Plant Signaling & Behavior

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Reactive oxygen species signaling in plants under

abiotic stress

Shuvasish Choudhury, Piyalee Panda , Lingaraj Sahoo & Sanjib Kumar Panda

To cite this article: Shuvasish Choudhury, Piyalee Panda , Lingaraj Sahoo & Sanjib Kumar
Panda (2013) Reactive oxygen species signaling in plants under abiotic stress, Plant Signaling &
Behavior, 8:4, e23681, DOI: 10.4161/psb.23681

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 MINI-REVIEW
Plant Signaling & Behavior 8:4, e23681; April 2013; 2013 Landes Bioscience
Reactive oxygen species signaling in plants under
abiotic stress
Shuvasish Choudhury,1,2 Piyalee Panda,2 Lingaraj Sahoo3 and Sanjib Kumar Panda2,*
1
Central Instrumentation Laboratory; Assam University; Silchar, India; 2Plant Molecular Biotechnology Laboratory; Department of Life Science and Bioinformatics; Assam
University; Silchar, India; 3Department of Biotechnology; Indian Institute of Technology Guwahati; Guwahati, India
Keywords: abiotic stress, antioxidants, reactive oxygen species, signaling
Abiotic stresses like heavy metals, drought, salt, low
temperature, etc. are the major factors that limit crop
productivity and yield. These stresses are associated with
production of certain deleterious chemical entities called
reactive oxygen species (ROS), which include hydrogen
peroxide (H2O2), superoxide radical (O2-), hydroxyl radical (OH-),
etc. ROS are capable of inducing cellular damage by degradation
of proteins, inactivation of enzymes, alterations in the gene
and interfere in various pathways of metabolic importance.
Our understanding on ROS in response to abiotic stress is
revolutionized with the advancements in plant molecular
biology, where the basic understanding on chemical behavior
of ROS is better understood. Understanding the molecular
mechanisms involved in ROS generation and its potential role
during abiotic stress is important to identify means by which
plant growth and metabolism can be regulated under acute
stress conditions. ROS mediated oxidative stress, which is the
key to understand stress related toxicity have been widely
studied in many plants and the results in those studies clearly
revealed that oxidative stress is the main symptom of toxicity.
Plants have their own antioxidant defense mechanisms to
encounter ROS that is of enzymic and non-enzymic nature.
Coordinated activities of these antioxidants regulate ROS
detoxification and reduces oxidative load in plants. Though
ROS are always regarded to impart negative impact on plants,
some reports consider them to be important in regulating key
cellular functions; however, such reports in plant are limited.
Molecular approaches to understand ROS metabolism and
signaling have opened new avenues to comprehend its critical
role in abiotic stress. ROS also acts as secondary messenger that
signals key cellular functions like cell proliferation, apoptosis
and necrosis. In higher eukaryotes, ROS signaling is not fully
understood. In this review we summarize our understanding
on ROS and its signaling behavior in plants under abiotic stress.
Introduction
Reactive oxygen species (ROS) is considered as unavoidable
chemical entity of aerobic life.1,2 They are considered as by
*Correspondence to: Sanjib Kumar Panda; Email: drskpanda@gmail.com
Submitted: 01/17/13; Accepted: 01/18/13
http://dx.doi.org/10.4161/psb.23681
Citation: Choudhury S, Panda P, Sahoo L, Panda SK. Reactive oxygen species
signaling in plants under abiotic stress. Plant Signal Behav 2013; 8: e23681
www.landesbioscience.com Plant Signaling & Behavior e23681-1
MINI-REVIEW
2013 Landes Bioscience. Do not distribute
product of aerobic metabolism and whose production is confined
to cellular compartments with strong electron flow. These include
chloroplast, mitochondria and peroxisomes. ROS includes
hydrogen peroxide (H2O2), superoxide radical (O2-), hydroxyl
radical (OH) and singlet oxygen (1O2) etc. ROS exerts wide
range of physiological responses in plants along with changes in
cellular structure and degrades enzymes, proteins, nucleic acid,
etc.1 It has been hypothesized that ROS production can be the
primary symptom of phytotoxicity and this mechanism has been
widely studies in plants under abiotic stress.3 ROS productions in
plants have a distinctive property of exerting its serious impact
on metabolism. Higher the production of ROS more will be the
toxicity and in such conditions the plant growth is affected. Loss
of crop productivity under abiotic stress is indeed related to high
production of ROS (Fig. 1). In plant cells, the ROS production
is strictly regulated by ROS scavenging pathways involving enzy-
mic and non-enzymic antioxidants. Under unfavorable condi-
tions, for example, during abiotic stress the balance is disturbed
due to diminution of antioxidants leading to oxidative stress. In
higher plants, abiotic stress induces the formation of ROS leading
to wide range of physiological changes. ROS generation under
the influence of heavy metal, salinity, drought, etc. leads to lipid
peroxidation, degradation of antioxidants and ultimately initiates
changes in gene expression. The generation of ROS is a com-
mon event during all types of abiotic stress regardless of the plant
species.
Redox metabolism and its associated signaling are important
machinery during abiotic stress.4 During the course of evolu-
tion, plants have accomplished high degree of control over ROS
and successfully used them as a signaling molecule.5 Mitller et
al.5 in their review showed that in Arabidopsis, ROS like H2O2
and O2- can act as a signaling molecule, which requires a huge
gene network comprising of about 152 genes. Moreover, related
studies with Arabidopsis have also unravelled certain important
components in ROS signaling involving receptor proteins, redox-
sensitive transcription factors and ROS induced inhibition of
phosphatases.5 In this review we focus on the basic mechanisms
of ROS signaling in plants under abiotic stress.
Redox Homeostasis in Plants: Role of Antioxidants
In the course of evolution, plants have learned to scavenge the
deleterious effects of ROS which is achieved by an array of anti-
oxidants. These scavengers interact with cellular components and

Figure 1. Generation of reactive oxygen species (ROS) by various abiotic stress factors in plants.
provide defense against the ROS.6 Antioxidants play the criti-
cal role of ROS removal and its activation is directly correlated
with defense against abiotic stress and plant development.6 The
survival in the stressed environment requires stable redox state,
which practically needs efficient antioxidant pathways to remove
the ROS in different cellular compartments.2,7,8 In order to have
an efficient antioxidant activity, cellular and physiological pro-
cesses needs to be effective. ROS are produced in cells constantly
and any imbalance between ROS and antioxidants implicates to
oxidative stress.9 ROS generation is also genetically programmed.8
For examples, ROS like H2O2 and O2- acts as second messengers,
but its accumulation at high levels causes oxidative stress leading
to cell death.
The major antioxidants that play crucial role in ROS detoxi-
fication includes ascorbic acid (AA), -tocopherol, glutathi-
one, catalase (CAT), peroxidases (POX), superoxide dismutase
(SOD), glutathione reductase (GR) etc. Synchronized action
of these antioxidants result in detoxification of ROS and limit
oxidative stress in plants (Fig. 2). Ascorbic acid is distributed
in almost all the plants. It is synthesized in the mitochondria
and transported to other parts of the plants.8,10,11 AA is used as
e23681-2 Plant Signaling & Behavior Volume 8 Issue 4
2013 Landes Bioscience. Do not distribute
a substrate by ascorbate peroxidase (APX) to reduce H 2O2 to
H 2O in the ascorbateglutathione cycle and generate mono-
dehydroascorbate, which further dissociate to AA and dehy-
droascorbate.12 Under abiotic stress conditions, the role of AA
is diverse. Decline or elevation of AA content was reported in
plants under heavy metal stress.3,13-15 -tocopherol along with
other antioxidants scavenges lipid peroxy radical.8,16 It acts as
lipophilic antioxidant and interacts with polyunsaturated acyl
groups of lipids and reduces the deleterious effects of ROS.17
-tocopherol stabilizes membrane and also acts as substance
that modulates signal transduction. Glutathione are non-pro-
tein thiols that has a key role in H 2O2 detoxification.6,8,18 It has
been reported that the conversion ratio of reduced glutathione
(GSH) to its oxidized form (GSSG) during the detoxification
of H 2O2 is the indicator of cellular redox balance.8 These events
were widely reported in plants under various abiotic stresses.
Glutathione and AA are now considered as important compo-
nent of redox signaling in plants.19-21
One of the major lines of defense against ROS is superox-
ide dismutase (SOD) along with other enzymes like ascorbate
peroxidase (APX), glutathione peroxidase (GPX) and catalase

Figure 2. Antioxidant system in plants involved in detoxification of reactive oxygen species through various pathways.
(CAT). SOD converts superoxide to H 2O2, while APX, GPX
and CAT detoxifies H 2O2.22 The conversion of H2O2 to H2O by
APX requires ascorbate and reduced glutathione (GSH) regener-
ation system via ascorbate-glutathione cycle. H2O2 is converted
to H 2O by oxidation of ascorbate to mono dehydroascorbate
(MDA), which further dismutate to dehydroascorbate.22 Like
APX, GPX uses GSH as a reducing agent to detoxify H 2O2
to H 2O. The organellar redox state is regulated by different
enzymic antioxidants like glutathione reductase (GR), mono
dehydroascorbate reductase (MDHAR) in addition to GPX.23
It was observed that these redox regulator enzymes along with
ROS network genes are co-expressed in chloroplast and mito-
chondria, which can be important in understanding redox
state.5,23,24 Several reports suggest that certain GPX genes are
sturdily induced by ROS.6,25-27 In comparison to other enzy-
mic antioxidants like CAT and ascorbate peroxidase, GPX has
got minimum role to play in peroxide metabolism.6 Studies on
plant GPX genes have revealed significant homology with mam-
malian phospholipid hydroperoxide GPX (PHGPX), which has
got high empathy for lipid hydroperoxide rather than H2O2.
Further the overexpressions of PHGPX in transgenic plants
have shown better stress tolerance.6,28 Obviously, the degree
of oxidative stress is determined by the level of ROS and the
balance between ROS and antioxidants is essential to main-
tain balanced redox state. Under abiotic stress conditions, the
activities of certain antioxidants are disrupted. During such
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2013 Landes Bioscience. Do not distribute
conditions activity of other antioxidants are upregulated. Thus,
the balance between ROS production and antioxidant activity
is essential.
ROS Signaling in Plants
Chemically, ROS appears to be detrimental to cellular function.
Genetic evidences suggest that ROS can also act as a signal-
ing molecule in regulating diverse function in plants.6 O2- and
H2O2, which are considered as primary ROS in plants can act
as secondary messenger in plants by regulating diverse func-
tion of growth and development.6,29 The generation of ROS
in cell organelles like chloroplast and mitochondria are capa-
ble of inducing changes in the nuclear transcriptome, but the
mechanism of signal transduction still remains unclear to some
extent.22 ROS can influence gene expression by modifying tran-
scription factors.22 In the past few decades, significant progress
have been achieved in understanding ROS signaling in plants
and now it is clear beyond doubt that ROS acts as major sig-
naling molecule in diverse processes in plants.30 For examples,
H2O2 production is triggered during both biotic and abiotic
stress. This ROS, which is produced by the cytosolic membrane
bound NADPH oxidase is regarded as a signal during abiotic
stress.31 ROS influences expression of several genes, suggesting
that ROS acts as a biological signal in regulating stresses.31,32
Laloi et al.31 stated that ROS interacts with the target molecule
selectively. When the ROS concentration is increased, it con-
veys the change in gene expression. It was further stated that
such changes at gene level occurs via oxidation of components
of the signaling pathways resulting in the activation of tran-
scription factors or possibly those transcription factors that are
redox sensitive.31 Studies on mitogen activated protein kinase
(MAPK) in Arabidopsis have revealed that H2O2 can activate
MAPK (AtMPK3 and At MPK6 ) and sturdily induces nucleo-
tide diphosphate kinase 2 (AtNDPK2).31,33 Plants appear to be
tolerant to H2O2 due to controlled antioxidant system that helps
in the complete elimination of it and maintains the steady redox
state.34,35 In several reports, the role of glutathione and ascorbate
in redox signaling in plants have been emphasized.19,21,34,35 This
aspect has been critically discussed in one of the previous sec-
tions of this paper.
Chloroplast redox state has been well explored to understand
redox-regulated gene expression in plants.35,36 Any change in the
redox state of the chloroplast affects expression of chloroplast
proteins. In the chloroplast, plastoquinone (PQ), ascorbate, glu-
tathione and ROS along with ferredoxin or thioredoxin system
are the key signaling components.36 The photosystem II (PSII) is
associated with production of 1O2 and both photosytem I (PSI)
and PSII with O2-.37-38 Studies on flu mutants of Arabidopsis have
shown that 1O2 signaling associated with programmed cell death
(PCD) possesses certain explicit characteristic in terms of gene
induction as compared with other ROS.30,40 Lee et al.41 identified
proteins associated with 1O2 signaling, the EXECUTOR 1 and 2
proteins, which repress the 1O2 induced cell death. Peroxisomes
are the major sites of H2O2 production thorough different bio-
chemical reactions. During photosynthesis in C3 plants, peroxi-
somes generate high amount of H2O2 that is light dependent and
as such the antioxidant efficiency is extensively high in those
organelles.35 These include enzymes like CAT, APX and those
associated with ascorbate/glutathione system.35,42 These enzymes
are required for scavenging H2O2. The decline in the activity of
CAT during photorespiration leads to accumulation of oxidized
glutathione.35 It was also emphasized that the accumulation of
ascorbate and glutathione can balance CAT deficit briefly and the
glycollate oxidase reaction may be involved in passing the signal
from the chloroplast to peroxisomes.35,43 Such events have been
reported in plants under drought and high temperature stress.35
The cellular redox homeostasis has a direct correlation with
mitochondrial redox state. Since, the ROS scavenging capacity
of mitochondria is less as compared with chloroplast and peroxi-
somes, the stability of its own redox state decides the fate of total
cellular redox status.35
In comparison to mitochondria, the ROS production in chlo-
roplast and peroxisomes is high. Despite of this fact, the amount
of oxidized protein in mitochondria is high.35,38 One of the expla-
nations for presence of high concentration of oxidized protein
is possibly due to its susceptibility to ROS. Some of these oxi-
dized proteins are part of mitochondrial electron transport com-
plex I and III.38 The complexes are involved in ROS production,
which resulted in protein oxidation; moreover, certain proteins
are matrix proteins where oxidation takes place after ROS are
released from the inner mitochondrial membrane.38 Available
e23681-4 Plant Signaling & Behavior Volume 8 Issue 4
data suggests that the low ROS production in mitochondria is
mainly due to the presence of alternative oxidase (AOX).43,44
However, increase in the mitochondrial ROS production regu-
lates programmed cell death (PCD) in plant cells.31,45
Abiotic stress induces ROS production vis--vis plants have
evolved strategies to counteract ROS. Several phyto-compounds
like salicylic acid (SA), abscisic acid (ABA), jasmonic acid (JA)
and phytohormones regulate the protective responses in plants
under abiotic stress. The involvement of ROS in crosstalk with
2013 Landes Bioscience. Do not distribute
these phytocompounds has not been fully understood yet. For
example, ABA is comprehensively associated with wide range of
abiotic stress and administers growth and development process in
plants.46 In contrast to ABA, other phytocompounds like SA, JA
and ethylene have significant role during biotic stress and often
ABA acts as negative regulator of disease resistance.46
Cellular Retrograde Signaling
The organellar gene expression is regulated by nucleus. The
organelles in turn send signals that affect and regulate the nuclear
gene expression, called retrograde signaling. Retrograde signal-
ing coordinates the gene expression, metabolism and develop-
ment between the organelles and the nucleus that later modulates
the anterograde process.23 During adverse stress conditions, ROS
are produced in the chloroplast and mitochondria. The redox
state and metabolism in these organelles are important sources
of retrograde signals that play a potential role in stress acclima-
tion in plants.23,47 The chloroplast retrograde signaling is well
studied.48 The chloroplast-nucleus retrograde signaling involves
multiple signaling pathways of which Mg-Protoporphyrin IX
(Mg-PPIX) is best studied.48 However, the chloroplast retrograde
signaling is still not properly understood. Studies on carotenoid
biosynthesis inhibitors norflurazon and mutants of Arabidopsis
with underdeveloped chloroplast have shown that chloroplast
communicates signals to the nucleus that alter nuclear gene
expression.23,48 This is dependent on the presence of GUN1 in
the chloroplast and AB14 in the nucleus.23 Moreover, accumu-
lation of Mg-PPIX and Mg-PPIX methylester also alters the
gene expression in Arabidopsis.48 Recent studies in Arabidopsis
Mg-PPIX have shown that approximately 35% of identified pro-
teins are related to wide range of stress responses.23 These include
glutathione S-transferases (AtGST10, AtGSTT1 and AtGSTF3)
and peroxidases (ATP15, APX1, PER22 and ATP3), which play
a significant role in degradation of Mg-PPIX.23,49 The chloro-
plast-nucleus signal transduction mediated by ROS involves the
process of protein phosphorylation.48 The involvement of 1O2 in
chloroplast retrograde signaling has been studied in Arabidopsis
(flu) mutants using microarray, which revealed certain distinct
set of genes that are activated by 1O2.23,39
In contrast to chloroplast, the mitochondrial retrograde sig-
naling is not clearly understood. The mitochondrial ROS sig-
naling engages the elevated expression of alternative oxidase 1
(AOX1). The AOX1 is encoded by the nucleus and signifies itself
as a key biomarker for mitochondrial retrograde signaling.23 To
date, there is no such evidence of any protein involved in mito-
chondrial retrograde signaling. In Arabidopsis mutants deficient
in mitochondria retrograde signaling were unable to induce
luciferase activity driven by AOX1a promoter in retort to anti-
mycinA treatment.50,51 This clearly indicates that though signifi-
cant achievement has been made to understand ROS retrograde
signaling in plants, it is still not clear that how such regulation
is achieved. (Note to Author: Please cite refs. 15 and 37)
Conclusion
and development. Plants have developed complex antioxidant
defense mechanisms that limit the production of ROS and vis-
-vis removes them from the cellular environment. Recent stud-
ies on ROS have designated them to be important messengers
that are involved in transducing signals of metabolic impor-
tance. ROS mediated expression of genes that are important
in regulating developmental process and survival of plants in
adverse conditions have been elucidated. Though significant
advances have been achieved to understand the role of ROS in

2013 Landes Bioscience. Do not distribute

Aerobic life has made the presence of ROS inevitable. During
the course of evolution, plants have equipped themselves
to hunt the deleterious effects of ROS and subsequently use
them in different biological processes. High concentration of
ROS in cells as a result of abiotic stress limits plant growth
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