Oxidative Stress in Plants and Its
Sachin Teotia and Deepali Singh
We all live in an oxygen-rich environment which has to deal with the
danger of oxidative stress. During normal cell metabolism, reactive oxygen species (ROS) are constantly produced, mainly by respiratory and
photosynthetic components. These species mainly include superoxide
radicals (O2!), singlet oxygen (1O2), hydrogen peroxide (H2O2), and
hydroxyl radical (OH!). The others are hydroperoxyl radical (HO2˙),
alkoxy radical (RO˙), peroxyl radicals (ROO˙), and excited carbonyl
(RO). But during stress conditions like salinity, drought, metal toxicity,
herbicides, fungicides, air pollutants, hypoxia, and abnormal conditions of
light, temperature, and topography, ROS are produced in excess amount.
These highly reactive molecules can react with many cellular
biomolecules and other components and damage DNA, proteins, and
lipids. Thus, their concentration has to be tightly controlled. To counter
the deleterious effects of ROS, aerobic organisms are equipped with
antioxidant systems to scavenge ROS from the cells. Enzymatic
antioxidants are mainly superoxide dismutase (SOD), catalase, ascorbate
peroxidase, glutathione peroxidase, glutathione S-transferases, and
peroxiredoxin, while the nonenzymatic antioxidants are mainly ascorbate,
glutathione, proline, tocopherol, flavonoids, and carotenoids. These
antioxidants protect against the oxidative damage by inhibiting or
quenching free radicals and ROS. When the balance between the production of ROS and the quenching activities of antioxidants is disturbed, the
cell faces the risk of oxidative stress and damage. These ROS creating
stresses are numerous and often species or area specific. These stresses
cause significant crop losses. There is a growing need to develop crops
which can be resistant to the effects of various oxidative stresses. One
such way is to develop transgenic plants overexpressing one or more
S. Teotia (*) " D. Singh
School of Biotechnology, Gautam Buddha University,
Greater Noida 201312, India
e-mail: [email protected]
R.K. Gaur and P. Sharma (eds.), Approaches to Plant Stress and their Management,
DOI 10.1007/978-81-322-1620-9_13, # Springer India 2014
S. Teotia and D. Singh
antioxidants, which can confer resistance towards particular stress.
Another way is to develop mutants which are resistant towards certain
Reactive oxygen species " Oxidative stress tolerance " Enzymatic
Antioxidants " Nonenzymatic antioxidants " Transgenic plants and
Oxygen is the primary source of life. In an oxygen
atmosphere, the generation of ROS, especially
under metabolic stress, is unavoidable. ROS are
also produced continuously as by-products of various metabolic pathways localized in different
cellular compartments such as chloroplast,
mitochondria, peroxisomes, and apoplast (del Rio
et al. 2006; Panieri et al. 2013). Many metabolic
processes normally produce ROS, which comprise
mainly of superoxide radical, hydrogen peroxide,
hydroxyl radical, and singlet oxygen. ROS may
also be produced by abiotic stress such as salinity,
drought, heavy metals, nutrient deficiency,
herbicides, fungicides, air pollutants, ozone, light,
temperature, topography, and hypoxia and by
biotic factors such as pathogen attacks. Oxidative
stress is programmed to be a regulated process, and
the equilibrium between ROS and its quenching
determines the well-being of a plant. Oxidative
damage of cells happens when the balance
between the production of ROS and their
quenching by antioxidants reaches the state of
disequilibrium. The extent of oxidative stress
depends on the type of ROS that is produced, the
concentration and the site where it is released, their
interaction with other molecules in the cell, and the
developmental stage and potential of the cell
(Moller et al. 2007). The enhanced and prolonged
production of ROS can cause significant damage
to cell structures in plants like lipid peroxidation,
protein oxidation, damage to nucleic acids,
enzyme inhibition, and programmed cell death
(Mittler 2002; Perez-Perez et al. 2012) (Fig. 1).
However, plants have evolved protective scavenging systems in response to these ROS. High levels
of ROS are kept in check by dynamic and
synergistic mechanisms of ROS-scavenging
antioxidants that control the concentration of intracellular ROS (Apel and Hirt 2004). An antioxidant
is described as a compound capable of scavenging
ROS without itself undergoing conversion to a
destructive radical (Noctor and Foyer 1998).
These antioxidants can be conveniently divided
into two groups: enzymatic and nonenzymatic
antioxidants (Fig. 1).
Reactive Oxygen Species (ROS)
ROS are mostly free radicals produced as byproducts of redox reactions. ROS is formed as a
natural by-product of the normal metabolism in
the presence of oxygen. In plant cells, ROS are
continuously produced as a consequence of
aerobic metabolism in all of the the intracellular
organelles; as by-products in the electron transport chains of chloroplasts, mitochondria, and the
plasma membrane (cytochrome b-mediated electron transfer); and in peroxisomes (Apel and Hirt
2004; Asada 1999). Several apoplastic enzymes
may also lead to ROS production under normal
and stress conditions. ROS include a number of
molecules derived from oxygen, such as oxygen
ions, free radicals, and peroxides. All of these
molecules are highly reactive due to the presence
of unpaired electrons at valence shell. ROS
have important roles in cell signaling, cellular
homeostasis, and oxidative stress (Kotchoni and
Gachomo 2006; Neill et al. 2002). ROS play two
main divergent roles in plants; when present in
low concentrations, they act as signaling
molecules mediating several responses in plant,
Oxidative Stress in Plants and Its Management
Fig. 1 Diagrammatic representation of various agents generating ROS in plants and various antioxidants scavenging
those ROS molecules
including growth and development, and
responses under stresses, whereas when present
in high concentrations, they cause extensive
damage to cellular components. However, as
described above, during times of various environmental stresses, ROS levels can increase dramatically. Thus, ROS has multiple roles in cells,
and therefore, it is not feasible to eliminate them
completely, but at the same time, it is extremely
necessary to control them tightly to avoid any
oxidative damage. High levels of ROS can cause
damage to cellular structures, nucleic acids,
lipids, and proteins (Bergamini et al. 2004;
Wiseman and Halliwell 1996). ROS is quenched
by a number of enzymatic antioxidants and
molecules (see next section) (Fig. 1). The problem arises in stressful conditions, when there is
disequilibrium between ROS production and its
quenching. Then, modulation of ROS by the
antioxidants is necessary for the survival of the
cell. When the level of ROS in a cell exceeds
the antioxidative capacity of the antioxidants, a
cell is said to be in a state of oxidative stress.
Superoxide Radicals (O2!)
In plants, photosynthesis takes place in
chloroplasts, and oxygen is generated which can
accept electrons passing through the photosystems, thus forming O2!. O2! is mainly produced in the thylakoid membrane-bound primary
electron acceptor of photosystem I. Normally O2
is converted to H2O by transfer of four electrons,
but occasionally O2 can react with other electron
transfer chain components and only one electron
is transferred, producing the O2! (Giba et al.
1998). With one unpaired electron, O2! is a
free radical (Forman et al. 2004). The generation
of O2! may trigger the formation of more reactive ROS like OH!, 1O2, and also H2O2
(Halliwell 2006).
Singlet Oxygen (1O2)
Singlet oxygen, 1O2, is the first excited electronic
state of O2 and is not related to electron transfer
to O2. During photosynthesis in plants, sometimes insufficient energy dissipation can lead to
the formation of a chlorophyll triplet state that
can transfer its excitation energy to ground-state
O2 to form 1O2 (Halliwell 2006). This can oxidize chloroplast molecules and also trigger cell
death. Additionally, 1O2 is formed by low intercellular CO2 concentration in the chloroplast
resulting from the closed stomata because of
various abiotic stresses such as salinity and
drought. 1O2 production has also been produced
as a mechanism of resistance in plant–pathogen
interactions through the production of
phytoalexins (Flors and Nonell 2006; Flors
et al. 2006). Formation of 1O2 during photosynthesis has a substantial damaging effect on essential components of the whole photosynthetic
machinery. 1O2 activates a signaling cascade
that can stimulate a specific gene expression
response and can interact with signal cascades
of other ROS, thereby activating several stressresponse pathways (op den Camp et al. 2003).
O2 is highly diffusive and destructive, as it
reacts with most biomolecules and rapidly
oxidizes amino acids, lipids, pigments, and
DNA (Agnez-Lima et al. 2012; Fischer et al.
2013). It reacts with nitric oxide (NO) to form
peroxynitrite (ONOO!).
Hydrogen Peroxide (H2O2)
H2O2 is mainly produced by dismutation of O2! by
superoxide dismutase (SOD), NADPH oxidase,
cell-wall peroxidase, amino oxidase, oxalate oxidase, and flavin-containing oxidase (Neill et al.
2002). Excess of H2O2 in the plant cells leads to
the occurrence of oxidative stress. H2O2 is moderately reactive, relatively stable, and highly diffusible. At low concentrations, H2O2 acts as a signaling
molecule involved in mediating the acquisition of
tolerance to both biotic and abiotic stresses (Desikan
et al. 2004), while at high concentrations, it leads to
programmed cell death (Quan et al. 2008). H2O2
oxidizes the thiol groups of enzymes and thereby
S. Teotia and D. Singh
inactivates them. It plays a role as an intermediate in
the formation of other ROS, including hypochlorous
acid (HOCl) and •OH.
Hydroxyl Radicals (OH!)
This radical is formed from H2O2 in a reaction
catalyzed by metal ions (Fe2+ or Cu+), often
present in complex with different proteins or
other molecules. This is known as the Fenton
reaction: Fe2+ + H2O2 ! Fe3+ + •OH + OH!.
OH! can also be produced from O2! and H2O2
at neutral pH and ambient temperatures by the
iron-catalyzed O2!. This is called the
Haber–Weiss reaction: O2! + H2O2 ! •OH +
OH! + O2. OH! is the most reactive among
all ROS and dangerous as it can potentially
react with all biomolecules like DNA, proteins,
lipids, and almost any constituent of cells and
ultimately leads to cell death (Halliwell 2006).
It causes lipid peroxidation, protein damage, and
membrane destruction.
Effects of ROS
On Metabolism
Lipid peroxidation: When higher ROS levels are
reached, lipid peroxidation takes place in both
cellular and organelle membranes, thereby not
only directly affecting normal cellular functioning but also aggravating the oxidative stress
through production of lipid-derived radicals
(Catala 2010). Hydroperoxyl radical (HO2˙)
which is formed from O2! by protonation in
aqueous solutions can subtract hydrogen atoms
from polyunsaturated fatty acids (PUFAs) and
lipid hydroperoxides and cause lipid autooxidation. Because of the presence of double
bonds, PUFAs are excellent targets for attack
by free radicals (particularly 1O2 and OH!),
forming mixture of lipid hydroperoxides
(LOOH) (Moller et al. 2007). Extensive PUFA
peroxidation decreases the membrane fluidity,
increases leakiness, and causes secondary damage to membrane proteins (Moller et al. 2007).
Oxidative Stress in Plants and Its Management
Protein oxidation: It is defined as covalent modification of a protein which can be induced by
ROS or components of oxidative stress. Reaction
of proteins with ROS causes modifications in the
form of the following: (i) side chains oxidation
mainly at cysteine, methionine, and tryptophan;
(ii) carbonylation; (iii) nitrosylation; and (iv)
interaction with products of PUFA oxidation
(Moller et al. 2007). Formation of a disulfide
between two cysteine residues to form cystine
and oxidation of methionine to form methionine
sulfoxide are some of the common modifications.
Other amino acids can also be target of redox
modifications in proteins. Protein nitrosylation
mainly involves the covalent attachment of a
nitric oxide (NO) group to the thiol side chain
of select cysteine residues. This attachment
impacts the protein function. But among all
modifications, protein carbonylation is the main
feature of protein oxidation. Carbonylation of
amino acid residues like arginine, lysine, threonine, or proline is one of the most commonly
occurring oxidative modifications of proteins.
This modification might lead to alteration in protein activity, its proteolytic breakdown or aggregate formation (Debska et al. 2012; Moller et al.
On Growth and Development
Oxidative stress has marked effect on growth and
development of plants. The common stressassociated phenotypes seen under various abiotic
stresses have been termed stress-induced morphogenetic response (SIMR; (Potters et al. 2007)).
Typical SIMR responses include decreases in
root length, stem height, and leaf area, altered
xylem development, and redistribution of cell
division and elongation (reviewed by (Potters
et al. 2009)).
DNA Damage
Exposure to various biotic and abiotic stress
factors might damage the DNA and exerts
genotoxic stress (Balestrazzi et al. 2011; Tuteja
et al. 2009). OH! is most reactive and damages
both purine and pyrimidine bases and also
deoxyribose backbone of the DNA molecule
(Cooke et al. 2003). This can induce cleavage of
DNA, base deletion, formation of pyrimidine
dimers, DNA–protein cross-links, and alkylation
and oxidation of bases of DNA (Tuteja et al.
2001). 1O2 primarily attacks guanine and
converts it into eight-hydroxyguanine (Britt
1996). In addition to mutations, oxidative
DNA modifications can lead to changes in the
methylation of cytosines, which is important for
regulating gene expression (Moller et al. 2007).
Cellular Protection Against Oxidative
Stress by Scavenging of ROS
Under normal conditions, the ROS molecules are
scavenged by various antioxidants (Foyer and
Noctor 2005). In order to control ROS levels
and protect the cells from oxidative damage,
plants deploy a complex antioxidant defense system which scavenges the ROS. These antioxidant
systems include various enzymes and nonenzymatic metabolites that may also play a significant
role in ROS signaling in plants (Vranova et al.
2002). Many of these enzymes and molecules
are overexpressed and accumulate in various
stressed conditions.
Enzymatic Antioxidants
Superoxide Dismutase (SOD)
SOD is the most effective intracellular enzymatic
antioxidant which is ubiquitously found in all
cellular compartments of organisms (Table 1).
SODs are metalloproteins that catalyze
dismutation of superoxide radical (O2!) into O2
and H2O2. SODs are classified by their metal
cofactors into three known families: CuZnSODs,
localized in cytosol or in plastids; MnSOD,
mainly restricted to mitochondria; and FeSOD,
localized in the plastid (Asensio et al. 2012).
These SODs can be tissue specific such as
CuZnSOD (Ogawa et al. 1997; Karlsson et al.
2005) or MnSOD (Corpas et al. 2006). SOD acts
Table 1 ROS-scavenging enzymes and molecules
Antioxidant enzymes
Superoxide dismutase
Ascorbate peroxidase
Glutathione peroxidase
Glutathione reductase
Glutathione Stransferases
Methionine sulfoxide
E. C.
Cyt, Chl, Mit,
Per Gly, Cyt, Mit,
Per Cyt, Per, Chl,
Chl stroma,
Mit, Cyt
Cyt, Chl, Mit
Reaction(s) catalyzed
2O2! + 2H+ ! 2H2O2 + O2
2H2O2 ! O2 + 2H2O
2AsA + H2O2 ! 2MDHA + 2H2O
Vac, Chl, Cyt, Donor + H2O2 ! oxidized donor + 2H2O
Mit, ER Cyt, Chl, Mit, ROOH + 2RSH ! ROH + RSSR + H2O
Nuc Cyt, Mit, Chl GSH + ROOH ! GSSG + ROH + 2H2O
GSH + H2O2 ! GSSG + 2H2O
Cyt, Chl, Mit NADPH + GSSG ! NADP+ + GSH Cyt, Mit, Chl RX + GSH ! HX + R-S-GSH
Cyt, Chl, Mit,
Cyt, Chl, Mit,
Nuc Cyt, Chl, Mit,
Subcellular localization
Chl, Apo, Cyt, Vac, Mit,
Met. + thioredoxin disulfide ! Met.(S)-S oxide + Thioredoxin
Thioredoxin + NADP+ ! thioredoxin disulfide + NADPH
Arsenate + glutaredoxin ! arsenite + glutaredoxin
disulfide + H2O
Antioxidant molecules
Reaction(s) catalyzed
Ascorbate (vitamin C)
O2! + AsA + H+ ! A.! + H2O2
O2 + AsA + H+ ! H2O2 + DHA
H2O2 + AsA ! MDHA + 2H2O
Glutathione (GSH)
Chl, Apo, Cyt, Vac, Mit, ROOH + 2GSH ! ROH + GSSG + H2O
Scavenges H2O2, OH!, and 1O2
Cyt (normal conditions), Proline + OH!/1O2 ! proline nitroxide/proline peroxide
Chl (stressed conditions)
Cell and Chl memb
α-Tocopherol + 1O2 ! α-tocopherylquinone
(vitamin E)
Also, scavenges OH, ROO,·and ROOH (lipid peroxyl) radicals in
thylakoid membranes
Carotenoids (ß-Carotene Chl, chromoplast,
Quench 1O2 by involving their own oxidation and forming
and zeaxanthin)
elaioplast, and
β-carotene endoperoxide in high-light conditions,
modulate formation of triplet chlorophyll, and prevent formation
of 1O2
Vac, Nuc, Chl, Apo, Cyt, Scavenge H2O2 and OH!
ER, Cwl
Nuc, Chl, Mit, Cyt, Vac, Scavenge O2!, 1O2, OH!
Glycine betaine
Stabilizes PS II repair proteins and alleviate lipid peroxidation
O2 singlet oxygen, A.!, ascorbate free radical, AsA ascorbate, Apo apoplast, APX ascorbate peroxidase, Cyt cytosol,
Chl chloroplast, Cwl cell wall, DHA dehydroascorbate, DHAR dehydroascorbate reductase, ER endoplasmic reticulum,
Gly glyoxysomes, GSH glutathione, GSSG oxidized glutathione, GSTs glutathione S-transferases, H+ hydrogen ion,
H2O water, H2O2 hydrogen peroxide, Met methionine, MDHA monodehydroascorbate, MDHAR monodehydroascorbate reductase, Mit mitochondria, NADP+ nicotinamide adenine dinucleotide phosphate, NADPH reduced
NADP+, Nuc nucleus, O2 oxygen, O2! superoxide radical, OH˙ hydroxyl radical, Per peroxisomes, PSII photosystem
II, R may be an aliphatic, aromatic, or heterocyclic group, ROO! peroxy radical, ROOH organic peroxide, S sulfide, SP
secreted pathway, Vac vacuole, X may be a sulfate, nitrite, or halide group
Oxidative Stress in Plants and Its Management
in the first line of defense against the toxic effects
of elevated levels of ROS. The SODs remove
superoxide radical and hence decrease the risk
of OH! formation. SODs are upregulated in
response to many abiotic and biotic stresses and
have a crucial role in the survival of plants
under stressed conditions (Alscher et al. 2002;
Raychaudhuri and Deng 2000). There have been
many reports of the production of both biotic and
overexpressing different SODs (Table 2).
MDHAR has a high specificity for monodehydroascorbate (MDHA) as the electron acceptor
and NADPH as the electron donor. Oxidation
of ascorbate (AsA) leads to the formation of
MDHA. If MDHA is not reduced again to AsA
by MDHAR, it will spontaneously convert
into AsA and dehydroascorbate (DHA). Therefore, MDHAR rapidly reduce MDHA to AsA
using NADPH. This rapid regeneration is
necessary in order to maintain the antioxidative
capacity of AsA.
Catalase (CAT)
CAT is a heme-coordinated tetrameric protein
encoded by nuclear genes that plays an important
role in maintaining cellular concentration of
hydrogen peroxide to a level, necessary for all
aspects of normal plant growth and development.
CATs are located mostly in peroxisomes and
glyoxysomes, where they play a key role in the
removal of H2O2 generated by various oxidases.
CAT directly dismutates H2O2 into H2O and O2
and are required for ROS detoxification during
stressed conditions (Mittler et al. 2004). CAT
also reacts with some hydroperoxides.
Dehydroascorbate Reductase (DHAR)
DHAR is a monomeric thiol enzyme which
regenerates ascorbate from dehydroascorbate
(DHA) (Foyer and Mullineaux 1998). DHAR
catalyzes the reduction of DHA to AsA using
GSH as the reducing substrate. This is a key in
conferring tolerance to various abiotic stresses
which produce ROS. Stresses such as drought,
chilling, ozone, and metal toxicity increase the
activity of the DHAR in plants (Maheshwari and
Dubey 2009; Yoshida et al. 2006). It has also
been found that DHAR overexpression also
enhances plant tolerance against various abiotic
stresses (Lee et al. 2007) (Table 2).
Thus, MDHAR and DHAR are equally
important in regulating the level of AsA and its
redox state under oxidative stress (Eltayeb et al.
2006, 2007).
Ascorbate Peroxidase (APX)
The APX are heme-containing enzymes. The APX
family has many isoforms located at different subcellular locations like thylakoid (tAPX),
glyoxisome membrane (gmAPX), chloroplast
stroma (sAPX), and cytosol (cAPX) (Da˛browska
et al. 2007). APX is involved in scavenging of
H2O2. APX catalyzes the reduction of H2O2 to
water and uses ascorbate as a reductant for this
reaction (Shigeoka et al. 2002; Asada 1999). The
scavenging of H2O2 by APX is the first step of
the ascorbate–glutathione (ASH-GSH) cycle.
APX activity is enhanced in plants in response to
different abiotic stresses. In Arabidopsis thaliana
APX activity increased during exposure of plants
to ozone, sulfur dioxide, chilling, and UV-B (Kubo
et al. 1995; Rao et al. 1996).
Guaiacol Peroxidase (GPOX)
GPOX is a heme-containing protein. GPOX has a
role in the biosynthesis of lignin and defense
against biotic stresses by consuming H2O2.
GPOX in plants use guaiacol and pyrogallol as a
reducing substrate to oxidize many substrates in
the presence of H2O2 (Vianello et al. 1997). This
means that GPOX oxidize certain substrates at the
expense of H2O2 and rid the cell of excess peroxide produced, especially under stress conditions.
They are also effective quenchers of reactive
intermediary forms of O2 and peroxyl radicals.
Monodehydroascorbate Reductase
MDHAR is a flavin adenine dinucleotide (FAD)
enzyme, present in cytosol and chloroplast.
Peroxiredoxins (PRXs)
Peroxiredoxins are non-heme containing peroxidases, which have to rely on an external electron
donor to reduce H2O2, alkyl hydroperoxide, and
S. Teotia and D. Singh
Table 2 Transgenic plants accumulating various antioxidant enzymes and molecules
Gene and source
Superoxide dismutase (SOD)
FeSOD from Arabidopsis thaliana
Transgenic organism
Nicotiana tabacum
Cu/ZnSOD from Hevea brasiliensis
Hevea brasiliensis
Chloroplastic Cu/ZnSOD from Pisum
Nicotiana tabacum
MnSOD from Triticum aestivum
Brassica napus
MnSOD from Nicotiana
MnSOD from Pisum sativum
Medicago sativa
Oryza sativa
Cu/Zn SOD from Spinacia oleracea
Malus domestica
Cu/Zn SOD from Oryza sativa
Nicotiana tabacum
Cu/Zn SOD from Avicennia marina
Oryza sativa
Cu/Zn SOD from Solanum
Cytosolic Cu/ZnSOD from Solanum
Solanum tuberosum
MnSOD from Tamarix androssowii
Populus davidiana
Catalase (CAT)
Catalase from Broccoli
Arabidopsis thaliana
Catalase gene, katE, from E. coli
Oryza sativa
Catalase gene, Cat2, from Zea mays
Nicotiana tabacum
Catalase gene, Cat2, from Nicotiana
Catalase gene from Triticum aestivum
Solanum tuberosum
Beta vulgaris
Oryza sativa
Ascorbate peroxidase (APX)
Ascorbate peroxidase-like 1 gene from Nicotiana tabacum
Capsicum annuum
tAPX from Brassica napus
Brassica napus
Response of transgenic against
various stresses
Enhanced tolerance to oxidative
stress induced by methyl viologen
Protection against ROS and
tolerance to water deficit
Resistance against MV-mediated
oxidative stress
(Van Camp
et al. 1996)
Tolerance against heat stress by
removing H2O2
Tolerance against salt stress by
removing H2O2
Tolerance to MV-mediated
oxidative stress and resistance to
bacterial pathogen
Enhanced resistance to fungal
pathogen, P. infestans
Increased resistance to lowtemperature stress by removing
(Chiang et al.
et al. 2007)
et al. 2001)
(Leclercq et al.
(Gupta et al.
1993a; Kwon
et al. 2002)
Resistance to aluminum
(Basu et al.
Resistance to cold stress
et al. 1999)
Resistance to drought and MV and (Wang et al.
polyethylene glycol (PEG)-induced 2005)
oxidative stress
Resistance to high and freezing
(Artlip et al.
Enhanced tolerance to salt, water, (Badawi et al.
and PEG stresses
Tolerance to MV-mediated
oxidative stress, salinity and
et al. 2008)
drought stress
Elevated tolerance to MV
(Perl et al.
Increased tolerance to MV and to (Tertivanidis
leaf infection with the fungus
et al. 2004)
Cercospora beticola
Enhanced salt tolerance
(Wang et al.
Increased tolerance to MVmediated oxidative stress and to the
oomycete pathogen, Phytophthora
Increases resistance to salt stress
and drought, and reduced
accumulation of H2O2
(Yu et al.
et al. 2002)
(Sarowar et al.
(Wang et al.
Oxidative Stress in Plants and Its Management
Table 2 (continued)
Gene and source
cAPX from Pisum sativum
APX3 from Arabidopsis thaliana
Two cytosolic ascorbate peroxidases
from Oryza sativa
Glutathione reductase (GR)
GR from bacteria
Transgenic organism
Nicotiana tabacum
Arabidopsis thaliana
GR from E. coli
A poplar hybrid,
Populus tremula x
Populus alba
Nicotiana tabacum
GR from Pisum sativum
Nicotiana tabacum
Monodehydroascorbate reductase (MDHAR)
cMDHAR from Solanum lycopersicum Solanum
MDAR1 gene from Arabidopsis
Nicotiana tabacum
Dehydroascorbate reductase (DHAR)
DHAR from Homo sapiens
Nicotiana tabacum
DHAR from Oryza sativa
Arabidopsis thaliana
cDHAR from Arabidopsis thaliana
Nicotiana tabacum
cDHAR from Arabidopsis thaliana
Nicotiana tabacum
Glutathione S-transferases (GSTs)
GST and GPX from tobacco
Nicotiana tabacum
GST from cotton
Nicotiana tabacum
GST from maize
Triticum aestivum
GST from rice
Oryza sativa
GST from Trichoderma virens
Nicotiana tabacum
GST, from wild soybean (Glycine soja) Nicotiana tabacum
GST from maize
Nicotiana tabacum
Response of transgenic against
various stresses
Tolerance to chilling and salt stress (Wang et al.
Increases protection against
(Wang et al.
oxidative stress
Increases protection against salt
(Lu et al. 2007)
Tolerance to oxidative stress
caused by MV
(Foyer et al.
(Lederer and
Tolerance to oxidative stress
caused by MV, H2O2, heavy metal Boger 2003;
stress, and UV-B radiation
Poage et al.
Tolerance to oxidative stress
(Creissen et al.
caused by MV
Resistant to salt- and PEG-induced
osmotic stress, showing lower level
of H2O2, higher APX activity.
Enhanced tolerance to temperature
and MV-mediated oxidative
Enhanced tolerance against ozone,
salt, and PEG stress
(Li et al.
2010a; Li et al.
Enhanced tolerance to MV, H2O2,
low temperature, and salt
Enhanced resistance to salt stress
(Kwon et al.
et al. 2006)
(Yin et al.
(Eltayeb et al.
Enhanced tolerance to aluminum
Enhanced tolerance to ozone,
drought, salt, and PEG stresses
Enhanced tolerance to oxidative,
chilling, and salt stress
Enhanced tolerance to oxidative
stress induced by a low
concentration of MV
Tolerant to herbicide
(Eltayeb et al.
(Roxas et al.
2000, 1997)
(Yu et al.
(Milligan et al.
Enhanced tolerance to low
et al. 2002)
Enhanced tolerance to cadmium
(Dixit et al.
Enhanced tolerance to drought and (Ji et al. 2010)
Higher tolerance to alachlor
et al. 2005)
S. Teotia and D. Singh
Table 2 (continued)
Gene and source
GST from Prosopis juliflora
Transgenic organism
Nicotiana tabacum
GST (GSTL1) from Oryza sativa
GST (GSTL2) from Oryza sativa
Oryza sativa
Arabidopsis thaliana
Peroxiredoxins (PRXs)
2-Cys PRX from Arabidopsis thaliana
Response of transgenic against
various stresses
Enhanced tolerance to drought
Enhanced tolerance to herbicides
Enhanced tolerance for heavy
metals and other abiotic stresses
like cold, osmotic stress and salt
(George et al.
(Hu et al. 2009)
(Kumar et al.
Tall fescue (Festuca Increased tolerance against heat
arundinacea) and
and MV
Solanum tuberosum L.
cv. Atlantic
Nicotiana tabacum
Improved resistance to MV and
Botrytis infection
Arabidopsis thaliana Increased tolerance to salt and cold
Nicotiana tabacum
Increased tolerance to oxidative
(Kim et al.
2010, 2011)
GRX5 from Pteris vittata
Arabidopsis thaliana
Enhanced tolerance to oxidative
and heat stress
More tolerance to arsenic
(Wu et al.
et al. 2009)
Thioredoxin (TRX)
TRX-h1 from Oryza sativa
Oryza sativa
More tolerance to salt stress
(Zhang et al.
(Li et al. 2010b)
PRX-Q from Gentiana triflora cv.
Yahaba Y514
PRX-Q from Suaeda salsa
1-Cys- PRX from Oryza sativa
Glutaredoxin (GRX)
AtGRXS17 from Arabidopsis thaliana
P-TRX from Phalaris coerulescens
Hordeum vulgare
Methionine sulfoxide reductase (MSR)
Peptide MSR from Arabidopsis
Arabidopsis thaliana
MSRB2 gene from Capsicum annuum Solanum
MSRB3 from Arabidopsis thaliana
Arabidopsis thaliana
Cytosolic MSRB7 and MSRB8 from
Arabidopsis thaliana
MSRA4.1 from Oryza sativa
Arabidopsis thaliana
Oryza sativa
Glutathione Peroxidase (GPX)
GPX from Chlamydomonas
Nicotiana tabacum
GST and GPX from Nicotiana tabacum Nicotiana tabacum
GPX2 from Synechocystis
Arabidopsis thaliana
Increased aluminum resistance
(Kiba et al.
(Jing et al.
(Lee et al.
Enhanced tolerance to MV and
high light in cold conditions
Showed reduced production of
H2O2 and resistance towards
Phytophthora capsici and
Phytophthora infestans
Enhanced tolerance to MV and cold
Enhanced tolerance to MV and
H2O2 treatment
Enhanced tolerance to salt stress
(Romero et al.
(Oh et al.
Increased tolerance to oxidative
stress caused by MV, cold, and salt
Increased tolerance to cold and salt
Enhanced tolerance to oxidative
damage caused by H2O2, MV, Fe
ions, and other stresses such as
chilling, high salinity, or drought
et al. 2004)
(Kwon et al.
(Li et al.
(Guo et al.
(Roxas et al.
(Gaber et al.
Ascorbate (AsA)
L-Gulono-gamma-lactone oxidase from Solanum tuberosum L. Increased levels of AsA in transgenic (Hemavathi
cv. Taedong Valley
plants leading to enhanced tolerance et al. 2010)
to MV, salt, and mannitol
Oxidative Stress in Plants and Its Management
Table 2 (continued)
Gene and source
acid reductase from
strawberry (this enzyme converts Dgalacturonic acid into L-Galactonic acid
which is converted to L-galactono-1,4lactone, the immediate precursor of AsA)
Glutathione (GSH)
Glutathione synthetase (GS) from E.
Glutathione synthetase enzyme from
Streptococcus thermophilus
γ-Glutamylcysteine synthetase and
Glutathione synthetase from Brassica
γ-Glutamylcysteine synthetase (γ-ECS)
from Oryza sativa
γ-Glutamylcysteine synthetase (γ-ECS)
from E. coli
Response of transgenic against
Transgenic organism various stresses
Solanum tuberosum L. Increased levels of AsA in
cv. Taedong Valley
transgenic plants leading to
et al. 2009)
enhanced tolerance to MV, salt, and
Brassica juncea
Enhanced tolerance to cadmium
Nicotiana tabacum
Enhancing tolerance to abiotic
Enhanced tolerance to atrazine; 1chloro-2, 4-dinitrobenzene;
phenanthrene; and metolachlor
Enhanced tolerance to salt and MV (Choe et al.
Enhanced tolerance to
(Gullner et al.
chloroacetanilide herbicides,
acetochlor, and metolachlor
Brassica juncea
Oryza sativa
Poplar hybrid
(Populus tremula X
Populus alba)
Proline (Pro)
P5CS from Vigna aconitifolia L.
Nicotiana tabacum
P5CS from Vigna aconitifolia L.
Medicago truncatula
P5CS from Vigna aconitifolia L.
Cicer arietinum
Osmotin gene
Nicotiana tabacum
P5CS from Vigna aconitifolia
P5CS from Vigna aconitifolia
Oryza sativa L. ssp.
indica cv. ADT 43
Triticum aestivum
P5CR from Triticum aestivum
Arabidopsis thaliana
P5CR from Arabidopsis thaliana
Glycine max
Ornithine-δ-aminotransferase (δ-OAT)
from Arabidopsis thaliana
Oryza sativa L. ssp.
japonica cv.
Zhongzuo 321
Arabidopsis thaliana
Antisense of proline dehydrogenase
(ProDH) from Arabidopsis thaliana
Tocopherols (TOCs)
Tocopherol cyclase (VTE1) from
Arabidopsis thaliana
VTE2.1 from Solanum chilense
Nicotiana tabacum
Nicotiana tabacum
Carotenoids (CARs)
Beta-carotene ketolase gene (bkt) from Daucus carota
green algae
(Liang Zhu
et al. 1999)
et al. 2010)
(Flocco et al.
Increased tolerance to osmotic
Enhanced tolerance to osmotic
Enhanced tolerance to salt stress
(Kishor et al.
(Verdoy et al.
(Kiran Kumar
Ghanti et al.
Enhanced tolerance to salinity and (Barthakur
et al. 2001)
Enhanced tolerance to salt stress
et al. 2011)
Enhanced tolerance to drought
et al. 2007)
Enhanced stress tolerance
(Ma et al.
Enhanced tolerance to heat and
(De Ronde
drought stress
et al. 2004)
Accumulation of proline and
(Liangqi et al.
enhanced tolerance to drought and 2003)
salt stress
Proline accumulation and more
(Nanjo et al.
tolerance to freezing and high
Enhanced tolerance to drought
induced oxidative stress
Increased tolerance to oxidative
stress damage as evidenced by
reduced lipid peroxidation and
delayed leaf senescence
(Liu et al.
et al. 2013)
Plants accumulate ketocarotenoids
and show enhanced tolerance to
UV-B radiation, H2O2, and MV
(Jayaraj and
Punja 2008)
S. Teotia and D. Singh
Table 2 (continued)
Gene and source
chyB gene that encodes beta-carotene
hydroxylase to make zeaxanthin from
Arabidopsis thaliana
chyB gene that encodes beta-carotene
hydroxylase from Arabidopsis thaliana
DSM2 gene which encodes β-carotene
hydroxylase (BCH) from Oryza sativa
Flavonoids (FLVs)
Anthocyanidin synthase (ANS) from
Oryza sativa
Flavonol synthase 1 (FLS1) from Zea
Polyamines (PAs)
decarboxylase (SAMDC) from yeast
Arginine decarboxylase (ADC) from
Datura stramonium
Spermidine synthase (SPDS) from
apple (Malus domestica)
Spermidine synthase (SPDS) from
Cucurbita ficifolia
ADC from oat (Avena sativa)
Transgenic organism
Arabidopsis thaliana
Nicotiana tabacum
Oryza sativa
Oryza sativa mutant
Nootripathu (NP)
Arabidopsis thaliana
Oryza sativa
Nicotiana tabacum
var. Xanthi
SAMDC from carnation (Dianthus
caryophyllus L.) flower
SPDS from Cucurbita ficifolia
Nicotiana tabacum
Choline oxidase (codA) from
Arthrobacter globiformis
Choline monooxygenase (CMO) from
Atriplex hortensis
Choline dehydrogenase (CDH),
encoded by betA from E. coli
Choline monooxygenase (CMO) from
Spinacia oleracea
Betaine aldehyde dehydrogenase
(BADH) from Spinacia oleracea
A chloroplastic BADH from Spinacia
More tolerance to drought stress,
reduced lipid peroxidation
Increased resistance to drought and
oxidative stresses and increase of
the xanthophylls and nonphotochemical quenching
(Zhao et al.
(Du et al.
Accumulation of a mixture of
flavonoids and anthocyanins, with
increased antioxidant potential
Increased resistance to UV-B
(Reddy et al.
Enhanced tolerance to hightemperature stress
Enhanced tolerance to drought
(Cheng et al.
(Capell et al.
(Wen et al.
et al. 2004)
European pear (Pyrus Enhanced tolerance to salinity,
communis L. ‘Ballad’) osmotic, and heavy metal stress
Arabidopsis thaliana Enhanced tolerance to chilling,
freezing, salinity, hyperosmosis,
drought, and MV
Oryza sativa
Enhanced tolerance to salt stress
SAMDC from human
Glycine betaine (GB)
Choline oxidase (codA) from
Arthrobacter globiformis
Response of transgenic against
various stresses
More tolerance to high light, high (Davison et al.
temperature, and lipid peroxidation 2002)
(Emiliani et al.
(Roy and Wu
(Waie and
Rajam 2003)
Enhanced tolerance to salinity,
drought, and fungal pathogens (V.
dahliae and F. oxysporum)
Enhanced tolerance to salt, cold,
acidic, and abscisic acid stress
Increased tolerance to chilling,
heat, and MV
(Wi et al.
et al. 2006)
lycopersicum Mill. cv.
Solanum tuberosum L.
cv. Superior
Gossypium hirsutum
Enhanced tolerance to chilling,
high salt, and oxidative stresses
(Park et al.
Enhanced tolerance to salt,
drought, and MV
Increased tolerance to salt stress
Nicotiana tabacum
Improved tolerance to salinity and
cold stress
Enhanced tolerance to salt stress
and temperature stress
Protection of Rubisco activity in
high-temperature stress
Improved tolerance to salt,
oxidative stress, and low
(Ahmad et al.
(Zhang et al.
et al. 2000)
et al. 2006)
(Yang et al.
(Fan et al.
Ipomoea batatas, cv.
Kokei 14
Oryza sativa
Nicotiana tabacum
Ipomoea batatas,
Oxidative Stress in Plants and Its Management
Table 2 (continued)
Gene and source
Aldose/aldehyde reductase from
Medicago sativa
Transgenic organism
Oxalate oxidase (OxO) from wheat
Nicotiana tabacum
Nicotiana tabacum
Apolipoprotein D ortholog (AtTIL) from Arabidopsis thaliana
Arabidopsis thaliana
Aldehyde dehydrogenase ALDH3I1 and Arabidopsis thaliana
ALDH7B4 from Arabidopsis thaliana
BcZAT12 from Brassica carinata
cv. H-86
Serotonin N-acetyltransferase (NAT)
Oryza sativa
from sheep, producing more melatonin
Isoprene synthase from Populus alba,
producing more isoprene
Nicotiana tabacum
other peroxides. This electron donor is often
reduced thioredoxin; hence, PRXs are often
called thioredoxin peroxidases. The PRX family
in plants can be divided into four groups (A to D)
(Dietz 2011). A-type PRX are 2-Cys peroxiredoxin (2-CysPRX), the B-type PRX are 1-Cys
peroxiredoxin (1-CysPRX), the C-type PRX are
peroxiredoxin Q (PRX-Q), and the D-type PRXs
are type II peroxiredoxins (PRXII). These four
groups can be further divided depending on their
subcellular locations. In plants, 2-Cys-PRXs are
the most abundant PRXs and are located in
chloroplasts. The 2-Cys-PRXs reduce peroxides
through a thiol-based mechanism. During catalysis, these enzymes are sometimes inactivated by
the substrate-dependent oxidation of the catalytic
cysteine to the sulfinic acid (!SO2H) form
and are reactivated by reduction carried by
sulfiredoxin (SRX) (Jonsson et al. 2008).
Glutathione Peroxidase (GPX)
GPXs are considered as a fifth class of PRX, but
evolutionary PRX and GPX are considered two
different protein families. GPXs are a large family
of diverse isozymes (Rodriguez Milla et al. 2003).
GPXs help plants alleviate oxidative stress by
reducing a broad range of hydroperoxides, including H2O2 and organic and lipid hydroperoxides
Response of transgenic against
various stresses
Tolerance against oxidative
damage caused by paraquat, heavy
metal treatment, and drought
Increased tolerance to MV or high
light-induced oxidative stress
Enhances tolerance to freezing and
oxidative stress
Enhances tolerance to osmotic and
oxidative stress
Tolerance to heat-shock
(HS)-induced oxidative stress
et al. 2000)
Increased resistance to the singletoxygen-generating peroxidizing
herbicide butafenacil and increased
SOD and CAT activity
Increased resistance to ozoneinduced oxidative damage and high
(Park et al.
(Wan et al.
(Charron et al.
et al. 2006)
(Shah et al.
(Vickers et al.
(LOOH) (Arthur 2000). They use GSH to do this
function. They help prevent lipid peroxidation of
cellular membranes by removing free peroxide in
the cell. GPX also functions as an oxidative signal
transducer (Miao et al. 2006). GPXs are reduced
by thioredoxins.
Glutathione Reductase (GR)
GR is a flavoprotein oxidoreductase and is a key
player against ROS defense by maintaining the
reduced status of glutathione (GSH). It is
localized mainly in chloroplasts but also in
small amounts in mitochondria and cytosol
(Edwards et al. 1990). GR catalyzes the conversion of GSSG into GSH (Meister and Anderson
1983). GR transfers electrons from NADPH to
GSSG to generate GSH. Thus, GR maintains a
high ratio of GSH/GSSG in plant cells which is
important for scavenging H2O2. GR and GSH
play a crucial role in determining the tolerance
of a plant under various stresses (Foyer et al.
1997). In rice, expression of GR was found to
be induced by ABA and chilling, drought, and
salinity (Kaminaka et al. 1998).
Glutathione S-Transferases (GSTs)
Plant GSTs can be divided into eight classes of: phi,
tau, theta, zeta, lambda, dehydroascorbate reductase
(DHAR), EF1Bγ and tetrachlorohydroquinone
dehalogenase (TCHQD). Arabidopsis encodes
about 55 GSTs (Dixon and Edwards 2010). GSTs
catalyze the transfer of the tripeptide glutathione (γglutamyl-cysteinyl-glycine; GSH) to a cosubstrate
(R-X) containing a reactive electrophilic center to
form a polar S-glutathionylated reaction product (RSG). GSTs detoxify electrophilic herbicides and
other xenobiotics by catalyzing their conjugation
with GS, to produce less toxic and more watersoluble conjugates. Apart from herbicide detoxification, plant GSTs are known to function in hormone homeostasis, tyrosine metabolism,
hydroxyperoxide detoxification, and plant
responses to various stresses. GST activity in
plants is induced in response to many abiotic
stresses (Dixon et al. 2010). GSTs safeguard
proteins from oxidative damage and maintain
redox homeostasis by regenerating AsA from
DHA (Dixon and Edwards 2010).
S. Teotia and D. Singh
are composed of six well-defined types (TRXs f, m,
x, y, h, and o) that reside in different cell
compartments and function in different processes
(Meyer et al. 2005). TRX can exist either in reduced
(dithiol) or in oxidized (disulfide) form. Reduced
TRX acts to directly reduce protein disulfides and
cysteine sulfenic acid (Meyer et al. 2012).
Land plants contain a large GRX family.
GRXs are small, nearly ubiquitous, oxidoreductases constituting an alternative reducing
system to TRXs. GRXs catalyze the reduction
of disulfide bonds of their substrate proteins in
the presence of glutathione (GSH) and help
binding of iron–sulfur clusters (Rouhier 2010).
GRXs are important proteins for the response of
plants to oxidative stress because they help in
regenerating antioxidant enzymes. GRXs are
directly reduced by GSH to produce GSSG.
Nonenzymatic Antioxidants
Methionine Sulfoxide Reductase (MSR)
In proteins, methionine (Met) residues are especially sensitive to oxidation, as ROS can oxidize
them to form S and R methionine sulfoxide
(MetSO) diastereoisomers. Thus, Met residues
form Met-S-sulfoxide or Met-R-sulfoxide, causing inactivation or malfunction of the proteins.
To rescue the proteins, the oxidized forms of
methionine, S-MetSO and R-MetSO, are reduced
back to Met by the MetSO reductases, MsrA and
MsrB, respectively (Sharov and Schoneich
2000). These proteins catalyze the thioredoxindependent reduction of MetSO back to Met (Brot
et al. 1981), thereby repairing proteins. MSRs are
proposed to act as a last-chance antioxidants and
importantly repair proteins damaged from oxidative stress (Cabreiro et al. 2006).
Glutaredoxin (GRX) and Thioredoxin (TRX)
(GRX) constitute families of thiol oxidoreductases,
furnishing reducing power to PRX, MSR, and arsenate reductases, which are key players for the plant
response to the oxidative environment.
TRXs are small redox proteins, widely
distributed, and function in redox regulation in a
broad spectrum of cellular reactions. Plant TRXs
Ascorbate (AsA)
AsA is the most potent and abundant antioxidant
that protects the cell from the damage caused by
ROS in plants (Foyer and Noctor 2011; Smirnoff
2007). Exogenous application of AsA renders the
plants to be resistant to salt stress as shown in case
of durum wheat (Azzedine et al. 2011). AsA can
directly scavenge O2!, OH!, and 1O2 and reduce
H2O2 to water via ascorbate peroxidase reaction
(Noctor and Foyer 1998). APX requires a reducing substrate, ascorbate, which is then oxidized to
monodehydroascorbate (MDHA). Transgenic
plants overexpressing genes leading to increased
ascorbate content confer resistance to oxidative
and other stresses (Table 2). AsA is a reduced
form, while its oxidized forms are MDHA and
DHA. Regeneration of AsA is catalyzed by either
MDHAR (from MDHA) or DHAR (from DHA)
by using NADPH or reduced glutathione (GSH),
respectively. AsA also maintains α-tocopherol in
a reduced state. AsA regenerate tocopherol from
tocopheroxyl radicals, thus providing protection
to the membranes. Exogenous application of
AsA positively influences the activity of many
antioxidative enzymes and minimizes the oxidative damage (Shalata and Neumann 2001).
Oxidative Stress in Plants and Its Management
Glutathione (GSH)
Reduced glutathione (GSH) is a major watersoluble antioxidant in plant cells, localized in
all cell compartments (Table 1) (Moran et al.
2000). GSH is a tripeptide (γ-glutamylcysteinyl-glycine), which is synthesized from
Cys and that exists interchangeably with the
oxidized form, GSSG, and is vital for normal
cellular function. Two sequential ATPdependent reactions allow the synthesis of γglutamylcysteine (γ-EC) from L-glutamate and
L-cysteine, followed by the formation of GSH by
addition of glycine to the C-terminal end of γ-EC
(Meister 1988). These reactions are catalyzed by
γ-glutamylcysteine synthetase (γ-ECS) and glutathione synthetase (GS). Glutathione plays
important roles in protecting cells from biotic
and abiotic stress. In a cell, it is the major antioxidant and major cellular redox buffer which
directly scavenges most free radicals and reactive oxygen species (Noctor and Foyer 1998).
GSH is a key ROS scavenger and can protect
macromolecules like proteins, lipids, and DNA
by acting as a proton donor forming GSSG. The
reduced state of cells brought by GSH
counteracts the effects of oxidative stress
(Meyer 2008) by scavenging 1O2, H2O2, and
OH! (Alscher 1989). Additionally, GSH is critical in regenerating another antioxidant like
ascorbate (AsA), via the ASH-GSH cycle
(Foyer and Halliwell 1976). Biosynthesis of glutathione is stimulated under oxidative stress
conditions, as GSH gets converted to GSSG. In
oxidative stress, GSH prevents the denaturation
of proteins caused by the oxidation of protein
thiol groups. Moreover, GSH acts as a substrate
for GPX and GST, which are also involved in the
removal of ROS (Noctor et al. 2002).
The AsA-GSH cycle constitutes one of the
most important antioxidant systems in plants.
In this cycle, the ascorbate and the glutathione
are utilized as reducers which are recycled through
consuming the ATP and NADPH by the action of
four enzymes: APX, MDHAR, DHAR, and GR.
Proline (Pro)
Pro is also considered as a potent antioxidant and
potential inhibitor of adverse effects of ROS
(Krishnan et al. 2008; Matysik et al. 2002;
Szabados and Savoure 2010). In plants the synthesis of L-Pro takes place from L-glutamic
acid by the action of enzymes D1-pyrroline-5carboxylate synthetase (P5CS) and D1pyrroline-5-carboxylate
(Verbruggen and Hermans 2008). Following
salt, drought, and metal stress, there is a dramatic
accumulation of Pro. Free Pro has been proposed
to act as an osmoprotectant, a protein stabilizer, a
metal chelator, maintainer of redox homeostasis,
and OH! and 1O2 scavenger (Ashraf and Foolad
2007; Matysik et al. 2002). Pro appeared as an
effective scavenger of OH! (Smirnoff and
Cumbes 1989). The constitutive or stressinducible expression of P5CS cDNA in plants
leads to Pro accumulation and confers tolerance
to various abiotic stresses (Hmida-Sayari et al.
2005; Su and Wu 2004) (Table 2).
Tocopherols (TOCs)
TOCs are lipid-soluble antioxidant and are potential scavengers of ROS (Shao et al. 2007). TOCs
are considered general antioxidants for protection
of membrane stability, including quenching or
scavenging ROS like 1O2 and OH!(KriegerLiszkay and Trebst 2006). TOCs are localized in
plants in the thylakoid membrane of chloroplasts.
Out of the four isomers of TOCs (α, β, γ, δ) found
in plants, α- and γ-tocopherol are predominant. αtocopherol has the highest antioxidant activity,
which together with the hydrophilic antioxidants,
glutathione and ascorbate participates in the detoxification of ROS (Kamal-Eldin and Appelqvist
1996). TOCs also reduce lipid peroxyl radicals
(LOO!) to their corresponding hydroperoxides
(Maeda et al. 2005). TOCs also participate in cell
signaling. Oxidative stress activates the expression
of genes responsible for the synthesis of TOCs in
higher plants (Ahmad et al. 2008a). Tocopherol
cyclase (VTE1) catalyzes the penultimate step of
TOC synthesis Porfirova et al. 2002.
Carotenoids (CARs)
CARs are the most abundant pigmented plantderived compounds. CARs are considered to be
the first line of defense of plants against toxicity.
Like TOCs, CARs are lipid-soluble antioxidants
that play a role in oxidative stress tolerance (Edge
et al. 1997). Oxygenated CARs are known as
xanthophylls. Examples of these compounds are
zeaxanthin and lutein. In all photosynthetic
organisms, the carotenoids β-carotene and zeaxanthin, together with TOCs play a photoprotective
role, either by dissipating excess excitation energy
as heat or by scavenging ROS and suppressing
lipid peroxidation. They play a role of an antioxidant by preventing the formation of singlet oxygen
by quenching the triplet chlorophylls (Chl3) and
other harmful free radicals which are naturally
formed during photosynthesis (Ramel et al. 2012).
Flavonoids (FLVs)
FLVs are a group of polyphenolic compounds
produced as secondary metabolites by plants.
FLVs occur widely in the plant kingdom and accumulate in the plant vacuole as glycosides and also
as exudates on the surface of leaves and other
aerial plant parts. FLVs serve as ROS scavengers
by neutralizing harmful radicals under adverse
environmental conditions (Agati et al. 2007).
FLVs absorb UV light, and plants able to synthesize these compounds were more tolerant to high
UV irradiation than mutants impaired in the flavonoid pathway (Emiliani et al. 2013). FLVs play a
key role in quenching free radicals, 1O2, and
decomposing peroxides (Vieyra et al. 2009).
Many flavonoid biosynthetic genes are induced
under stress conditions (Kim et al. 2012).
Polyamines (PAs)
PAs are a group of natural compounds with aliphatic nitrogen structure and present in almost all
living organisms. Putrescine, spermidine, and
spermine are the most commonly found PAs in
higher plants and could be present in free,
soluble-conjugated, and insoluble-bound forms.
PAs play important roles in plant growth and
development (Kusano et al. 2008). They are also
potent ROS scavengers and inhibitors of lipid peroxidation (Belle et al. 2004). The accumulation of
conjugated and free polyamines in plants is very
important for their protection against oxidative
stress induced by abiotic factors (Jang et al. 2012;
Nayyar and Chander 2004). Among the common
polyamines, putrescine appears to be the most sensitive for external stress. Plant PAs are involved
in imparting tolerance to such stresses such as
cold, heat, salinity, hyperosmosis, hypoxia, and
S. Teotia and D. Singh
atmospheric pollutants (Liu et al. 2007). An exogenous supply of polyamines can protect plant
against ozone damage (Bors et al. 1989). PAs are
powerful OH! scavengers and can also quench
O2! at a higher concentrations (Drolet et al.
1986). Spermine or spermidine also can quench
O2 at higher concentrations (Das and Misra
2004). Exogenously applied PAs counteracted the
toxic effects of paraquat in Arabidopsis (Kurepa
et al. 1998a).
Glycine Betaine (GB)
GB is a nitrogenous compound, a quaternary
amine. GB is synthesized by either oxidation of
choline or N-methylation of glycine (Chen and
Murata 2002). In plants, the enzyme choline
monooxygenase (CMO) first converts choline
into betaine aldehyde, followed by the action of
betaine aldehyde dehydrogenase (BADH) (a
NAD+, dependent enzyme), to produce glycine
betaine. These enzymes are mainly found in chloroplast stroma. GB biosynthetic genes have been
widely used to improve abiotic stress in transgenic
plants (Chen and Murata 2011). GB biosynthetic
gene, choline oxidase (codA) from Arthrobacter
globiformis, has been widely used for GB production in transgenic plants (Ahmad et al. 2008b;
Park et al. 2004). codA converts choline into GB
in a single step. GB has been implicated in
inhibiting ROS accumulation and activation of
some stress-related genes. It helps in controlling
water balance but can also help to maintain protein and membrane structure. During salt or
drought stress, synthesis of proteins involved in
PSII repair is affected, leading to photoinhibition.
GB stabilizes those PSII repair proteins and thus
helps in the repair of PSII, which eventually
increases stress tolerance (Li et al. 2013). There
have been reports of GB alleviating lipid peroxidation (Li et al. 2013; Cruz et al. 2013).
Genetic Engineering of Oxidative
Stress Resistance in Plants
Development of Transgenic Plants
A number of transgenic plants with improved
tolerance to various abiotic stresses have been
Oxidative Stress in Plants and Its Management
achieved through development of plants
overexpressing enzymes involved in oxidative
protection, such as GPX, SOD, APX, GST, and
GR (Gupta et al. 1993a, b; Lee et al. 2007; Lu
et al. 2007; Miao et al. 2006; Roxas et al. 1997)
(Table 2). Sometimes, overexpression of one
gene may not be enough to confer desired stress
resistance upon transgenic plants (Lee et al.
2009). In those cases combinations of two or
more antioxidants in transgenic plants have
shown to have synergistic effects on stress tolerance (Tseng et al. 2008). Therefore, there has
been increased emphasis on production of such
transgenic plants.
Development of Mutants
Many plant mutants show reduced tolerance to
oxidative stress (Charron et al. 2008; Filkowski
et al. 2004; Li et al. 2011; Ning et al. 2010; Shin
et al. 2009). But there are several examples of
plant mutants which show enhanced tolerance to
oxidative stress as summarized in Table 3.
Conclusions and Future Perspectives
ROS are unavoidable part of cell metabolism.
They are generated by electron transport
activities of chloroplast, mitochondria, and
plasma membrane or as a by-product of various
metabolic pathways in different cellular
compartments. ROS can also be produced as
result of various prolonged abiotic stresses.
Under normal environmental conditions, ROS
production in various cell compartments is low.
These ROS are highly reactive and toxic and
ultimately result in oxidative stress and damage
to the cell. In oxidative stress ROS or free
radicals are generated which can damage the
biomolecules and cell structures and homeostasis, including oxidative damage to nucleic acids,
lipids, and proteins. This leads to altered membrane properties like fluidity, loss of enzyme
activity, protein structures, folding and crosslinking, inhibition of protein synthesis, DNA
damage, impaired ion transport, and apoptosis.
The free radicals of ROS interact with each other
and also with antioxidant systems. If ROS has to
play a role of signaling molecules or preventing
the spread of pathogens, their localization and
concentration needs to be controlled. For this
purpose, plant cell and its compartments like
chloroplast, mitochondria, and peroxisomes
deploy antioxidant defense systems to protect
themselves against the oxidative damage caused
by ROS. This repertoire of antioxidants
comprises of enzymatic and nonenzymatic
components. When ROS is produced in excess
or when the antioxidant defense system is not
properly functioning, the cell faces the danger
of oxidative damage.
To evaluate the negative role of ROS, it is
important to understand mechanisms of its resistance and tolerance in plants. In the recent years,
a lot of progress has been done in the field of
oxidative stress, but still a lot of gaps in our
knowledge of ROS metabolism and their effects
on plants are left. Further progress in the fields of
genomics, proteomics, and metabolomics will
help in untying the knots of hidden biochemical
networks involved in establishing oxidative
stress in the cell. Knowledge of improved understanding of these, together with the biotechnological tools, will be helpful in producing plants
with enhanced levels of tolerance to ROS. Past
and ongoing research has already proven that
induced expression of various antioxidant
enzymes and accumulation of various antioxidant
molecules have key roles in detoxification of
ROS. Overexpression of ROS-scavenging
enzymes like SODs, CAT, APX, GPX, PRX,
GR, MDHAR, DHAR, and GST results in abiotic
stress tolerance in various crop plants due to
increased ROS-scavenging capacity. Significant
loss to the yield of crops is done because of the
cumulative effect of abiotic stress factors. Therefore, steps for better understanding of the
mechanisms of abiotic stress and finding the
ways that would increase stress tolerance in plants
are crucial for nations’ economy and worldwide
agriculture. ROS detoxification system is very
complex and controlled at multiple levels in various subcellular locations, and modulating one
component of the antioxidative defense system
Table 3 Mutants showing tolerance to oxidative stress
Response against
oxidative stresses
Resistance to ROS
generating herbicides
aminotriazole (AT)
and MV
Involved in karrikin and
Increased tolerance
strigolactone signaling
to MV and H2O2
NAC-domain transcription
Increased tolerance
factor regulates senescence in to MV and H2O2
Involved in ethylene signal
Increased tolerance
to MV and H2O2
Forms subunits of histone
Increased tolerance
acetyltransferase complex
to MV and CsCl
Involved in signal
Increased tolerance
transduction of plant defense to H2O2
and trichome development
Involved in photoautotrophic Increased tolerance to
salt tolerance
MV, high-light intensity
Mutated gene
AAL-TOXIN RESISTANT Arabidopsis Not known
(ATR) 1, 2, 7, 9
(Gechev et al.
2008; Qureshi
et al. 2011)
ORE9 (AT2G42620)
(Woo et al. 2004)
ORE1 (AT5G39610)
ORE3 (AT5G39610)
ELONGATOR subuntis,
ELP2 and ELP6
Arabidopsis A putative PARP protein,
interacts with many stressrelated transcription factors
SIMILAR TO RCD ONE 1 Arabidopsis
(Woo et al. 2004)
(Woo et al. 2004)
(Zhou et al.
(Hong-Ying et al.
(Tsugane et al.
(Ahlfors et al.
2004; Overmyer
et al. 2000;
Fujibe et al.
(Teotia and
A putative PARP protein has Increased tolerance to
redundant roles with RCD1
H2O2, salt, and osmotic Lamb 2009)
Promotes flowering under
Increased tolerance
(Kurepa et al.
long days in a circadian clock- to MV
controlled flowering
Encodes an SIncreased tolerance
(Chen et al.
nitrosoglutathione reductase
to MV
that is a key regulator of cell
Glycosylate the 3-OH of
Increased tolerance
(Lim et al. 2008)
hydroxycinnamates and
to MV
Poly (ADP-ribosylation) of
Increased tolerance to
(De Block et al.
target proteins
MV, high light, drought, 2005)
and heat
Involved in the brassinolide
Increased tolerance
(Cao et al. 2005)
biosynthetic pathway
to oxidative stress
Reduction of α-tocopherol and Increased tolerance
(Abbasi et al.
increase in γ-tocopherol
to MV and sorbitol
Silencing of γ-tocopherol Nicotiana
methyltransferase (γtabacum
Lysine decarboxylase-like Oryza sativa Accumulation of the
polyamines, putrescine,
spermidine, and spermine
under conditions of oxidative
GLUTATHIONE SArabidopsis Participates in light signaling
and affects GSH and ABA
Peroxiredoxin Q
Arabidopsis Peroxiredoxin Q decomposes
peroxides using thioredoxin as
an electron donor
Increased tolerance to
MV, UV-B, freezing,
and osmotic stress
Reduced accumulation (Jang et al. 2012)
of ROS after exposure to
oxidative, high salt, and
acid stresses
Plants were more
tolerant to drought and
salt stresses
Decreased oxidative
stress sensitivity
(Chen et al.
et al. 2006)
Oxidative Stress in Plants and Its Management
might not be enough to confer resistance to the
whole ROS pathway which may be emanating
from multiple stressors. Genetic engineering to
develop transgenic crops with gene stacking of
different classes of ROS-scavenging enzymes
and their isoforms may also be used to obtain
synergistic and diversified tolerance to multiple
environmental stresses. Similarly, mutants with
enhanced tolerance to various stresses are also
the answer to the growing demand of developing crops to withstand harsh environmental
conditions. Therefore, plants with the ability to
control or alleviate ROS levels are the need of
the hour and answer to the future to enhance food
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