a central hub under abiotic stress tolerance.
Broadly, these studies indicate how NO crosstalk with
other signaling compounds regulates the cell machinery
in optimum ways. Although the mode of NO crosstalk
with other signaling compounds is not always synergistic,
sometimes antagonist responses also benefit plants under
stressful situations. Moreover, the NO crosstalk response
under similar stress could vary plant by plant due to the
complex nature of signaling compounds and their interact-
ing signals. Components of this crosstalk include genes,
transcription factors, and enzymes associated with the NO
synthesis and expression during different environmental
signals, which need to be more elaborate to understand
the exact mechanism of NO crosstalk. However, most
studies have shown that the NO crosstalk regulates stress
responses via the synthesis and expression of SOD, CAT,
APX, MDA, GR, POX, DHAR, and other antioxidant
defense enzymes and genes. These factors help in the
maintenance of oxidative stress situations at the cell level.
Likewise, stress proteins (HSP), phytochelatins, signaling
cascades (MAPK, CDPK, GMP), osmoprotectants (sugar,
proline), and ion proteins (H+-ATPase) are linked with
NO crosstalk. However, the molecular mechanism of NO
crosstalk is still unclear and needs to explore more for
deep understanding and development of multiple stress
tolerance varieties. Most studies focused on single stress
conditions, and the mechanism of NO crosstalk under
combined and multiple stress still needs to be deciphered.
These studies are limited to the germination and vegeta-
tive stage. However, the responses of NO crosstalk under
the reproductive phase and yield attributing traits are still
unclear, which need to be investigated to develop higher
yield lines under stress situations. In recent years, integrat-
ing omics approaches (integrating genomics, proteomics,
metabolomics, and transcriptomics) has further clues on
understanding gene–gene, gene–protein, gene–environ-
ment interactions and can be a potential approach to under-
standing the complex NO signaling mechanisms. Further,
the integration of omics approaches to next-generation
techniques explores the signaling mechanism at molecular
levels and insights into full understanding of regulatory
pathways and crosstalk mechanism to develop climate-
resilient crops. Moreover, the engineering of NO biosyn-
thesis and crosstalk pathways will be crucial for providing
novel insights into the crop stress improvements program.
Acknowledgements Authors are very thankful to the researchers
whose excellent work has been cited in the presented study, which
helps us to prepare an up to date review.
Author Contributions Author contribution statement: RKS and HSJ
conceived the idea. All authors contributed equally in writing and fig-
ure and table preparation. All authors have read and approved the final
version of review.
Data Availability The present paper covered the concluded remarks
on No Nitric oxide cross-talking covered in various findings studied
by researchers.
Declarations
Conflict of interest The authors declare they do not have any conflict
of interest.
Ethical Approval All the authors have been agreed to submit it.
Consent to Participate Before the submission of paper, all the author
have given the consent to publish.
Consent to Publish All the authors have given the consent to publish.
References
Ahmad P, Abass Ahanger M, Nasser Alyemeni M, Wijaya L, Alam
P, Ashraf M (2018) Mitigation of sodium chloride toxicity in
Solanum lycopersicum L. by supplementation of jasmonic acid
and nitric oxide. J Plant Interact 13:64–72
Alamri S, Ali HM, Khan MIR, Singh VP, Siddiqui MH (2020) Exoge-
nous nitric oxide requires endogenous hydrogen sulfide to induce
the resilience through sulfur assimilation in tomato seedlings

Journal of Plant Growth Regulation
1 3
under hexavalent chromium toxicity. Plant Physiol Biochem
155:20–34
Amooaghaie R, Enteshari S (2017) Role of two-sided crosstalk
between NO and H2S on improvement of mineral homeostasis
and antioxidative defense in Sesamum indicum under lead stress.
Ecotoxicol Environ Saf 139:210–218
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Inter-
action between polyamine and nitric oxide signaling in adap-
tive responses to drought in cucumber. J Plant Growth Regul
28:177–186
Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA
crosstalk with ethylene and nitric oxide in seed dormancy and
germination. Front Plant Sci 4:63
Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sun-
flower seedling growth under salt stress accompanying differ-
ential expression of Cu/Zn SOD and Mn SOD. Free Radic Biol
Med 106:315–328
Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of
nitric oxide crosstalk with reactive oxygen species scavenging
enzymes during abiotic stress tolerance in plants. Free Radic
Res 50:291–303
Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan
NA (2017) Nitric oxide signaling and its crosstalk with other
plant growth regulators in plant responses to abiotic stress.
Environ Sci Pol Res 24:2273–2285
Astier J, Gross I, Durner J (2018) Nitric oxide production in plants:
an update. J Exp Bot 69:3401–3411
Aydın B, Nalbantoğlu B (2011) Effects of cold and salicylic acid
treatments on nitrate reductase activity in spinach leaves. Turk
J Biol 35:443–448
Bai S, Yao T, Li M, Guo X, Zhang Y, Zhu S, He Y (2014) PIF3 is
involved in the primary root growth inhibition of Arabidopsis
induced by nitric oxide in the light. Mol Plant 7:616–625
Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama
R, Palma J, Lupiáñez JA, del Río LA (1999) Localization
of nitric-oxide synthase in plant peroxisomes. J Biol Chem
274:36729–36733
Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ,
Fernández-Ocana A, Chaki M, Romero-Puertas MC, Valderrama
R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglu-
tathione and expression of S-nitrosoglutathione reductase in pea
plants under cadmium stress. J Exp Bot 57:1785–1793
Basylinski DA, Hollocher TC (1985) Evidence from the reaction
between trioxodinitrate (II) and 15NO that trioxidinitrate (II)
decomposes into nitrosyl hydride and nitrite in neutral aqueous
solution. Inorg Chem 24:4285–4288
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-
Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant
systems are regulated by nitric oxide-mediated post-translational
modifications (NO-PTMs). Front Plant Sci 7:152. https:// doi. org/
10. 3389/ fpls. 2016. 00152
Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germina-
tion and de-etiolation, and inhibits hypocotyl elongation, three
light-inducible responses in plants. Planta 210:215–221
Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric
oxide by plant tissues. Plant Cell 16:332–341
Bethke PC, Libourel IGL, Jones RL (2006) Nitric oxide reduces seed
dormancy in Arabidopsis. J Exp Bot 57:517–526
Bethke PC, Libourel IGL, Aoyama N, Chung YY, Still DW, Jones RL
(2007) The Arabidopsis aleurone layer responds to nitric oxide,
gibberellin, and abscisic acid and is sufficient and necessary for
seed dormancy. Plant Physiol 143:1173–1188
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-
induced NO generation and stomatal closure in Arabidopsis are
dependent on H2O2 synthesis. Plant J 45:113–122
Camejo D, del Carmen R-P, Rodríguez-Serrano M, Sandalio LM,
Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes
in S-nitrosylation of pea mitochondrial proteins. J Proteom
79:87–99
Campos FV, Oliveira JA, Pereira MG, Farnese FS (2019) Nitric oxide
and phytohormone interactions in the response of Lactuca sativa
to salinity stress. Planta 250:1475–1489
Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010)
Nitric oxide acts downstream of auxin to trigger root ferric-che-
late reductase activity in response to iron deficiency in Arabidop-
sis. Plant Physiol 154:810–819
Chen YS, Lo SF, Sun PK, Lu CA, Ho TH, Yu SM (2015) A late embry-
ogenesis abundant protein HVA1 regulated by an inducible pro-
moter enhances root growth and abiotic stress tolerance in rice
without yield penalty. Plant Biotech J 13:105–116
Chmielowska-Bąk J, Lefèvre I, Lutts S, Deckert J (2013) Short term
signaling responses in roots of young soybean seedlings exposed
to cadmium stress. J Plant Physiol 170:1585–1594
Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LS (2012) Chro-
mium stress mitigation by polyamine-brassinosteroid applica-
tion involves phytohormonal and physiological strategies in
Raphanus sativus L. PLoS ONE 7:e33210
Cui X, Zhang Y, Chen X, Jin H, Wu X (2009) Effects of exogenous
nitric oxide protects tomato plants under copper stress. In: 2009
3rd International Conference on Bioinformatics and Biomedical
Engineering. 1–7
Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reac-
tive oxygen species and nitric oxide control early steps of the
legume—rhizobium symbiotic interaction. Front Plant Sci 7:454.
https:// doi. org/ 10. 3389/ fpls. 2016. 00454
Davis KL, Martin E, Turko IV, Murad F (2001) Novel effects of nitric
oxide. Annu Rev Pharmacol Toxicol 41:203–236
de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias
Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko
E, Prat S (2008) A molecular framework for light and gibberellin
control of cell elongation. Nature 451:480–484
Del Río LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003)
Plant peroxisomes, reactive oxygen metabolism and nitric oxide.
IUBMB Life 55:71–81
del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen
species signal molecules. Arch Biochem Biophys 506:1–11
Desikan R, Soheila AH, Hancock JT, Neill SJ (2001) Regulation of
the Arabidopsis transcriptome by oxidative stress. Plant Physiol
127:159–172
Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an
old enzyme: nitrate reductase-mediated nitric oxide generation is
required for abscisic acid-induced stomatal closure in Arabidop-
sis thaliana. Proc Natl Acad Sci USA 99:16314–16318
Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ
(2004) ABA, hydrogen peroxide and nitric oxide signalling in
stomatal guard cells. J Exp Bot 55:205–212
Diao Q, Song Y, Shi D, Qi H (2017) Interaction of polyamines, abscisic
acid, nitric oxide, and hydrogen peroxide under chilling stress in
tomato (Lycopersicon esculentum Mill.) seedlings. Front Plant
Sci. https:// doi. org/ 10. 3389/ fpls. 2017. 00203
Dong F, Simon J, Rienks M, Lindermayr C, Rennenberg H (2015)
Effects of rhizopheric nitric oxide (NO) on N uptake in Fagus
sylvatica seedlings depend on soil CO2 concentration, soil N
availability and N source. Tree Physiol 35:910–920
Dubovskaya LV, Bakakina YS, Kolesneva EV, Sodel DL, McAinsh
MR, Hetherington AM, Volotovski ID (2011) cGMP-dependent
ABA-induced stomatal closure in the ABA-insensitive Arabidop-
sis mutant abi1-1. New Phytol 191:57–69
Duszyn M, Świeżawska B, Szmidt-Jaworska A, Jaworski K (2019)
Cyclic nucleotide gated channels (CNGCs) in plant signalling-
Current knowledge and perspectives. J Plant Physiol 241:153035

Journal of Plant Growth Regulation
1 3
Falak N, Imran QM, Hussain A, Yun BW (2021) Transcription factors
as the “Blitzkrieg” of plant defense: A pragmatic view of nitric
oxide’s role in gene regulation. Int J Mol Sci 22:522. https:// doi.
org/ 10. 3390/ ijms2 20205 22
Fan HF, Du CX, Ding L, Xu YL (2013a) Effects of nitric oxide on the
germination of cucumber seeds and antioxidant enzymes under
salinity stress. Acta Physiol Plant 35:2707–2719
Fan HF, Du CX, Guo SR (2013b) Nitric oxide enhances salt tolerance
in cucumber seedlings by regulating free polyamine content.
Environ Exp Bot 86:52–59
Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in
plant abiotic stress. Plant Cell Environ 40:462–472
Fatma M, Masood A, Per TS, Khan NA (2016) Nitric oxide alleviates
salt stress inhibited photosynthetic performance by interacting
with sulfur assimilation in mustard. Front Plant Sci 7:521. https://
doi. org/ 10. 3389/ fpls. 2016. 00521
Feng J, Wang C, Chen Q, Chen H, Ren B, Li X, Zuo J (2013) S-nitros-
ylation of phosphotransfer proteins represses cytokinin signaling.
Nat Commun 4:1529
Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O
(2011) Nitric oxide causes root apical meristem defects and
growth inhibition while reducing PIN-FORMED 1 (PIN1)-
dependent acropetal auxin transport. Proc Nat Acad Sci USA
108:18506–18511
Floryszak-Wieczorek J, Milczarek G, Arasimowicz M, Ciszewski A
(2006) Do nitric oxide donors mimic endogenous NO-related
response in plants? Planta 224:1363–1372
Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Izbiańska K (2016)
The combined nitrate reductase and nitrite-dependent route of
NO synthesis in potato immunity to Phytophthora infestans.
Plant Physiol Biochem 108:468–477
Ford PC, Wink DA, Stanbury DM (1993) Autoxidation kinetics of
aqueous nitric oxide. FEBS Lett 326:1–3
Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina
L (2010) Characterization of a nitric oxide synthase from the
plant kingdom: NO generation from the green alga Ostreococ-
cus tauri is light irradiance and growth phase dependent. Plant
Cell 22:3816–3830
Foyer CH, Noctor G (2015) Defning robust redox signalling within the
context of the plant cell. Plant Cell Environ 38:239
Freschi L (2013) Nitric oxide and phytohormone interactions: Current
status and perspectives. Front Plant Sci 4:1–22
Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase
(NOS): is one really needed? Plant Sci 181:401–404
García MJ, Lucena C, Romera FJ, Alcántara E, Pérez-Vicente R (2010)
Ethylene and nitric oxide involvement in the up-regulation of key
genes related to iron acquisition and homeostasis in Arabidopsis.
J Exp Bot 61:3885–3899
Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR
(2003) Nitric oxide regulates K+ and Cl-channels in guard cells
through a subset of abscisic acid-evoked signaling pathways.
Proc Natl Acad Sci USA 100:11116–11121
Garcıa-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross
talk in guard cells. Plant Physiol 128:790–792
Gaupels F, Furch AC, Zimmermann MR, Chen F, Kaever V, Buhtz
A, Kehr J, Sarioglu H, Kogel KH, Durner J (2016) Systemic
induction of NO-, redox-, and cGMP signaling in the pumpkin
extra fascicular phloem upon local leaf wounding. Front Plant
Sci 7:154. https:// doi. org/ 10. 3389/ fpls. 2016. 00154
Ghori NH, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M
(2019) Heavy metal stress and responses in plants. Int J Environ
SciTech 16:1807–1828
Gisone P, Dubner D, PÉREZ MD, Michelin S, Puntarulo S (2004)
The role of nitric oxide in the radiation-induced effects in the
developing brain. InVivo 18:281–292
Gniazdowska A, Krasuska U, Bogatek R (2010a) Dormancy removal in
apple embryos by nitric oxide or cyanide involves modifications
in ethylene biosynthetic pathway. Planta 232:1397–1407
Gniazdowska A, Krasuska U, Dębska K, Andryka P, Bogatek R
(2010b) The beneficial effect of small toxic molecules on dor-
mancy alleviation and germination of apple embryos is due to
NO formation. Planta 232:999–1005
González A, de Los Ángeles Cabrera M, Henríquez MJ, Contreras RA,
Morales B, Moenne A (2012) Cross talk among calcium, hydro-
gen peroxide, and nitric oxide and activation of gene expression
involving calmodulins and calcium-dependent protein kinases
in Ulva compressa exposed to copper excess. Plant Physiol
158:1451–1462
Goretski J, Hollocher TC (1988) Trapping of nitric oxide produced
during denitrification by extracellular hemoglobin. J Biol Chem
263:2316–2323
Gouvea CMCP, Souza JF, Magalhaes CAN, Martins IS (1997) NO·–
releasing substances that induce growth elongation in maize root
segments. Plant Growth Regul 21:183–187
Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric
oxide, polyamines and Cd-induced phytotoxicity in wheat roots.
Phytochem 69:2609–2615
Gross I, Durner J (2016) In search of enzymes with a role in 3’,
5’-cyclic guanosine monophosphate metabolism in plants. Front
Plant Sci 7:576. https:// doi. org/ 10. 3389/ fpls. 2016. 00576
Guillas I, Zachowski A, Baudouin E (2011) A matter of fat: interaction
between nitric oxide and sphingolipid signaling in plant cold
response. Plant Signal Behav 6:140–142
Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is
targeted to mitochondria and protects against oxidative damage
and dark-induced senescence. Plant Cell 17:3436–3450
Guo Z, Tan J, Zhuo C, Wang C, Xiang B, Wang Z (2014) Abscisic
acid, H2O2 and nitric oxide interactions mediated cold-induced
S-adenosylmethionine synthetase in Medicago sativa subsp. fal-
cata that confers cold tolerance through up-regulating polyamine
oxidation. Plant Biotech J 12:601–612
Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as
a nitrite: NO reductase. Mitochondrion 11:537–543
Gupta KJ, Igamberdiev AU (2016) Reactive nitrogen species in
mitochondria and their implications in plant energy status and
hypoxic stress tolerance. Front Plant Sci 7:369. https:// doi. org/
10. 3389/ fpls. 2016. 00369
Gupta KJ, Igamberdiev AU, Manjunatha G etal (2011) The emerg-
ing roles of nitric oxide (NO) in plant mitochondria. Plant Sci
181:520–526
Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen
peroxide and polyamines act as double edged swords in plant
abiotic stress responses. Front Plant Sci. https:// doi. org/ 10. 3389/
fpls. 2016. 01343
Gupta P, Srivastava S, Seth CS (2017) 24-Epibrassinolide and sodium
nitroprusside alleviate the salinity stress in Brassica juncea L. cv.
Varuna through cross talk among proline, nitrogen metabolism
and abscisic acid. Plant Soil 411:483–498
Hajihashemi S, Skalicky M, Brestic M, Pavla V (2020) Cross-talk
between nitric oxide, hydrogen peroxide and calcium in salt-
stressed Chenopodium quinoa Willd. At seed germination stage.
Plant Physiol Biochem 154:657–664
Hancock JT, Neill SJ, Wilson ID (2011) Nitric oxide and ABA in the
control of plant function. Plant Sci 181:555–559
Hasanuzzaman M, Oku H, Nahar K, Bhuyan MB, Al Mahmud J, Bal-
uska F, Fujita M (2018) Nitric oxide-induced salt stress tolerance
in plants: ROS metabolism, signaling, and molecular interac-
tions. Plant Biotech Rep 12:77–92

Journal of Plant Growth Regulation
1 3
He HY, He LF, Gu MH, Li XF (2012) Nitric oxide improves aluminum
tolerance by regulating hormonal equilibrium in the root apices
of rye and wheat. Plant Sci 183:123–130
Hebelstrup KH, Van Zanten M, Mandon J, Voesenek LA, Harren FJ,
Cristescu SM, Møller IM, Mur LA (2012) Haemoglobin modu-
lates NO emission and hyponasty under hypoxia-related stress
in Arabidopsis thaliana. J Exp Bot 63:5581–5591
Henry Y, Ducrocq C, Drapier JC, Servent D, Pellat C, Guissani A
(1991) Nitric oxide, a biological effector. Electron paramagnetic
resonance detection of nitrosyl-iron-protein complexes in whole
cells. Eur Biophys J 20:1–15
Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of
drought-related gene expression in Arabidopsis thaliana to hor-
monal and environmental factors. J Exp Bot 59:2991–3007
Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant
adaptation to hypoxia: an alternative to classic fermentation path-
ways. J Exp Bot 55:2473–2482
Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric
oxide cycling in plants: participating reactions and possible
mechanisms. Physiol Plant 138:393–404
Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloro-
plasts as a nitric oxide cellular source. Effect of reactive nitro-
gen species on chloroplastic lipids and proteins. Plant Physiol
142:1246–1255
Jiménez-Quesada MJ, Traverso JÁ, Alché J (2016) NADPH oxidase-
dependent superoxide production in plant reproductive tissues.
Front Plant Sci 7:359. https:// doi. org/ 10. 3389/ fpls. 2016. 00359
Karpets YV, Kolupaev YE, Yastreb TO, Oboznyi AI (2016) Induction
of heat resistance in wheat seedlings by exogenous calcium,
hydrogen peroxide, and nitric oxide donor: functional interac-
tion of signal mediators. Russ J Plant Physiol 63:490–498
Kaya C, Ashraf M, Wijaya L, Ahmad P (2019) The putative role of
endogenous nitric oxide in brassinosteroid-induced antioxidant
defence system in pepper (Capsicum annuum L.) plants under
water stress. Plant Physiol Biochem 143:119–128
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020a) Responses
of nitric oxide and hydrogen sulfide in regulating oxidative
defence system in wheat plants grown under cadmium stress.
Physiol Plant 168:345–360
Kaya C, Higgs D, Ashraf M, Alyemeni MN, Ahmad P (2020b) Inte-
grative roles of nitric oxide and hydrogen sulfide in melatonin-
induced tolerance of pepper (Capsicum annuum L.) plants to
iron deficiency and salt stress alone or in combination. Physiol
Plant 168:256–277
Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-
Sattari T (2010) Effects of exogenous salicylic acid and nitric
oxide on lipid peroxidation and antioxidant enzyme activities
in leaves of Brassica napus L. under nickel stress. Sci Hort
126:402–407
Khan MI, Nazir F, Asgher M, Per TS, Khan NA (2015a) Selenium
and sulfur influence ethylene formation and alleviate cadmium-
induced oxidative stress by improving proline and glutathione
production in wheat. J Plant Physiol 173:9–18
Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015b) Sali-
cylic acid-induced abiotic stress tolerance and underlying
mechanisms in plants. Front Plant Sci 6:642
Khan MN, Mobin M, Abbas ZK, Siddiqui MH (2017) Nitric oxide-
induced synthesis of hydrogen sulfide alleviates osmotic stress
in wheat seedlings through sustaining antioxidant enzymes,
osmolyte accumulation and cysteine homeostasis. Nitric Oxide
68:91–102
Khan MN, Siddiqui MH, AlSolami MA, Alamri S, Hu Y, Ali HM,
Al-Amri AA, Alsubaie QD, Al-Munqedhi BM, Al-Ghamdi A
(2020) Crosstalk of hydrogen sulfide and nitric oxide requires
calcium to mitigate impaired photosynthesis under cadmium
stress by activating defense mechanisms in Vigna radiata.
Plant Physiol Biochem 156:278–290
Khokon MD, Okuma EI, Hossain MA, Munemasa S, Uraji M, Naka-
mura Y, Mori IC, Murata Y (2011) Involvement of extracel-
lular oxidative burst in salicylic acid-induced stomatal closure
in Arabidopsis. Plant Cell Environ 34:434–443
Kolbert ZS, Barroso JB, Brouquisse R, Corpas FJ, Gupta KJ, Lin-
dermayr C, Loake GJ, Palma JM, Petřivalský M, Wendehenne
D, Hancock JT (2019) A forty year journey: the generation and
roles of NO in plants. Nitric Oxide 93:53–70
Kong X, Wang T, Li W, Tang W, Zhang D, Dong H (2016) Exog-
enous nitric oxide delays salt induced leaf senescence in cotton
(Gossypium hirsutum L.). Acta Physiol Plant 38:1–9
Krasuska U, Ciacka K, Gniazdowska A (2017) Nitric oxide-poly-
amines cross-talk during dormancy release and germination
of apple embryos. Nitric Oxide 68:38–50
Kushwaha BK, Singh S, Tripathi DK, Sharma S, Prasad SM, Chau-
han DK, Kumar V, Singh VP (2019) New adventitious root for-
mation and primary root biomass accumulation are regulated
by nitric oxide and reactive oxygen species in rice seedlings
under arsenate stress. J Hazard Mat 361:134–140
Lamattina L, Beligni MV, Garcia-Mata C, Laxalt AM (2001)Method
of enhancing the metabolic function and the growing condi-
tions of plants and seeds. US Patent 6, 242
León J, Costa-Broseta Á (2020) Present knowledge and controversies,
deficiencies, and misconceptions on nitric oxide synthesis, sens-
ing, and signaling in plants. Plant Cell Environ 43:1–15
Leshem YY, Wills RBH (1998) Harnessing senescence delaying gases
nitric oxide and nitrous oxide: a novel approach to postharvest
control of fresh horticultural produce. Biol Plant 41:1–10
Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso
JB, Corpas FJ (2011) Function of S-nitrosoglutathione reductase
(GSNOR) in plant development and under biotic/abiotic stress.
Plant Signal Behav 6:789–793
Li X, Gong B, Xu K (2014) Interaction of nitric oxide and polyam-
ines involves antioxidants and physiological strategies against
chilling-induced oxidative damage in Zingiber officinale Roscoe.
Sci Hort 170:237–248
Li ZG, Luo LJ, Sun YF (2015) Signal crosstalk between nitric oxide
and hydrogen sulfide may be involved in hydrogen peroxide-
induced thermotolerance in maize seedlings. Russ J Plant Physiol
62:507–514
Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and
hydrogen peroxide alleviate drought stress in marigold explants
and promote its adventitious root development. Plant Physiol
Biochem 58:6–15
Liu YG, Shi L, Ye NH, Liu R, Jia WS, Zhang JH (2009) Nitric
oxide-induced rapid decrease of abscisic acid concentration is
required in breaking seed dormancy in Arabidopsis. New Phytol
183:1030–1042
Liu Y, Ye N, Liu R, Chen M, Zhang J (2010) H2O2 mediates the regu-
lation of ABA catabolism and GA biosynthesis in Arabidopsis
seed dormancy and germination. J Exp Bot 61:2979–2990
Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M, Gao Q, Tian
LL, Xu ZH, Bao F, Hu Y (2013) Cytokinins can act as sup-
pressors of nitric oxide in Arabidopsis. Proc Nat Acad Sci USA
110:1548–1553
Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces
root meristem size by nitric oxide-mediated modulation of
auxin accumulation and signaling in Arabidopsis. Plant Physiol
168:343–356
Liu Y, Yang X, Zhu S, Wang Y (2016) Postharvest application of MeJA
and NO reduced chilling injury in cucumber (Cucumis sativus)
through inhibition of H2O2 accumulation. Postharvest Biol Tech
119:77–83

Journal of Plant Growth Regulation
1 3
Liu M, Zhang H, Fang X, Zhang Y, Jin C (2018) Auxin acts down-
stream of ethylene and nitric oxide to regulate magnesium defi-
ciency-induced root hair development in Arabidopsis thaliana.
Plant Cell Physiol 59:1452–1465
Liu X, Yin L, Deng X, Gong D, Du S, Wang S, Zhang Z (2020) Com-
bined application of silicon and nitric oxide jointly alleviated
cadmium accumulation and toxicity in maize. J Hazard Mat
395:122679
Lombardi L, Ceccarelli N, Picciarelli P, Sorce C, Lorenzi R (2010)
Nitric oxide and hydrogen peroxide involvement during pro-
grammed cell death of Sechium edule nucellus. Physiol Plant
140:89–102
Lozano-Juste J, Leon J (2010) Enhanced abscisic acid-mediated
responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-
and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis.
Plant Physiol 152:891–903
Lozano-Juste J, León J (2010) Nitric oxide modulates sensitivity to
ABA. Plant Signal Behav 5:314–316
Lozano-Juste J, León J (2011) Nitric oxide regulates DELLA content
and PIF expression to promote photomorphogenesis in Arabi-
dopsis. Plant Physiol 156:1410–1423
Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as
a positive regulator of ABA response and drought tolerance in
rice. Planta 229:605–615
Lv X, Ge S, Jalal Ahammed G, Xiang X, Guo Z, Yu J, Zhou Y (2017)
Crosstalk between nitric oxide and MPK1/2 mediates cold accli-
mation-induced chilling tolerance in tomato. Plant Cell Physiol
58:1963–1975
Lytvyn DI, Raynaud C, Yemets AI, Bergounioux C, Blume YB (2016)
Involvement of inositol biosynthesis and nitric oxide in the medi-
ation of UV-B induced oxidative stress. Front Plant Sci 7:430.
https:// doi. org/ 10. 3389/ fpls. 2016. 00430
Ma Z, Marsolais F, Bykova NV, Igamberdiev AU (2016) Nitric oxide
and reactive oxygen species mediate metabolic changes in barley
seed embryo during germination. Front Plant Sci 7:138. https://
doi. org/ 10. 3389/ fpls. 2016. 00138
Majláth I, Szalai G, Soós V, Sebestyén E, Balázs E, Vanková R, Dobrev
PI, Tari I, Tandori J, Janda T (2012) Effect of light on the gene
expression and hormonal status of winter and spring wheat plants
during cold hardening. Physiol Plant 145:296–314
Mazid M, Khan TA, Mohammad F (2011) Role of nitric oxide in regu-
lation of H2O2 mediating tolerance of plants to abiotic stress: a
synergistic signaling approach. J Stress Physiol Biochem 7(2):34
Mioto PT, Mercier H (2013) Abscisic acid and nitric oxide signal-
ing in two different portions of detached leaves of Guzmania
monostachia with CAM up-regulated by drought. J Plant Physiol
170:996–1002
Mohn MA, Thaqi B, Fischer-Schrader K (2019) Isoform-specific NO
synthesis by Arabidopsis thaliana nitrate reductase. Plants 8:67
Molassiotis A, Job D, Ziogas V, Tanou G (2016) Citrus plants: A model
system for unlocking the secrets of NO and ROS-inspired prim-
ing against salinity and drought. Front Plant Sci 7:229. https://
doi. org/ 10. 3389/ fpls. 2016. 00229
Montilla-Bascón G, Rubiales D, Hebelstrup KH, Mandon J, Harren
FJ, Cristescu SM, Mur LA, Prats E (2017) Reduced nitric oxide
levels during drought stress promote drought tolerance in barley
and is associated with elevated polyamine biosynthesis. Sci Rep
7:1–15
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/
AtNOA1 is a functional Arabidopsis thaliana cGTPase and not
a nitric-oxide synthase. J Biol Chem 283:32957–32967
Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoi-
shi Y, Murata Y (2007) The coronatine-insensitive 1 mutation
reveals the hormonal signaling interaction between abscisic
acid and methyl jasmonate in Arabidopsis guard cells. Specific
impairment of ion channel activation and second messenger pro-
duction. Plant Physiol 143:1398–1407
Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova
GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric
oxide in plants: an assessment of the current state of knowledge.
AoB Plants 5:pls052. https:// doi. org/ 10. 1093/ aobpla/ pls052
Nabi RB, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun BG,
Yun BW (2019) Nitric oxide regulates plant responses to drought,
salinity, and heavy metal stress. Environ Exp Bot 161:120–133
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M
(2016) Polyamine and nitric oxide crosstalk: antagonistic effects
on cadmium toxicity in mung bean plants through upregulating
the metal detoxification, antioxidant defense and methylglyoxal
detoxification systems. Ecotoxicol Environ Saf 126:245–255
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen
peroxide and nitric oxide as signalling molecules in plants. J Exp
Bot 53:1237–1247
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in
plants. New Phytol 159:11–35
Oliveira H, Salgado I, Sodek L (2013) Nitrite decreases ethanol pro-
duction by intact soybean roots submitted to oxygen deficiency: a
role for mitochondrial nitric oxide synthesis? Plant Signal Behav
8:e23578
Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root
development. Cold Spring Harb Perspect Biol 2:a001537
Ozfidan-Konakci C, Yildiztugay E, Elbasan F, Kucukoduk M, Tur-
kan I (2020) Hydrogen sulfide (H2S) and nitric oxide (NO)
alleviate cobalt toxicity in wheat (Triticum aestivum L.) by
modulating photosynthesis, chloroplastic redox and antioxidant
capacity. J Hazard Mat 388:122061
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002)
Nitric oxide is required for root organogenesis. Plant Physiol
129:954–956
Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lin-
dermayr C (2008) Nitric oxide responsive genes and promoters
in Arabidopsis thaliana: A bioinformatics approach. J Exp Bot
59:177–186
Parankusam S, Adimulam SS, Bhatnagar-Mathur P, Sharma KK
(2017) Nitric oxide (NO) in plant heat stress tolerance: cur-
rent knowledge and perspectives. Front Plant Sci. https:// doi.
org/ 10. 3389/ fpls. 2017. 01582
Peck S, Mittler R (2020) Plant signaling in biotic and abiotic stress.
J Exp Bot 71:1649–1651. https:// doi. org/ 10. 1093/ jxb/ eraa0 51
Poór P, Czékus Z, Ördög A (2019) Role of nitric oxide in physiologi-
cal and stress responses of plants under darkness. In: Hasa-
nuzzaman M, Fotopoulos V, Nahar K, Fujita M (eds) Reac-
tive oxygen, nitrogen and sulfur species in plants: production,
metabolism, signaling and defense mechanisms. Wiley, New
York, pp 515–531
Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regula-
tion of nitric oxide (NO) production by plant nitrate reductase
invivo and invitro. J Exp Bot 53:103–110
Rodríguez-serrano MA, Romero-puertas MC, Zabalza AN, Corpas
FJ, Gómez M, Del Rio LA, Sandalio LM (2006) Cadmium
effect on oxidative metabolism of pea (Pisum sativum L.) roots.
Imaging of reactive oxygen species and nitric oxide accumula-
tion invivo. Plant Cell Environ 29:1532–1544
Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testil-
lano PS, Risueño MC, Luis A, Sandalio LM (2009) Cellular
response of pea plants to cadmium toxicity: cross talk between
reactive oxygen species, nitric oxide, and calcium. Plant Phys-
iol 150:229–243
Romera FJ, García MJ, Alcántara E, Pérez-Vicente R (2011) Lat-
est findings about the interplay of auxin, ethylene and nitric
oxide in the regulation of Fe deficiency responses by strategy
I plants. Plant Signal Behav 6:167–170

Journal of Plant Growth Regulation
1 3
Romero-Puertas MC, Sandalio LM (2016) Nitric oxide level is self-
regulating and also regulates its ROS partners. Front Plant Sci
7:316. https:// doi. org/ 10. 3389/ fpls. 2016. 00316
Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Poly-
amines modulate nitrate reductase activity in wheat leaves:
involvement of nitric oxide. Amino Acids 42:857–865
Roszer T (2012a) Nitric oxide synthesis in leaf peroxisomes and
in plant-type mitochondria. In: Roszer T (ed) The biology of
subcellular nitric oxide. Springer, New York, pp 67–80
Roszer T (2012b) Nitric oxide synthesis in the chloroplast. In: Roszer
T (ed) The biology of subcellular nitric oxide. Springer, New
York, pp 49–66
Roszer T, Kiss-Tóth E, Rózsa D etal (2010) Hypothermia translo-
cates nitric oxide synthase from cytosol to membrane in snail
neurons. Cell Tissue Res 342:191–203
Ruan HH, Shen WB, Xu LL (2004) Nitric oxide involved in the
abscisic acid induced proline accumulation in wheat seedling
leaves under salt stress. Acta Bot Sin 46:1307–1315
Rubbo H, Parthasarathy S, Barnes S, Kirk M, Kalyanaraman B, Free-
man BA (1995) Nitric oxide inhibition of lipoxygenasedepend-
ent liposome and low density lipoprotein oxidation: termina-
tion of radical chain propagation reactions and formation of
nitrogen containing oxidized lipid derivatives. Arch Biochem
Biophys 324:15–25
Rumer S, Kapuganti JG, Kaiser WM (2009) Oxidation of hydroxy-
lamines to NO by plant cells. Plant Signal Behav 4:853–855
Saito N, Yoshimasa N, Mori IC, Murata Y (2009) Nitric oxide
functions in both methyl jasmonate signaling and abscisic
acid signaling in Arabidopsis guard cells. Plant Signal Behav
4:119–120
Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric
oxide-mediated integrative alterations in plant metabolism to
confer abiotic stress tolerance, NO crosstalk with phytohormones
and NO-mediated post translational modifications in modulating
diverse plant stress. Nitric Oxide 73:22–38
Sánchez-Vicente I, María G, Fernández-Espinosa OL (2019) Nitric
oxide molecular targets: reprogramming plant development upon
stress. J Exp Bot 70:4441–4460
Santisree P, Sanivarapu H, Gundavarapu S, Sharma KK, Bhatnagar-
Mathur P (2020) Nitric oxide as a signal in inducing secondary
metabolites during plant stress. In: Mérillon JM, Ramawat KG
(eds) Co-evolution of secondary metabolites. Springer, Cham,
pp 593–621
Santner A, Estelle M (2009) Recent advances and emerging trends in
plant hormone signalling. Nat 459:1071–1078
Santos MP, Zandonadi DB, de Sá AFL, Costa EP, de Oliveira CJL,
Perez LE, Façanha AR, Bressan-Smith R (2020) Abscisic acid-
nitric oxide and auxin interaction modulates salt stress response
in tomato roots. Theor Exp Plant Physiol 32(4):301–313
Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H
(2007) Inhibition of AtMYB2 DNA-binding by nitric oxide
involves cysteine S-nitrosylation. Biochem Biophy Res Com-
mun 361:1048–1053
Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regula-
tion of the ascorbate-glutathione cycle by exogenous jasmonic
acid in the leaves of wheat seedlings under drought stress. Pro-
toplasma 252:1397–1405
Shao R, Wang K, Shangguan Z (2010) Cytokinin-induced photosyn-
thetic adaptability of Zea mays L. to drought stress associated
with nitric oxide signal: probed by ESR spectroscopy and fast
OJIP fluorescence rise. J Plant Physiol 167:472–479
Shi H, Liu W, Wei Y, Ye T (2017) Integration of auxin/indole-
3-acetic acid 17 and RGA-LIKE3 confers salt stress resistance
through stabilization by nitric oxide in Arabidopsis. J Exp Bot
68:1239–1249
Si T, Wang X, Wu L, Zhao C, Zhang L, Huang M, Cai J, Zhou Q, Dai
T, Zhu JK, Jiang D (2017) Nitric oxide and hydrogen peroxide
mediate wounding-induced freezing tolerance through modifi-
cations in photosystem and antioxidant system in wheat. Front
Plant Sci 8:1284
Siddiqui M, Alamri SA, Mutahhar YY, Al-Khaishany MA, Al-Qutami
HM, Nasir Khan MA (2017) Nitric Oxide and calcium induced
physiobiochemical changes in tomato (Solanum Lycopersicum)
plant under heat stress. Fresen Environ Bull 26:1663–1672
Simaei M, Khavari-Nejad RA, Bernard F (2012) Exogenous applica-
tion of salicylic acid and nitric oxide on the ionic contents and
enzymatic activities in NaCl-stressed soybean plants. Am J Plant
Sci 3(10):1495–1503
Simon R, Dresselhaus T (2015) Peptides take centre stage in plant
signalling. J Exp Bot 66:5135–5138
Singh N, Bhatla SC (2018) Nitric oxide regulates lateral root formation
through modulation of ACC oxidase activity in sunflower seed-
lings under salt stress. Plant Signal Behav 13:e1473683
Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide
(as sodium nitroprusside) supplementation ameliorates Cd tox-
icity in hydroponically grown wheat roots. Environ Exp Bot
63:158–167
Singh S, Husain T, Kushwaha BK, Suhel M, Fatima A, Mishra V, Singh
SK, Tripathi DK, Rai M, Prasad SM, Dubey NK (2020) Regula-
tion of ascorbate-glutathione cycle by exogenous nitric oxide and
hydrogen peroxide in soybean roots under arsenate stress. J Haz
Mat. https:// doi. org/ 10. 1016/j. jhazm at. 2020. 123686
Sivakumaran A, Akinyemi A, Mandon J, Cristescu SM, Hall MA,
Harren FJ, Mur LA (2016) ABA suppresses Botrytis cinerea
elicited NO production in tomato to influence H2O2 generation
and increase host susceptibility. Front Plant Sci 7:709. https://
doi. org/ 10. 3389/ fpls. 2016. 00709
Slinger D, Tenison K (2005) Salinity glove box guide: NSW Murray
& Murrumbidgee catchments. An initiative of the Southern salt
action team. NSW Department of Primary Industries, Newington
Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects
against oxidative stress under heat stress in the calluses from two
ecotypes of reed. Plant Sci 171:449–458
Song L, Ding W, Shen J, Zhang Z, Bi Y, Zhang L (2008) Nitric oxide
mediates abscisic acid induced thermotolerance in the cal-
luses from two ecotypes of reed under heat stress. Plant Sci
175:826–832
Song XG, She XP, Wang J, Sun YC (2011) Ethylene inhibits darkness-
induced stomatal closure by scavenging nitric oxide in guard
cells of Vicia faba. Funct Plant Biol 38:767–777
Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide
and its redox-activated forms. Science 258:1898–1902
Sturms R, Dispirito AA, Hargrove MS (2011) Plant and cyanobacterial
hemoglobins reduce nitrite to nitric oxide under anoxic condi-
tions. Biochem 50:3873–3878
Sun H, Bi Y, Tao J, Huang S, Hou M, Xue R, Liang Z, Gu P, Yoneyama
K, Xie X, Shen Q (2016) Strigolactones are required for nitric
oxide to induce root elongation in response to nitrogen and phos-
phate deficiencies in rice. Plant Cell Env 39:1473–1484
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molas-
siotis A, Job D (2009) Proteomics reveals the overlapping roles
of hydrogen peroxide and nitric oxide in the acclimation of citrus
plants to salinity. Plant J 60:795–804
Tavares CP, Vernal J, Delena RA, Lamattina L, Cassia R, Terenzi H
(2014) S-nitrosylation influences the structure and DNA bind-
ing activity of AtMYB30 transcription factor from Arabidopsis
thaliana. Biochim Biophys Acta 1844:810–817
Taylor JE, McAinsh MR (2004) Signalling crosstalk in plants: emerg-
ing issues. J Exp Bot 55:147–149
Terrile MC, París R, Calderón-Villalobos LI, Iglesias MJ, Lamattina
L, Estelle M, Casalongué C (2012) Nitric oxide influences auxin

Journal of Plant Growth Regulation
1 3
signaling through S-nitrosylation of the Arabidopsis TRANS-
PORT INHIBITOR RESPONSE 1 auxin receptor. Plant J
70:492–500
Thalineau E, Truong HN, Berger A, Fournier C, Boscari A, Wende-
henne D, Jeandroz S (2016) Cross-regulation between N metab-
olism and nitric oxide (NO) signaling during plant immunity.
Front Plant Sci 7:472. https:// doi. org/ 10. 3389/ fpls. 2016. 00472
Tian X, He M, Wang Z, Zhang J, Song Y, He Z, Dong Y (2015) Appli-
cation of nitric oxide and calcium nitrate enhances tolerance of
wheat seedlings to salt stress. Plant Growth Regul 77:343–356
Tiso M, Tejero J, Basu S, Azarov I, Wang X, Simplaceanu V, Frizzell
S, Jayaraman T, Geary L, Shapiro C, Ho C (2011) Human neu-
roglobin functions as a redox-regulated nitrite reductase. J Biol
Chem 286:18277–18289
Tossi V, Cassia R, Bruzzone S, Zocchi E, Lamattina L (2012) ABA
says NO to UV-B: a universalresponse? Trends Plant Sci
17:510–517
Tossi V, Lamattina L, Cassia R (2013) Pharmacological and genetical
evidence supporting nitric oxide requirement for 2, 4-epibrassi-
nolide regulation of root architecture in Arabidopsis thaliana.
Plant Signal Behav 8:e24712
Tossi VE, Lamattina L, Jenkins G, Cassia R (2014) UV-B-induced
stomatal closure in Arabidopsis is regulated by the UVR8
photoreceptor in an NO-dependent mechanism. Plant Physiol
164:2220–2230
Tun NN, Holk A, Scherer GF (2001) Rapid increase of NO release in
plant cell cultures induced by cytokinin. FEBS Lett 509:174–176
Turkan I (2017) Emerging roles for ROS and RNS—versatile mol-
ecules in plants. J Exp Bot 68:4413–4416. https:// doi. org/ 10.
1093/ jxb/ erx236
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects
of hydrogen peroxide and nitric oxide on both salt and heat stress
tolerance in rice. Plant Sci 163:515–523
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in
plants: an overview. Environ Exp Bot 61:199–223
Wang L, Yang L, Yang F, Li X, Song Y, Wang X, Hu X (2010) Involve-
ments of H2O2 and metallothionein in NO-mediated tomato tol-
erance to copper toxicity. J Plant Physiol 167:1298–1306
Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide
enhances alfalfa (Medicago sativa) tolerance against salinity
during seed germination by nitric oxide pathway. Plant Soil
351:107–119
Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reac-
tive oxygen species in plant programed cell death. Front Plant
Sci. https:// doi. org/ 10. 3389/ fpls. 2013. 00314
Wang L, Guo Y, Jia L, Chu H, Zhou S, Chen K, Wu D, Zhao L (2014)
Hydrogen peroxide acts upstream of nitric oxide in the heat shock
pathway in Arabidopsis seedlings. Plant Physiol 164:2184–2196
Wang D, Liu Y, Tan X, Liu H, Zeng G, Hu X, Jian H, Gu Y (2015a)
Effect of exogenous nitric oxide on antioxidative system and
S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under
cadmium stress. Environ Sci Pol Res 22:3489–3497
Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA,
Song CP, Zhu JK (2015b) Nitric oxide negatively regulates absci-
sic acid signaling in guard cells by S-nitrosylation of OST1. Proc
Natl Acad Sci USA 112:613–618
Wang H, Ji F, Zhang Y, Hou J, Liu W, Huang J, Liang W (2019) Inter-
actions between hydrogen sulphide and nitric oxide regulate two
soybean citrate transporters during the alleviation of aluminium
toxicity. Plant Cell Environ 42:2340–2356
Wei L, Zhang M, Wei S, Zhang J, Wang C, Liao W (2020) Roles of
nitric oxide in heavy metal stress in plants: cross-talk with phy-
tohormones and protein S-nitrosylation. Environ Pol. https:// doi.
org/ 10. 1016/j. envpol. 2020. 113943
Wimalasekera R, Tebartz F, Scherer GF (2011) Polyamines, polyam-
ine oxidases and nitric oxide in development, abiotic and biotic
stresses. Plant Sci 181:593–603
Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide:
insights into regulatory, cytotoxic, and cytoprotective mecha-
nisms of nitric oxide. Free Radic Biol Med 25:434–456
Wink DA, Osawa Y, Darbyshire JF, Jones CR, Eshenaur SC, Nims RW
(1993) Inhibition of cytochrome P450 by nitric oxide and a nitric
oxide-releasing agent. Arch Biochem Biophys 300:115–123
Wu H, Zheng Y, Liu J, Zhang H, Chen H (2016a) Heme oxygenase-1
delays gibberellin-induced programmed cell death of rice aleu-
rone layers subjected to drought stress by interacting with nitric
oxide. Front Plant Sci 6:1267. https:// doi. org/ 10. 3389/ fpls. 2015.
01267
Wu Q, Su N, Zhang X, Liu Y, Cui J, Liang Y (2016b) Hydrogen per-
oxide, nitric oxide and UV RESISTANCE LOCUS8 interact
to mediate UV-B-induced anthocyanin biosynthesis in radish
sprouts. Sci Rep 6:1–12
Wu P, Xiao C, Cui J, Hao B, Zhang W, Yang Z, Ahammed GJ, Liu H,
Cui H (2020) Nitric oxide and its interaction with hydrogen per-
oxide enhance plant tolerance to low temperatures by improving
the efficiency of the calvin cycle and the ascorbate-glutathione
cycle in cucumber seedlings. J Plant Growth Regul. https:// doi.
org/ 10. 1007/ s00344- 020- 10242-w
Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances
cadmium tolerance of rice by increasing pectin and hemicellulose
contents in root cell wall. Planta 230:755–765
Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric
oxide improves antioxidative capacity and reduces auxin degra-
dation in roots of Medicago truncatula seedlings under cadmium
stress. Plant Soil 326:321–330
Xu LL, Fan ZY, Dong YJ, Kong J, Bai XY (2015) Effects of exog-
enous salicylic acid and nitric oxide on physiological character-
istics of two peanut cultivars under cadmium stress. Biol Planta
59:171–182
Xu YF, Chu XT, Fu JJ, Yang LY, Hu TM (2016) Crosstalk of nitric
oxide with calcium induced tolerance of tall fescue leaves to high
irradiance. Biol Plant 60:376–384
Yamasaki H (2000) Nitrite-dependent nitric oxide production path-
way: implications for involvement of active nitrogen species in
photoinhibition invivo. Philos Trans R Soc Lond B Biol Sci
355:1477–1488
Yang L, Ji J, Wang H, Harris-Shultz KR, Abd Allah EF, Luo Y, Guan
Y, Hu X (2016) Carbon monoxide interacts with auxin and nitric
oxide to cope with iron deficiency in Arabidopsis. Front Plant
Sci. https:// doi. org/ 10. 3389/ fpls. 2016. 00112
Yang J, Deng X, Wang X, Wang J, Du S, Li Y (2019) The calcium
sensor OsCBL1 modulates nitrate signaling to regulate seedling
growth in rice. PLoS ONE 14:e0224962
Yuan HM, Huang X (2016) Inhibition of root meristem growth by
cadmium involves nitric oxide-mediated repression of auxin
accumulation and signalling in Arabidopsis. Plant Cell Environ
39:120–135
Zaharah SS, Singh Z (2011) Postharvest nitric oxide fumigation allevi-
ates chilling injury, delays fruit ripening and maintains quality
in cold-stored ‘Kensington Pride’mango. PostharvestBiol Tech
60:202–210
Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A, Inupakutika
MA, Mittler R (2016) ABA is required for the accumulation of
APX1 and MBF1c during a combination of water deficit and heat
stress. J Exp Bot 67:5381–5390
Zhang J, Jia W, Yang J, Ismail AM (2006a) Role of ABA in integrat-
ing plant responses to drought and salt stresses. Field Crops Res
97:111–119
Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006b) Nitric
oxide enhances salt tolerance in maize seedlings through

Journal of Plant Growth Regulation
1 3
increasing activities of proton-pump and Na+/H+ antiport in
the tonoplast. Planta 224:545–555
Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007a)
Nitric oxide induced by hydrogen peroxide mediates abscisic
acid-induced activation of the mitogen-activated protein kinase
cascade involved in antioxidant defense in maize leaves. New
Phytol 175:36–50
Zhang F, Wang Y, Yang Y, Wu HAO, Wang DI, Liu J (2007b) Involve-
ment of hydrogen peroxide and nitric oxide in salt resistance
in the calluses from Populus euphratica. Plant Cell Environ
30:775–785
Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering
ethylene biosynthesis and ripening of tomato fruit. J Exp Bot
60:1579–1588
Zhang X, Shen L, Li F, Meng D, Sheng J (2011) Methyl salicylate-
induced arginine catabolism is associated with up-regulation of
polyamine and nitric oxide levels and improves chilling tolerance
in cherry tomato fruit. J Agric Food Chem 59:9351–9357
Zhang X, Liu Y, Liu Q, Zong B, Yuan X, Sun H, Wang J, Zang L,
Ma Z, Liu H, He S (2018) Nitric oxide is involved in absci-
sic acid-induced photosynthesis and antioxidant system of tall
fescue seedlings response to low-light stress. Environ Exp Bot
155:226–238
Zhao Z, Chen G, Zhang C (2001) Interaction between reactive oxy-
gen species and nitric oxide in drought-induced abscisic acid
synthesis in root tips of wheat seedlings. Funct Plant Biol
28:1055–1061
Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012)
Gibberellic acid alleviates cadmium toxicity by reducing nitric
oxide accumulation and expression of IRT1 in Arabidopsis thali-
ana. J Hazard Mat 239:302–307
Zhu XF, Zhu CQ, Wang C, Dong XY, Shen RF (2017) Nitric oxide
acts upstream of ethylene in cell wall phosphorus reutilization in
phosphorus-deficient rice. J Exp Bot 68:753–760
Zhu Y, Gao H, Lu M, Hao C, Pu Z, Guo M, Hou D, Chen LY, Huang
X (2019) Melatonin-nitric oxide crosstalk and their roles in the
redox network in plants. Int J Mol Sci. https:// doi. org/ 10. 3390/
ijms2 02462 00
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