71
PHYSIOLOGICAL AND MOLECULAR ASPECTS OF
MECHANISMS INVOLVED IN PLANT RESPONSE TO
SALT STRESS
Xiaoli Tang2 and Hongbo Shao1
1
Jiangsu Key Laboratory for Bioresources of Saline Soils; Provincial Key Laboratory of Agrobiology, Institute of Agro-Biotechnology,
Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
2
Sericultural Research Institute of Shandong, Shandong Academy of Agricultural Sciences, Yantai 264002, China
71.1 INTRODUCTION
Globally, soil salinity is becoming an increasing threaten to
plant growth [1, 2]. According to FAO, at least 800 million
hectares (ha) of land are subjected to salinity [3], accounting
for as much as 6% of the world’s total land area. Although
some of the salt-affected influence is the result of natural
causes, most is derived from the degraded cultivated agri-
cultural land [4, 5]. At present the world’s cultivated land
affected by salinity has achieved 20% [6]. Currently, food
supply is basically sufficient, but approximately 800 million
people are undernourished [7]. It has been reported that food
production must increase to 150% to meet the constantly
growing population by 2050 [3,8]. The amount of cultivated
agricultural land is narrowed by the increasingly serious
salinization, and there is an increasing demand for food with
the increase in population. To meet these challenges, breed-
ing crops which are able to survive abiotic stress, and to
maximize performance under unfavorable conditions seem
to be the major topics for research [9].
Generally, the so-called saline soil has a high concen-
tration of soluble salts. Soils are regarded as saline if
the soil solution electrical conductivity (EC) values reach
≥4 dS/m [10]. The solution concentration is equivalent to
40 mM NaCl, generating an osmotic pressure of approx-
imately 0.2 MPa and significantly reducing the yields of
most cereal crops [4]. However, the deleterious effects vary
Encyclopedia of Biocolloid and Biointerface Science, Volume 2, First Edition. Edited by Hiroyuki Ohshima.
© 2016 John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc.
870
according to several related factors, including climatic con-
ditions, plant species, and soil regime. For instance, rice is
the most sensitive species among the grain crops, while bar-
ley displays a relatively pronounced resistance [11,12]. High
salinity can threaten plant health by imposing two general
types of stress: hyperosmotic stress and hyperionic stress
[13]. On the basis of their capacity to grow in high-salinity
soil, plants are classified into two types: glycophytes and
halophytes [14]. Some of the halophytes have the ability
to exclude salts from their roots and shoots, some are able
to endure high-concentration salt, and others adopt mea-
sures such as ion compartmentalization, synthesis of com-
patible solute, and osmotic adjustment [15]. Yet almost all
the crops are glycophytes, thus two key measures (produc-
ing salt-tolerant lines/cultivars through conventional breed-
ing or genetic engineering) to overcome this challlenge have
been put forward for a long time [16]. Growing halophytes
and salt-tolerant crops on saline soil is regarded as the
biotic approach, which is similar to the concept of biosaline
agriculture [17–19]. As is well known, other than ani-
mals, plants maintain a sessile lifestyle subjected to vari-
ous types of environmental stress [20]. Modern-day plants
are all the products of primal living, experienced eons of
evolution with abiotic and biotic changes. Thus they have
acquired various adaptive mechanisms to optimize growth
and development under stress [21]. Sodium chloride is the
most common and widespread salt in soil, so the evolved

mechanisms of plants regulate its accumulation and distri-
bution [22a]. For glycophytes, high-concentration salts can
produce ionic stress, osmotic stress, and secondary stress
[23]. In order to guarantee survival under such detrimental
circumstances, plants have evolved a series of biochemi-
cal and molecular processes to acclimatize themselves to
the environment [24–27]. The specific biochemical strat-
egy consists in (1) ion regulation and compartmentalization,
(2) induced biosynthesis of compatible solutes, (3) induction
of antioxidant enzymes, (4) induction of plant hormones,
and (5) changes in the photosynthetic pathway [28]. The
molecular mechanism includes (1) the SOS (salt overly sen-
sitive) pathway for ion homeostasis, (2) the protein kinase
pathway for stress signaling, (3) the phytohormone signaling
pathway under high salt stress [23], and (4) the associated
genes encoding salt stress proteins (e.g., genes for photo-
synthetic enzymes, for synthesis of compatible solutes, for
vacuolar sequestering enzymes, and for radical-scavenging
enzymes) [29].
In recent years, tremendous advances have been achieved
in salt stress studies. Plant breeders have fostered some salt-
tolerant lines of crops by conventional breeding; moreover,
a transgenic approach is employed to improve the crop salt
tolerance, and a number of transgenic lines have been con-
firmed effective under control conditions [16]. Metabolomics
is becoming a tool to help researchers understand the cellu-
lar mechanism of abiotic stress and is also a viable option
for the biotechnological improvement of halophytes [30].
Small noncoding RNAs, mainly microRNAs and siRNAs
(short interfering RNAs), can regulate gene expression by
silencing of the genes [31]. MiR393 has been reported to be
strongly upregulated by drought and high-salinity treatment
[32, 33]. In the most recent study, ribosomal RNA methy-
lation was discovered to response to abiotic stress [34]. In
addition, the mitogen-activated protein kinase (MAPK) sig-
naling pathways, which are involved in stress response, are
highly conserved and important regulating systems in plants
[35, 36].
Reviews on salinity responses began to appear three
decades ago, and new reports have appeared continuously
[1,4,13,14,28,37]. The molecular, cellular, and holistic mech-
anisms of plant salt tolerance have been discussed in detail
[4]. One team of researchers chose to stand at the point of
uptake and transport of ions to review the concrete mech-
anisms of salt tolerance [15]. Two investigators described
how plants manage to control ion homeostasis by sensing,
transduction, and responding to salt stress signaling [13].
Thanks to the rapid development of life science, our under-
standing of salinity tolerance in both physiological and
molecular fields has experienced a qualitative leap. In this
chapter we will focus on the molecular, cellular, and physio-
logical mechanisms of salt tolerance in detail, especially the
latest findings in this sphere.
GROWTH AND PHOTOSYNTHESIS 871
71.2 GROWTH AND PHOTOSYNTHESIS
Environmental stress can trigger various plant responses
ranging from gene expression to metabolism, and all the
way to growth rate and productivity [38]. Salinity, which
is the most common and comprehensive negative influence,
can lead to apparent stunting of plant growth [39, 40]. From
another perspective, slower growth is an available measure
for ensuring plant survival under stress [1]. In other words,
adverse environments affect the plant, and the plant takes the
necessary measures to accommodate it. Actually, all physio-
logical functions or activities are adaptive strategies for plants
under salt stress. Research on Arabidopsis revealed a link
between stress and cell division, illustrating the mechanism
at the molecular level [41]. Cyclin-dependent protein kinase
inhibitor (ICK1), which is induced by abscisic acid (ABA),
can reduce the activities of cyclin-dependent protein kinase
to restrain cell division, and ABA is a central plant hormone
under abiotic stress, involved in cellular signaling, regulation
of plant growth, and stomatal conductance [37,42]. Yet stud-
ies on barley displayed that ABA concentration increased
transiently under salt stress and returned to normal after 24
h, with leaf growth rate reduced [43]. More recent research
shows that it is a Asp-Glu-Leu-Leu-Ala (DELLA) protein,
which is a common negative factor in plant growth and a key
component in gibberellic acid (GA) signal transduction that
integrates signals from hormones and abiotic stress to plant
growth [44].
The accumulated Na+ within plants also can produce
ionic toxicity. With only a few exceptions, the glycophytes,
especially a large proportion of crops, cannot tolerate Na+
concentration at ≥50 mM [4]. The excess salt can inhibit
enzyme activity and lead to death to leaves [22a]. Or salt may
build up in the chloroplast exerting a toxic effect on photo-
synthetic processes and photosynthetic components directly
[4]. Mitogen-activated protein kinase 6 (MPK6) has been
demonstrated to play an important role in sodium detoxifica-
tion through phosphorylation of the Na+ /H+ antiporters and
inducing the efflux of sodium [42].
Biomass is only a broad and morphological parameter,
while photosynthesis is one of the most direct and conclu-
sive factors in determining plant growth and crop yields.
Photosynthetic rate would decrease if any part of its process
was affected [27]. For instance, stress can reduce stomatal
and mesophyll conductance and decrease CO2 availability,
ultimately lowering photosynthesis [42]. Carbon fixation
can be destroyed by salt stress directly; for example, this
can occur in ribulose-1,5-bisphosphate (RuBP) carboxy-
lase/oxygenase (Rubisco) activity, which is the key enzyme
in photosynthesis [40,45,46]. Gas exchange and chlorophyll
a fluorescence are used to monitor photosynthesis to reflect
the disadvantageous influence of salt stress [47]. In order
to resist salt stress, some plants choose to change the
872 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
photosynthetic pathway to cope with this problem [28]. The
plant Mesembryanthemum crystallinum opted to transform
the C3 pathway to crassulacean acid metabolism (CAM)
to reduce water loss [48]. The halophytic plant Atriplex
lentiformis is able to shift from C3 to C4 to combat salt
stress [49]. Some transgenic C3 plants displayed higher pho-
tosynthetic efficiency and better growth characteristics [50].
Moreover, salt stress can weaken photosynthesis indirectly
by reducing chlorophyll and total carotenoid content. It was
reported that the contents of total chlorophyll and carotene
were depleted by NaCl stress in leaves of tomato and B.
parviflora [51, 52]. Overall, salinity is accompanied by a
significant reduction in photosynthesis.
71.3 OSMOTIC STRESS EFFECTS AND
TOLERANCE
As is mentioned above, there are two aspects of salt
tolerance: osmotic stress and ionic stress. Osmotic stress is
not only confined to drought but is also a result of salinity.
The abundance of ions in saline soil lowers the flow of water,
inhibiting water uptake or even causing loss of intracellular
water [27]. In such cases, to resist these effects, the plant
accumulates many metabolites, which are usually called
compatible solutes, to increase its osmotic tolerance [13].
These compatible solutes include sugars (fructose, sucrose,
and glucose), complex sugars (trehalose, raffinose, and
fructans), quaternary amino acid derivatives, tertiary amines,
and sulfonium compounds [4]. They are able to not only
counteract the ion load but also balance the osmotic potential
of Na+ and Cl− that are sequestered into the vacuole [53].
Among the compatible solutes, proline (Pro) and glycine
betaine (GB) are the most common and efficient. In 1977, a
research team reported that Pro or GB is able to accumulate
at high concentration, producing as much as 0.1 MPa osmotic
pressure [14]. With the continuing in-depth research, their
vital functions in salt stress are becoming increasingly
clear.
Pro is able to act as molecular chaperone to stabilize the
protein conformation, buffer cytosolic pH, and balance cell
redox conditions [54]. Under stress, the accumulation of Pro
is due to increased biosynthesis and decreased degradation. In
leaves of two rice cultivars with different salinity tolerance,
the accumulative rate of proline is quicker in the tolerant
line [55]. Research on sorghum also illustrated that the pro-
line concentration is at a higher level when subjected to salt
stress [56]. It is now known that there are two pathways and
three enzymes involved in the synthesis of Pro [57]. For the
three synthetic enzymes [pyrroline-5-carboxylate synthase
and reductase (P5CS, P5CR) and ord-𝛿-aminotransferase
(OAT)], P5CS is the rate-limiting enzyme and is adjusted
by feedback and transcriptional regulation [58, 59]. In
Arabidopsis the signaling pathway for the induction of
P5CS1 expression during salt stress depends on phospholi-
pase C (PLC) and ABA-responsive (ABRE) element [60,61].
Identifciation of the molecular mechanism in Pro metabolism
has been accompanied by progress in transgenic engineering.
The first transgenic plant with accumulated Pro was acquired
in 1995 [62]. In Arabidopsis, overexpression P5CS antisense
or the insertional mutant of this gene can reduce the salt toler-
ance of transgenic plants [63,64]. Meanwhile, we may lessen
the degradation of Pro to maintain its concentration, so the
key enzyme in degradation, proline dehydrogenase (PDH),
is also manipulated. However, in PDH antisense, lines with
higher stress tolerance have emerged at times but not always
[63,65].
Glycine betaine (GB) is synthesized and accumulated
under a variety of abiotic stress and acts as an osmolyte
to protect PSII under salinity [66]. It can also protect the
integrity of membrane and the activity of enzymes against
osmotic stress [67]. Generally, high-concentration salt is able
to increase GB concentration in many crop plants, such as
sugarbeet, spinach, barley, wheat, and sorghum [68–70]. In
view of its powerful features, transgenic engineering was
also employed to operate GB concentration. Transgenic Ara-
bidopsis expressing N-methyltransferase gene, which is one
of the three key enzymes in GB synthesis, showed improved
seed yield compared to the control under salt stress [71]. Sim-
ilarly, overexpression of galactinol peroxidase 2 (GOLS2),
a GB synthase, enhanced tolerance to high salinity in
Arabidopsis [72].
In fact, there are many other compatible solutes. For exam-
ple, in Arabidopsis, overexpression of mannose-6-phosphate
reductase was reported to increase growth and photosynthesis
in saline treatment [73]. Some plants that are able to tolerate
Na+ at high levels, such as barley, tend to adapt and main-
tain turgor in the face of high soil salinities by Na+ directly.
In addition, some plants tend to accumulate carbohydrates
such as sugars and starch to cope with salt stress [52]. In
conclusion, to survive salt stress successfully, plants have
to accumulate high concentrations of compatible solutes to
maintain low water potential in cells.
71.4 ION TOXICITY AND ION HOMEOSTASIS
Because of their similarity in physicochemical properties,
Na+ competes with K+ to bind to the active site of the
enzymes, causing the inactivation or degeneration of the
enzymes and the disorder of protein synthesis and ribosome
function [4]. The toxic position of Na+ is mainly in the leaf
blade, since Na+ in the transpiration stream is deposited
here or in the roots [22b]. One study indicated that the func-
tions of chloroplast were disturbed when K+ was replaced by
Na+ , resulting in uncontrolled water loss [74]. Although Cl−

is a necessary micronutrient for cells in regulating enzyme
activity, maintaining membrane protein and pH gradients, it
is toxic to cells at high levels [75, 76]. Accumulated Na+ in
shoots is associated with a decrease in stomatal conductance,
while Cl− in high concentration can damage chloropyll and
inhibit photosystem II (PS II) [77]. More seriously, the toxic
effects of Na+ and Cl− have a cumulative effect. Hence, bal-
ancing intracellular ion concentrations by maintaining high
K+ and low Na+ concentration in the cytosol are crucial for
plants [27].
Fortunately, during the lengthy evolution, most plants
have acquired capabilities to regulate ions accumulation and
to uptake ions selectively. Plants can exclude the toxic excess
Na+ ions from cytosol [78], and almost all the plants are
able to take up water and exclude Na+ and Cl− from soil
effectively [22a]. Some plants, especially halophytes, pos-
sess succulent leaves and stems to dilute the concentration
of the toxic ions; others evolve salt glands or bladders to
secret excess ions [27]. Studies in wheat and wild soybean
with better salt tolerance demonstrated that the Na+ con-
centration in shoots is maintained at lower levels by with-
holding it in roots [79, 80]. In other words, the abilities to
exclude Na+ from the cytoplasm and to accumulate Na+ in
vacuoles efficiently are the most important means of main-
taining ion homeostasis in cells [81]. By either exclusion by
roots or compartmentalization into vacuoles, the transport of
ions is mediated by H+ -ATPase, ion channels, and cotrans-
porters in plants. The plasma membrane Na+ /H+ antiporter
SOS1 and the tonoplast membrane antiporters vacuolar
Na+ /H + antiporter (NHX) are the most important trans-
porters in salt stress and have been investigated extensively
[37].
Salinity exposure triggers complicated signaling events,
so the means by which stresses are sensed and transported by
salt stress signaling provides us with a clue to understand the
regulation mechanism of plants. The SOS signaling pathway
has been identified in earlier studies as consisting of three
key components: SOS3, SOS2, and SOS1. SOS3 is a Ca2+
sensor [82]. SOS2 is a serine/threonine protein kinase [83].
SOS3 can sense the perturbation of Ca2+ levels in cytoplast
caused by salt stress and then bind to the SOS2. Then the
SOS3/SOS2 complex phosphorylates and activates SOS1;
hence the activated SOS1 has the ability to export excess
ions and contribute to Na+ ion homeostasis [82–84]. SOS1
was also discovered to be the downstream target of MPK6
by GST pulldown assay [85]. Moreover, during salt stress
the phosphorylation degree of SOS1 increases [42]. Many
other studies have stated that the components of the signaling
pathway may be regulated by salt stress directly or influence
other signaling pathways of the stress to affect responses
indirectly [86–88].
The NHXs are vacuolar Na+ /H+ antiporters. In one
review, NHXs were demonstrated to participate in cell
ION TOXICITY AND ION HOMEOSTASIS 873
expansion, cell volume regulation, ion homeostasis, osmotic
adjustment, pH regulation, protein processing, and other pro-
cesses [2]. In genetic engineering, the hypersensitive pheno-
type of sos1 demonstrated powerfully the key position of SOS
signaling pathway in salt stress. Compared to control leaves,
the H+ -ATPase in tonoplast vesicles increased twofold in
salt-treated leaves [89]. Overexpression of NHX may reduce
cytosolic Na+ concentration and improve salt tolerance by
efficient sequestration [90]. Its overexpression confers salt
tolerance to a wide range of plants [91]. In Table 71.1, trans-
genic plants for different ion transporters with enhanced ion
homeostasis are listed for reference.
In addition, the HKT family also plays vital functions
in maintaining ions homeostasis. The HKT proteins act as
Na+ /K+ symporters and Na+ -selective transporters, involved
in balancing of Na+ and K+ . More recently, AtHKT1 was
demonstrated to take charge of the resorption of Na+ from
xylem to reduce the amount of Na+ reaching the shoot in
Arabidopsis [112]. In durum wheat, TmHKT1 is correlated
with Na+ exclusion and a high K+ /Na+ rate in leaves [113]. In
rice, OsHKT1 appears to have the same function as AtHKT1
[114], yet much more work is needed to clarify the multiple
functions of the gene family.
Recently, maintaining intracellular high cytosolic K+ /Na+
ratio has been accepted as the key determinant in salin-
ity tolerance [4]. K+ possesses a significant role in activat-
ing enzymes, regulating osmotic pressure, regulating stoma
movement, and balancing turgor [115]. In wheat cells, the
contents of K+ and Na+ are kept at 150 mM and 30 mM,
respectively, so the K+ /Na+ ratio is approximately 5 [116].
Indeed, increasingly reports show that it should be the cytoso-
lic K+ /Na+ ratio that determine the plant salt tolerance.
Two other authors proposed that the low level of KNO3
could alleviate NaCl-induced stress [117]. Another group
further claimed that NaCl stress symptoms can be allevi-
ated by simultaneously applied KNO3 and that the opti-
mal K+ /Na+ ratio should be 100:16 for both salt-tolerant
and salt-sensitive cultivar [118]. Similarly, overexpression of
LeENH1 (a tomato enhancer of SOS3-1) in tobacco enhanced
salinity tolerance by excluding Na+ from cytosol and retained
high K+ levels in the cytosol [119]. Studies on NHXs also
attest to this point. More recently, mineral analysis of the
transgenic plants with overexpressed NHXs seems to indi-
cate that salt resistance is provided by a high K+ /Na+ ratio
through K+ retention rather than Na+ exclusion [120]. In
Arabidopsis, the phenotype of sos mutants may be allevi-
ated by an exogenous supply of K+ [37]. Compared to Ara-
bidopsis, the Thellungiella species (see Table 71.1) possess
stronger ability to adapt to saline soil. One reason is that the
cytosolic K+ concentration in Thellungiella is higher. One
group claimed that the transgenic tomato with high resis-
tance depended on cytosolic K+ homeostasis rather than on
vacuolar Na+ accumulation [121].
874 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS

TABLE 71.1 Improving Plant Salt Tolerance by Bioengineering Ion Homeostasis

Donor Acceptor Gene function Elevated character Ref.
+ + + +
Vacuolar Na /H A. thaliana Wheat Na /H antiporters in Biomass production, grain 92
Antiporter AtNHX1 tonoplast, exchange Na+ output, and leaf K+
or Li+ for H+ accumulation
Vacuolar Na+ /H+ A. thaliana Tall fescue Na+ /H+ antiporters in Activity of vacuolar 93
antiporter AtNHX1 tonoplast, exchange Na+ Na+ /H+ antiporter
or Li+ for H+
Vacuolar Na+ /H+ A. thaliana Tall fescue Na+ /H+ antiporters in Better growth at 200 mM 94
antiporter AtNHX1 tonoplast, exchange Na+ NaCl
or Li+ for H+
Vacuolar Na+ /H+ Pennisetum Rice Na+ /H+ antiporters in Advanced root system 95
antiporter PgNHX1 glaucum tonoplast, exchange Na+
or Li+ for H+
Vacuolar Na+ /H+ Rice Perennial Na+ /H+ antiporters in Elevated concentration of 96
antiporter OsNHX1 ryegrass tonoplast, exchange Na+ Na+ , K+ , and proline
or Li+ for H+
Vacuolar Na+ /H+ Alfalfa A. thaliana Na+ /H+ antiporters in Increased osmotic 97
antiporter MsNHX1 tonoplast, exchange Na+ adjustment
or Li+ for H+
Vacuolar Na+ /H+ Aeluropus Tobacco Na+ /H+ antiporters in A relatively high K+ /Na+ 98
antiporter AlNHXI littoralis tonoplast, exchange Na+ ratio in leaves and roots
or Li+ for H+
Vacuolar H+ A. thaliana Alfalfa Na+ /H+ antiporters in Increased content of Na+ , 99
pyrophosphatase AVP1 tonoplast, exchange Na+ K+ , and Ca2+ in leaves
or Li+ for H+ and roots
Vacuolar Na+ /H+ A. thaliana Kiwifruit Na+ /H+ antiporters in Improved salt tolerance 94
antiporter AtNHX1 tonoplast, exchange Na+
or Li+ for H+
Vacuolar Na+ /H+ Salsola soda Alfalfa Na+ /H+ antiporters in Growth in high 100a
antiporter SsNHX1 tonoplast, exchange Na+ concentrations of NaCl
or Li+ for H+ over 50 days
Vacuolar Na+ /H+ Malus Apple Na+ /H+ antiporters, A relatively high K+ /Na+ 100b
antiporter MdNHX1 exchange Na+ or Li+ ratio in leaves
for H+
Vacuolar Na+ /H+ A. thaliana Groundnut Na+ /H+ antiporters in Resistant to high 101
antiporter AtNHX1 tonoplast, exchange Na+ concentration of salt
or Li+ for H+
Vacuolar Na+ /H+ Aopiptanthus A. thaliana Na+ /H+ antiporters in Lower Na+ content in 102
antiporter NHX1 mongolicus tonoplast, exchange Na+ leaves
or Li+ for H+
Plasma membrane Na+ /H+ Yeast Rice Na+ /H+ antiporters in Enhanced net 103
antiporter sodium 2 plasma membrane, photosynthetic rate,
(SOD2) exchange Na+ or Li+ for higher K+ , lower Na+
H+
H+ -pyrophosphatase T. halophila Tobacco Pumping H+ from the Greater dry weight at 104
(PPase) gene TsVP cytoplasm into vacuoles 300 mM NaCl
to form the pH gradient
H+ -pyrophosphatase T. halophila Cotton Pumping H+ from the Accumulating more Na+ , 105
(PPase) gene TsVP cytoplasm into vacuoles K+, Ca2+ , Cl2− and
to form the pH gradient soluble sugars in their
root and leaf tissues
H+ -pyrophosphatase A. thaliana Alfalfa Pumping H+ from the Accumulating more Na+ , 106
(PPase) gene AVP1 cytoplasm into vacuoles K+, and Ca2+ in leaves
to form the pH gradient and roots
H+-pyrophosphatase A. thaliana Cotton Pumping H+ from the More vigorous growth in 107
(PPase) gene AVP1 cytoplasm into vacuoles the presence of 200 mM
to form the pH gradient NaCl
 OXIDATIVE STRESS AND ANTIOXIDANT DEFENSE RESPONSES 875

TABLE 71.1 (Continued)

Donor Acceptor Gene function Elevated character Ref.
+ + + + +
Plasma membrane Na /H A. thaliana A. thaliana Na /H antiporters in Accumulating less Na in 108
antiporter SOS1 plasma membrane, the xylem transpirational
exchange Na+ or Li+ for stream and in the shoot
H+
Plasma membrane Na+ /H+ Yeast A. thaliana Na+ /H+ antiporters in Accumulating less Na+ and 109
antiporter sodium 2 plasma membrane, more K+ in the symplast
(SOD2) exchange Na+ or Li+ for
H+
Plasma membrane Na+ /H+ A. thaliana A. thaliana Na+ /H+ antiporters in Increased salt tolerance 91
antiporter SOS plasma membrane,
exchange Na+ or Li+ for
H+
Plasma membrane Na+ /H+ Tomato Tomato Na+ /H+ antiporters in Active loading of Na+ into 110
antiporter SISOS plasma membrane, the xylem, and Na+ and
exchange Na+ or Li+ for K+
H+ compartmentalization
Plasma membrane Na+ /H+ A. thaliana Tall fescue Na+ /H+ antiporters in Superior growth and 111
antiporter SOS1, SOS2, plasma membrane, accumulated less Na+
SOS3 exchange Na+ or Li+ for and more K+ in roots
H+ after 350 mM NaCl
treatment

71.5 OXIDATIVE STRESS AND ANTIOXIDANT
DEFENSE RESPONSES
Besides osmotic stress and ion toxicity, salinity can also
induce the generation of reactive oxygen species (ROS) and
lead to oxidative stress. ROS derive from the excitation of
O2 including singlet oxygen (1 O2 ), superoxide anion (O2 − ),
hydrogen peroxide (H2 O2 ), and hydroxyl radical (OH⋅),
respectively [27]. Unlike atmospheric oxygen, ROS are able
to oxidize the various cellular components without unrestric-
tion, leading to the oxidative destruction of plant cells [122].
Actually, ROS are the common byproducts of the metabolic
pathways such as photosynthetic electron transport, respi-
ration, and photorespiration processes [123]. For example,
salt stress limits the supply of CO2 , causing overreduction
of the photosynthetic electron transport chain and a vast pro-
duction of ROS [13]. The overabundant ROS can oxidize
cellular components, hinder metabolic activities, and affect
organelle integrity [124]. The destructive effect of ROS is the
lipid peroxidation estimated by the content of malonyldialde-
hyde (MDA) [125]. Generally, under normal conditions, the
production and eliminate of ROS are in an equilibrium state
[26]. However, under salt stress conditions, the generation
rate of ROS overwhelms the scavenging of the antioxidant
system, and then oxidative damage occurs, leading to oxi-
dation to lipids, proteins, and nucleic acids. This occcurs
precisely because these biomacromolecules are components
of the plasma membrane; thus the membrane system is the
main subject of the ROS [27].
In higher plants, the ROS removal system includes ROS-
scavenging antioxidant enzymes and small nonenzymatic
molecules such as ascorbate, glutathione, flavonoids, antho-
cyanines, and carotenoids [13]. The nonenzymatic molecules
are able to donate electrons or hydrogen to scavenge free
radicals [26]. The antioxidant enzyme system consists of
superoxide dismutase (SOD), peroxidase (POD), ascorbate
peroxidase (APX), glutathione peroxidases (GPX), glu-
tathione reductase (GR), catalase (CAT), and the ascorbate–
glutathione cycle [16]. The SOD, APX, and GR (glutathione
reductase) are reported to scavenge H2 O2 in chloroplasts
and mitochondria, and the others are believed to be capable
of removing H2 O2 , neutralizing or scavenging free radicals
[126]. Among them, SOD and CAT are the most efficient
enzymes. Under salt stress, the second metabolites increased
more quickly than did the antioxidant enzyme activities in
Swertia chirata [127]. The levels and contents of superox-
ide and hydrogen peroxide can be decreased by most of
the antioxidant obviously, so in many species the antioxi-
dant capacity is associated with salinity tolerance tightly. For
example, the antioxidant enzyme activities of SOD, APX,
and GR increased 10–18 times after salt stress in P. pop-
ularis [128]. The correlation between antioxidant capacity
and salinity tolerance is being discovered in an increasing
number of species, containing cotton, citrus, foxtail millet,
purslane, sugarbeet, pea, and plantago [13].
During the last few decades, engineering the genes of
some antioxidant enzymes has been employed to ameliorate
plants exposed to stress. By observing the changes in the
876 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
expression level of related genes, researchers were able to
produce transgenic plants to probe the effects. Finally, in
the transgenic plants, overexpression antioxidant enzymes
such as SOD, CAT, and APX displayed elevated tolerance to
oxidative stress [13]. The transgenic Arabidopsis and Lycop-
ersicon esculentum possess a significant increase in salt tol-
erance with the overexpression of a Mn-SOD [129, 130].
Details are shown in Table 71.2. More importantly, most
of the transgenic plants with some overexpressed antioxi-
dant enzymes acquire an elevated tolerance to almost all
abiotic stresses instead of a specific stress. In our opinion,
the possible reason for this is that the oxidative stress is the
result of almost all the abiotic stresses, so the enhancement
of the antioxidative capacity is able to boost resistance in
general. Although the transgenic plants with overexpressed
antioxidant enzymes acquire enhanced tolerance, there exist
inevitable contradictions. The Arabidopsis mutants with loss
of either or both cytosolic and chloroplastic APX show
enhanced tolerance on the contrary [131]. Likewise, there
is a decline in CAT activity in Anabaena doliolum under
NaCl stress [132]. In Glycyrrhiza uralensis seedlings, CAT
activity is also decreased by salt and drought stress [133]. In
conclusion, the ROS pathway is plastic and redundant, more
strategies and principles remain to be seen.
Reactive oxygen species play a dual role in plants. Super-
fluous ROS are detrimental to plant cells, yet moderate ROS
components are necessary, playing important roles in signal-
ing transduction and cell homeostasis [85]. In fact, upreg-
ulation of the expression levels of enzyme genes or the
enhancement of their enzymatic activities results from cell
signaling. Ahead of their detoxification, the genes will have
initiated a series of signaling in cells. MAK3 and MAK6 can
be activated by the elevated content of ROS [150], and the
activated MAK3 and MAK6 were relocated in the nucleus
to strengthen or weaken gene expression, triggering plant
responses to ROS. Nevertheless, the MAPK phosphatase 2
(MKP2), which is induced by oxidative stress, is able to
dephosphorylate MPK3 and MPK6 to promote oxidative
stress tolerance [85]. Therefore, the signal regulatory path-
ways are intricate.
71.6 PHYTOHORMONE IN SALT STRESS
Plant hormones partipate in almost all plant contents and
processes, including different positions, different tissues, and
different developmental stages. ABA is the foremost one and
is induced by various obvious types of stress. It is able to reg-
ulate the adaption of plants to stresses such as cold, drought,
salinity, pathogen attacks, injury, and oxidative stress [85].
It has been proved responsible for the change in salt-stress-
induced genes back in the 1990s [151]. Its powerful functions
in salt stress are reflected in its involvement in the photo-
synthesis and growth, osmotic tolerance, ion homeostasis,
and antioxidant defense responses that we mentioned above.
Two decades ago, Popova and colleagues proposed that the
inhibitory effect of salt stress on growth and photosynthesis
can be alleviated by ABA [152]. Moreover, ABA partici-
pates in regulating stress-related gene expression. In ABA-
deficient mutants, P5CS, which is the rate-limiting enzyme
of the synthesis of Pro, is reduced or completely blocked
[153]. For ion homeostasis, ABA has the ability to reduce
anion channels to reduce Cl− transfer in saline conditions
[154]. The type 2C protein, phosphatase ABI2, which acts as
a vital component in ABA signaling, is able to bind to SOS2
directly and dephosphorylate it [155]. The involvement of
ABA in antioxidant defense responses is the induction of
antioxidant defense. During the ABA-induced antioxidant
defense, hydrogen peroxide (H2 O2 ), nitric oxide (NO), and
mitogen-activated protein kinase (MAPK) are the major com-
ponents [156–160]. Zhang and coworkers reported that the
zinc finger protein ZFP182 also mediated the ABA-induced
antioxidant defense [161]. In rice, ABA can significantly
induce the expression and activity of OsCAT to control the
accumulation of H2 O2 under stress [159]. More recently,
ABA was discovered to induce the production of primary
and secondary metabolites, the photosynthetic capacity, the
antioxidant ability, and the antioxidant enzymes [162].
In recent years, phytohormone—salicylic acid (SA) was
repeatedly reported to participate in salt stress responses
as well [42]. The exogenous SA can ameliorate toxicity
stress induced by salt stress, and its vital function under salt
stress manifests in its enhancement on antioxidant system.
In periwinkle, nonenzymatic and enzymatic antioxidants can
be induced by exogenous SA [163]. In mungbean, SA alle-
viates decreases in photosynthesis by means of enhancing
antioxidant metabolism [164]. Furthermore, SA can lessen
salt stress by maintaining ion homeostasis. It is well known
that ion homeostasis, especially the optimum K+ /Na+ ratio,
is crucial for plants under salt stress. Discoveries achieved
by noninvasive microelectrode ion flux estimation (MIFE)
technique [165] revealed that SA pretreatment can enhance
K+ retention, increase H+ -ATPase activity, and reduce K+
loss under salt stress [166]. Generally speaking, the potential
mechanism of SA to enhance salt tolerance lies in improving
photosynthesis, enhancing antioxidant protection, and main-
taining optimum K+ /Na+ ratio [164,166,167].
71.7 CONCLUSIONS
Salt stress is one of the most common types of abiotic
stress. Its negative influence on plants is comprehensive.
High-concentration salt can interfere with normal growth and
development tremendously and even lead to death to plant.
Fortunately, plants have acquired the abilities to ameliorate
these adverse effects by physiological, molecular, and genetic
by means of regulation. Plants reduce their growth rate to
 CONCLUSIONS 877

TABLE 71.2 Genetic Transformation of Antioxidant Enzymes for Enhancing Salt Tolerance
Gene symbol Donor Acceptor Gene functions Elevated character Ref.
Ascorbate peroxidase A. thaliana Tobacco Primary H2 O2 -scavenging Enhanced tolerance to active 134
(APX) enzyme oxygen-generating paraquat
and sodium sulfite
Superoxide dismutase A. thaliana A. thaliana A critical enzyme for eliminating Lower content of 129
(SOD) reactive oxygen species (ROS) malondialdehyde (MDA) and
in plant cells better growth than control
under salt stress
Ascorbate peroxidase Pea Tobacco Primary H2 O2 -scavenging Higher germination rate and 135
(APX) enzyme minimized leaf damage under
salt stress
Dehydroascorbate Rice A. thaliana A critical enzyme for ascorbate Enhanced resistance to salt stress 136
reductase (DHAR) recycling
Ascorbate peroxidase Rice A. thaliana Primary H2 O2 -scavenging Longer root length and higher 137
(APX) enzyme total chlorophyll content
Ascorbate peroxidase Tobacco Tobacco Primary H2 O2 -scavenging More resistant to 138
(APX) Superoxide enzyme; A critical enzyme paraquat-induced stress and
dismutase (SOD) and eliminating reactive oxygen enhanced tolerance to NaCI
DHAR species (ROS) in plant cells; a
critical enzyme for ascorbate
recycling
Monodehydroascorbate A. thaliana Tobacco Crucial for ascorbate (AsA) Higher net photosynthesis rates 139
reductase (MDAR) regeneration and essential for and greater PS II effective
maintaining a reduced pool of quantum yield under salt stress
AsA
Catalase (CAT) Escherichia coli Tobacco Catalyzing the dismutation of Increased the resistance of the 140
H2 O2 into water and oxygen chloroplast’s translational
machinery under salt stress
Superoxide dismutase Avicennia Rice The first enzyme in the More tolerant to methyl 141
(SOD) marina enzymatic antioxidative viologen–mediated oxidative
pathway stress
Superoxide dismutase Tobacco Pepper The first enzyme in the Increased resistance to oxidative 142
(SOD) enzymatic antioxidative damage
pathway
Ascorbate peroxidase Tomato Tobacco Primary H2 O2 -scavenging Higher seed germination rate and 143
(APX) enzyme elevated stress tolerance
during postgermination
Suaeda salsa glutathione Suaeda salsa A. thaliana Involved in the reduction of most Higher photosynthesis rate and 144
S_transferase gene active oxygen radicals fresh weight
(GST) generated by stress
Monodehydroascorbate Avicennia Tobacco Crucial for ascorbate (AsA) Enhanced redox state of 145
reductase (MDAR) marina regeneration and essential for ascorbate and reduced levels
maintaining a reduced pool of of malondialdehyde
AsA
Ascorbate peroxidase P. populus Tobacco Primary H2 O2 -scavenging Resistance to methyl viologen 146
(APX) enzyme and salt stress
Ascorbate peroxidase Tobacco Tobacco Primary H2 O2 -scavenging Improved seed longevity and 147
(APX), Superoxide enzyme; the first enzyme in germination under various
dismutase (SOD) the enzymatic antioxidative types of environmental stress
pathway
Glutathione peroxidases Wheat A. thaliana Reducing H2 O2 and organic Strong tolerance to salt, H2 O2 , 148
(GPXs) hydroperoxides to water and and ABA treatment
correspondingly alcohols
Ascorbate peroxidase Plums Plums Primary H2 O2 -scavenging Higher contents of nonenzymatic 149
(APX), superoxide enzyme; the first enzyme in antioxidants glutathione and
dismutase (SOD) the enzymatic antioxidative ascorbate and lower
pathway accumulation of hydrogen
peroxide
878 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
Adaptive growth and photosynthesis rate
Synthesis and accumulation of compatible solutes
FIGURE 71.1
guarantee their survival and maintain regular photosynthesis
by regulating enzymatic activities under salt stress [1]. Fac-
ing the osmotic stress produced by salt, plants accumulate
compatible solutes actively to reduce cell water potential [4].
Different channels and transporters are activated or inhib-
ited to regulate and maintain ion homeostasis. The clarified
signaling pathways tell us the complicated regulatory mech-
anisms employed by plants under salt stress. The discovery
of the SOS signaling pathway is a milestone of the signal
pathway in salt stress [82]. The antioxidant system covering
nonenzymatic and enzymatic antioxidant systems can help
plants escape the damage due to salt stress [26]. Plant hor-
mones are the growth regulators of plants and are involved in
the processes in every regard, so salt stress is no exception.
ABA plays a pivotal role in the metabolomic, physiologi-
cal, and signaling procedures. Thus we can conclude that the
relationships between salt stress and plants are processes of
both influence and adaptation. Exploring and understanding
the regulatory mechanisms underlying salt stress can provide
us with more methods and ideas to improve plant resistance.
In view of the research and developments in molecular
biology and transgenic engineering, plants with enhanced
tolerance are generating continuously. For example, overex-
pression of the synthetic genes of Pro and GB can improve the
content of Pro and GB obviously and endow the transgenic
plants with enhanced tolerance [62,71]. Similarly, transgenic
plants with more SOS1 or NHX1 transporters are able to reg-
ulate ion transport more quickly and effectively to improve
their growth under salt stress [83, 84,91]. Increasing the
antioxidants levels through genetic engineering is widely
adopted in breeding to produce crops with enhanced salt
stress. Yet the salt tolerance trait is a multigenic property, as
salt tolerance is related to physiological, biochemical, and
SALINITY
Signal perception and transduction
Transcription factors
Regulation of gene expression
Regulation of ion content and homeostasis
Gene expression
and responses
Activation of antioxidant substance and enzyme
RESISTANCE
The general pathway under salt stress.
molecular processes, so the ability of genetic engineering to
produce salt-tolerant crops is seriously limited by these natu-
ral plant processes [37]. More energy, materials, and financial
resources are needed to invest in the research. Only in this
way can the mechanisms and principles be discovered and
corresponding ameliorative solutions be proposed. In addi-
tion, there are other factors such as LEA proteins and WRKY
and MYB transcriptional factors affecting salt tolerance of
plants, which should also arouse attention [168–170]. In the
most recent reports, the microorganism in soil is found to
be involved in phytohormonal signaling to improve plant
nutrition, photosynthesis, and biomass production, thereby
enhancing crop salt tolerance [171]. Finally, we summa-
rize our points of view and blueprint for future research in
Fig. 71.1.
ACKNOWLEDGMENTS
This work was jointly supported by the National Natural
Science Foundation of China (Grant 41171216), Jiangsu
Autonomous Innovation of Agricultural Science and Tech-
nology [CX(15)1005], National Basic Research Program of
China (2013CB430403) and Shuangchuang Talent Plan of
Jiangsu Province.
REFERENCES
[1] Zhu, J.K. (2001). Plant salt tolerance. Trends Plant Sci. 6,
66–71.
[2] Rengasamy, P. (2010). Soil processes affecting crop produc-
tion in salt-affected soils. Funct. Plant Biol. 37, 613–620.

[3] FAO (2008). FAO Land and Plant Nutrition Management
Service (http://wwwfaoorg/ ag/agl/agll/spush).
[4] Munns, R., Tester, M. (2008). Mechanisms of salinity tol-
erance. Annu. Rev. Plant Biol. 59, 651–681.
[5] Lee, G., Boerma, H., Villagarcia, M., Zhou, X., Carter, T.Jr.,
Li, Z., Gibbs, M. (2004). A major QTL conditioning salt
tolerance in S-100 soybean and descendent cultivars. Theor.
Appl. Genet. 109, 1610–1619.
[6] Rhoades, J., Loveday, J. (1990). Salinity in irrigated agri-
culture. Agronomy 30, 1089–1142.
[7] Conway, G. (1998). The doubly green revolution. Biologist
45, 85–86.
[8] Rengasamy., P (2006). World salinization with emphasis
on Australia. J. Exp. Bot. 57, 1017–1023.
[9] Abreu, I.A., Farinha, A.P., Negrão, S., Gonçalves, N., Fon-
seca, C., Rodrigues, M., Batista, R., Saibo, N.J.M., Oliveira,
M.M. (2013). Coping with abiotic stress: Proteome changes
for crop improvement. J. Proteomics 93, 145–168.
[10] George, E., Brown, J. (2008). Mechanisms of salinity tol-
erance. Annu. Rev. Plant Biol. 59, 651–681.
[11] Aslam, M., Qureshi, R., Ahmed, N. (1993). A rapid screen-
ing technique for salt tolerance in rice (Oryza sativa L.).
Plant Soil 150, 99–107.
[12] Colmer, T., Munns, R., Flowers, T. (2006). Improving salt
tolerance of wheat and barley: Future prospects. Animal
Prod. Sci. 45, 1425–1443.
[13] Türkan, I., Demiral, T. (2009). Recent developments in
understanding salinity tolerance. Environ. Exp. Bot. 67, 2–
9.
[14] Flowers, T., Troke, P., Yeo, A. (1977). The mechanism of
salt tolerance in halophytes. Ann. Rev. Plant Physiol. 28,
89–121.
[15] Flowers, T.J., Colmer, T.D. (2008). Salinity tolerance in
halophytes. New Phytol. 179, 945–963.
[16] Ashraf, M., Akram, N.A. (2009). Improving salinity toler-
ance of plants through conventional breeding and genetic
engineering: An analytical comparison. Biotechnol. Adv.
27, 744–752.
[17] Wright, M.J., Ferrari, S. (1976). Plant Adaptation to Min-
eral Stress in Problem Soils. PhD thesis, Cornell Univ.
[18] Kingsbury, R., Epstein, E. (1984). Selection for salt-
resistant spring wheat. Crop Sci. 24, 310–315.
[19] Ashraf, M., Wu, L. (1994). Breeding for salinity tolerance
in plants. Crit. Rev. Plant Sci. 13, 17–42.
[20] Sarwat, M., Ahmad, P., Nabi, G., Hu, X. (2013). Ca2+ sig-
nals: The versatile decoders of environmental cues. Crit.
Rev. Biotechnol. 33, 97–109.
[21] Xue, X.X., Shao, H.B., Ma, Y.Y., Xu, G., Sun, J.N., Guo,
D.G., Ruan, C.J. (2010). Biotechnological implications
from abscisic acid (ABA) roles in cold stress and leaf senes-
cence as an important signal for improving plant sustain-
able survival under abiotic-stressed conditions. Crit. Rev.
Biotechnol. 30, 222–230.
[22] (a) Munns, R. (2005). Genes and salt tolerance: Bringing
them together. New Phytol. 167, 645–663; (b) Munns, R.
REFERENCES 879
(2002). Comparative physiology of salt and water stress.
Plant Cell Environ. 25, 239–250.
[23] Zhu, J.K. (2002). Salt and drought stress signal transduction
in plants. Annu. Rev. Plant Biol. 5, 247–269.
[24] Dufty, A.M. Jr., Clobert, J., Møller, A.P. (2002). Hormones,
developmental plasticity and adaptation. Trends Ecol. Evo-
lut. 17(4), 190–196.
[25] Glombitza, S., Dubuis, P.-H., Thulke, O., Welzl, G., Bovet,
L., Götz, M., Affenzeller, M., Geist, B, Hehn, A., Asnaghi,
C. (2004). Crosstalk and differential response to abiotic
and biotic stressors reflected at the transcriptional level of
effector genes from secondary metabolism. Plant Mol. Biol.
54, 817–835.
[26] Jaleel, C.A., Riadh, K., Gopi, R., Manivannan, P., Inès, J.,
Al-Juburi, H.J., Zhao, C.X., Shao, H.B., Panneerselvam,
R. (2009). Antioxidant defense responses: Physiological
plasticity in higher plants under abiotic constraints. Acta
Physiol. Plant 31, 427–436.
[27] Yan, K., Shao, H.B., Shao, C.Y., Chen, P., Zhao, S.J.,
Brestic, M., Chen, X.B. (2013). Physiological adaptive
mechanisms of plants grown in saline soil and implica-
tions for sustainable saline agriculture in coastal zone. Acta
Physiol. Plant 35, 2867–2878.
[28] Parida, A.K., Das, A.B. (2005). Salt tolerance and salinity
effects on plants: A review. Ecotoxicol. Environ. Safety 60,
324–349.
[29] Winicov, I. (1998). New molecular approaches to improv-
ing salt tolerance in crop plants. Ann. Bot. 82, 703–710.
[30] Ruan, C.J., Teixeira da Silva, J.A. (2011). Metabolomics:
Creating new potentials for unraveling the mechanisms in
response to salt and drought stress and for the biotechnolog-
ical improvement of xero-halophytes. Crit. Rev. Biotechnol.
31, 153–169.
[31] Carrington, J.C., Ambros, V. (2003). Role of microRNAs
in plant and animal development. Science 301, 336–338.
[32] Dharmasiri, N., Dharmasiri, S., Estelle, M. (2005). The F-
box protein TIR1 is an auxin receptor. Nature 435, 441–445.
[33] Kepinski, S., Leyser, O. (2005). The Arabidopsis F-box
protein TIR1 is an auxin receptor. Nature 435, 446–451.
[34] Baldridge, K.C., Contreras, L.M. (2013). Functional impli-
cations of ribosomal RNA methylation in response to envi-
ronmental stress. Crit. Rev. Biochem. Mol. Biol. 30, 1–21.
[35] Colcombet, J., Hirt, H. (2008). Arabidopsis MAPKs: A
complex signalling network involved in multiple biological
processes. Biochem. J. 413, 217–226.
[36] Sinha, A.K., Jaggi, M., Raghuram, B., Tuteja, N. (2011).
Mitogen-activated protein kinase signaling in plants under
abiotic stress. Plant Signal. Behav. 6, 196–203.
[37] Zhu, J.K. (2003). Regulation of ion homeostasis under salt
stress. Curr. Opin. Plant Biol. 6, 441–445.
[38] Shao, H.B., Chu, L.Y., Jaleel, C.A., Manivannan, P., Pan-
neerselvam, R., Shao, M.A. (2009). Understanding water
deficit stress-induced changes in the basic metabolism of
higher plants - biotechnologically and sustainably improv-
ing agriculture and the ecoenvironment in arid regions of
the globe. Crit. Rev. Biotechnol. 29(2), 131–151.
880 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
[39] Gorai, M., Ennajeh, M., Khemira, H., Neffati, M. (2011).
Influence of NaCl-salinity on growth, photosynthesis, water
relations and solute accumulation in Phragmites australis.
Acta Physiol. Plant 33, 963–971.
[40] Tarchoune, I., Degl’Innocenti, E., Kaddour, R., Guidi, L.,
Lachaâl, M., Navari-Izzo, F., Ouerghi, Z. (2011). Effects
of NaCl or Na2 SO4 salinity on plant growth, ion content
and photosynthetic activity in Ocimum basilicum L. Acta
Physiol. Plant 34, 607–615.
[41] Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L.,
Fowke, L.C. (1998). ICK1, a cyclin-dependent protein
kinase inhibitor fromArabidopsis thalianainteracts with
both Cdc2a and CycD3, and its expression is induced by
abscisic acid. Plant J. 15, 501–510.
[42] Davies, W.J., Kudoyarova, G., Hartung, W. (2005). Long-
distance ABA signaling and its relation to other signaling
pathways in the detection of soil drying and the mediation
of the plant’s response to drought. J. Plant Growth Regul.
24, 285–295.
[43] Fricke, W., Akhiyarova, G., Veselov, D., Kudoyarova, G.
(2004). Rapid and tissue-specific changes in ABA and in
growth rate in response to salinity in barley leaves. J. Exp.
Bot. 55, 1115–1123.
[44] Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schout-
teten, H., Moritz, T., Van Der Straeten, D., Peng, J., Harberd,
N.P. (2006). Integration of plant responses to environmen-
tally activated phytohormonal signals. Science 311, 91–94.
[45] Brugnoli, E., Björkman, O. (1992). Growth of cotton under
continuous salinity stress: Influence on allocation pattern,
stomatal and non-stomatal components of photosynthesis
and dissipation of excess light energy. Planta 187, 335–
347.
[46] Yang, X., Liang, Z., Wen, X., Lu, C. (2008). Genetic
engineering of the biosynthesis of glycinebetaine leads to
increased tolerance of photosynthesis to salt stress in trans-
genic tobacco plants. Plant Mol. Biol. 66, 73–86.
[47] Jedmowski, C., Ashoub, A., Brüggemann, W. (2013).
Reactions of Egyptian landraces of Hordeum vulgare and
Sorghum bicolor to drought stress, evaluated by the OJIP
fluorescence transient analysis. Acta Physiol. Plant 35,
345–354.
[48] Cushman, J.C., Meyer, G., Michalowski, C.B., Schmitt,
J.M., Bohnert, H.J. (1989). Salt stress leads to differential
expression of two isogenes of PEP case during CAM induc-
tion in the common ice plant. Plant Cell 1989, 715–725.
[49] Meinzer, F.C., Zhu, J. (1999). Efficiency of C4 photosyn-
thesis in Atriplex lentiformis under salinity stress. Funct.
Plant Biol. 26, 79–86.
[50] Ruan, C.J., Shao, H.B., Teixeira da Silva, J.A. (2012). A
critical review on the improvement of photosynthetic car-
bon assimilation in C3 plants using genetic engineering.
Crit. Rev. Biotechnol. 32, 1–21.
[51] Khavari-Nejad, R., Mostofi, Y. (1998). Effects of NaCl
on photosynthetic pigments, saccharides, and chloroplast
ultrastructure in leaves of tomato cultivars. Photosynthet-
ica 35, 151–154.
[52] Parida, A., Das, A.B., Das, P. (2002). NaCl stress causes
changes in photosynthetic pigments, proteins, and other
metabolic components in the leaves of a true mangrove,
Bruguiera parviflora, in hydroponic cultures. J. Plant Biol.
45, 28–36.
[53] Wyn Jones, R., Storey, R., Leigh, R., Ahmad, N., Pollard,
A. (1977). A Hypothesis on Cytoplasmic Osmoregulation.
Regulation of Cell Membrane Activities in Plants. Wiley,
New York, pp. 121–136.
[54] Maggio, A., Miyazaki, S., Veronese, P., Fujita, T., Ibeas,
J.I., Damsz, B., Narasimhan, M.L., Hasegawa, P.M., Joly,
R.J., Bressan, R.A. (2002). Does proline accumulation play
an active role in stress-induced growth reduction? Plant J.
31, 699–712.
[55] Demiral, T., Türkan, I. (2004). Does exogenous glycine-
betaine affect antioxidative system of rice seedlings under
NaCl treatment? J. Plant Physiol. 161, 1089–1100.
[56] Yan, K., Chen, P., Shao, H.B., Zhao, S.J., Zhang, L.H.,
Zhang, L.W., Xu, G., Sun, J.N. (2012). Photosynthetic char-
acterization of Jerusalem artichoke during leaf expansion.
Acta Physiol. Plant. 34(1), 353–360.
[57] Verbruggen, N., Hermans, C. (2008). Proline accumulation
in plants: A review. Amino Acids 35, 753–759.
[58] Savouré, A., Jaoua, S., Hua, X.J., Ardiles, W., Van Mon-
tagu, M., Verbruggen, N. (1995). Isolation, characteriza-
tion, and chromosomal location of a gene encoding theΔ1-
pyrroline-5-carboxylate synthetase in Arabidopsis thaliana.
FEBS Lett. 372, 13–19.
[59] Zhang, C.S., Li, Q., Verma, D.P.S. (1995). Removal of feed-
back inhibition of D1-pyrroline-5-carboxylate synthetase,
a bifunctional enzyme catalyzing the first two steps of
proline biosynthesis in plants. J. Biol. Chem. 20491–
20496.
[60] Parre, E., Ghars, M.A., Leprince, A.-S., Thiery, L., Lefeb-
vre, D., Bordenave, M., Richard, L., Mazars, C., Abdelly,
C., Savouré, A. (2007). Calcium signaling via phospholi-
pase C is essential for proline accumulation upon ionic but
not nonionic hyperosmotic stresses in Arabidopsis. Plant
Physiol. 144, 503–512.
[61] Abrahám, E., Rigó, G., Székely, G., Nagy, R., Koncz, C.,
Szabados, L. (2003). Light-dependent induction of proline
biosynthesis by abscisic acid and salt stress is inhibited by
brassinosteroid in Arabidopsis. Plant Mol. Biol. 51, 363–
372.
[62] Kavi, K.P., Hong, Z., Miao, G., Hu, C., Verma, D. (1995).
Overexpression of D1-pyrroline-5-carboxylate synthetase
increases proline production and confers osmotolerance in
transgenic plants. Plant Physiol. 108, 1387–1394.
[63] Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y.,
Yamaguchi-Shinozaki, K., Shinozaki, K. (1999). Antisense
suppression of proline degradation improves tolerance to
freezing and salinity in Arabidopsis thaliana. FEBS Lett.
461, 205–210.
[64] Székely, G., Abraham, E., Cséplő, Á., Rigo, G., Zsig-
mond, L., Csiszar, J., Ayaydin, F., Strizhov, N., Jasik,
J., Schmelzer, E. (2008). Duplicated P5CS genes of

Arabidopsis play distinct roles in stress regulation and
developmental control of proline biosynthesis. Plant J. 53,
11–28.
[65] Mani, S., Van de Cotte, B., Van Montagu, M., Verbruggen,
N. (2002). Altered levels of proline dehydrogenase cause
hypersensitivity to proline and its analogs in Arabidopsis.
Plant Physiol. 128, 73–83.
[66] Jagendorf, A.T., Takabe, T. (2001). Inducers of glycinebe-
taine synthesis in barley. Plant Physiol. 127, 1827–1835.
[67] Mäkelä, P., Kärkkäinen, J., Somersalo, S. (2000). Effect
of glycinebetaine on chloroplast ultrastructure, chlorophyll
and protein content, and Rubisco activities in tomato grown
under drought or salinity. Biol. Plant 43, 471–475.
[68] Weimberg, R., Lerner, H., Poljakoff-Mayber, A. (1984).
Changes in growth and water-soluble solute concentrations
in Sorghum bicolor stressed with sodium and potassium
salts. Physiol. Plant 62, 472–480.
[69] Fallon, K., Phillips, R. (1989). Responses to water stress
in adapted and unadapted carrot cell suspension cultures. J.
Exp. Bot. 40, 681–687.
[70] Yang, W.J., Rich, P.J., Axtell, J.D., Wood, K.V., Bonham,
C.C., Ejeta, G., Mickelbart, M.V., Rhodes, D. (2003). Geno-
typic variation for glycinebetaine in sorghum. Crop Sci. 43,
162–169.
[71] Waditee, R., Bhuiyan, M.N.H., Rai, V., Aoki, K., Tanaka, Y.,
Hibino, T., Suzuki, S., Takano, J., Jagendorf, A.T., Takabe,
T. (2005). Genes for direct methylation of glycine provide
high levels of glycinebetaine and abiotic-stress tolerance
in Synechococcus and Arabidopsis. Proc. Natl. Acad. Sci.
USA 102, 1318–1323.
[72] Sun, Z., Qi, X., Wang, Z., Li, P., Wu, C., Zhang, H., Zhao,
Y (2013). Overexpression of TsGOLS2, a galactinol syn-
thase, in Arabidopsis thaliana enhances tolerance to high
salinity and osmotic stresses. Plant Physiol. Biochem. 69,
82–89.
[73] Sickler, C.M., Edwards, G.E., Kiirats, O., Gao, Z.,
Loescher, W. (2007). Response of mannitol-producing Ara-
bidopsis thaliana to abiotic stress. Funct. Plant Biol. 34,
382–391.
[74] Slabu, C., Zörb, C., Steffens, D., Schubert, S. (2009). Is
salt stress of faba bean (Vicia faba) caused by Na+ or Cl−
toxicity? J. Plant Nutr. Soil Sci. 172, 644–651.
[75] White, P.J., Broadley, M.R. (2001). Chloride in soils and
its uptake and movement within the plant: A review. Ann.
Bot. 88, 967–988.
[76] Xu, G., Magen, H., Tarchitzky, J., Kafkafi, U. (1999).
Advances in chloride nutrition of plants. Adv. Agron. 68,
97–150.
[77] Tavakkoli, E., Fatehi, F., Coventry, S., Rengasamy, P.,
McDonald, G.K. (2011). Additive effects of Na+ and Cl–
ions on barley growth under salinity stress. J. Exp. Bot. 62,
2189–2203.
[78] Janicka-Russak, M., Kabała, K., Wdowikowska, A.,
Kłobus, G. (2013). Modification of plasma membrane pro-
ton pumps in cucumber roots as an adaptation mechanism
to salt stress. J. Plant Physiol. 170, 915–922.
REFERENCES 881
[79] Islam, S., Malik, A., Islam, A., Colmer, T.D. (2007).
Salt tolerance in a Hordeum marinum–Triticum aestivum
amphiploid, and its parents. J. Exp. Bot. 58, 1219–1229.
[80] Luo, Q., Yu, B., Liu, Y. (2005). Differential sensitivity to
chloride and sodium ions in seedlings of glycine max and G.
soja under NaCl stress. J. Plant Physiol. 162, 1003–1012.
[81] Silva, P., Gerós, H. (2009). Regulation by salt of vacuolar
H+ -ATPase and H+ -pyrophosphatase activities and Na+ /H+
exchange. Plant Signal. Behav. 4, 718–726.
[82] Liu, J., Zhu, J.K. (1998). A calcium sensor homolog
required for plant salt tolerance. Science 280, 1943–1945.
[83] Liu, J., Ishitani, M., Halfter, U., Kim, C.S., Zhu, J.K. (2000).
The Arabidopsis thaliana SOS2 gene encodes a protein
kinase that is required for salt tolerance. Proc. Natl. Acad.
Sci. USA 97, 3730–3734.
[84] Quintero, F.J., Ohta, M., Shi, H., Zhu, J.K., Pardo, J.M.
(2002). Reconstitution in yeast of the Arabidopsis SOS
signaling pathway for Na+ homeostasis. Proc. Natl. Acad.
Sci. 99, 9061–9066.
[85] Smékalová, V., Doskočilová, A., Komis, G., Šamaj, J.
(2013). Crosstalk between secondary messengers, hor-
mones and MAPK modules during abiotic stress sig-
nalling in plants. Biotechnol. Adv. S0734-9750(13)00123-7
(doi:10.1016/j.biotechadv.2013.07.009).
[86] Shabala, L., Cuin, T.A., Newman, I.A., Shabala, S. (2005).
Salinity-induced ion flux patterns from the excised roots of
Arabidopsis sos mutants. Planta 222, 1041–1050.
[87] Mahajan, S., Tuteja, N. (2005). Cold, salinity and drought
stresses: An overview. Arch. Biochem. Biophys. 444, 139–
158.
[88] Qiu, Q.S., Guo, Y., Dietrich, M.A., Schumaker, K.S., Zhu,
J.-K. (2002). Regulation of SOS1, a plasma membrane
Na+ /H+ exchanger in Arabidopsis thaliana, by SOS2 and
SOS3. Proc. Natl. Acad. Sci. 99, 8436–8441.
[89] Qiu, N., Chen, M., Guo, J., Bao, H., Ma, X., Wang, B.
(2007). Coordinate up-regulation of V-H+ -ATPase and vac-
uolar Na+ /H+ antiporter as a response to NaCl treatment in
a C3 halophyte Suaeda salsa. Plant Sci. 172, 1218–1225.
[90] Apse, M.P., Aharon, G.S., Snedden, W.A., Blumwald, E.
(1999). Salt tolerance conferred by overexpression of a vac-
uolar Na+ /H+ antiport in Arabidopsis. Science 285(5431),
1256–1258.
[91] Yang, Q., Chen, Z.Z., Zhou, X.F., Yin, H.-B., Li, X., Xin,
X.F., Hong, X.H., Zhu, J.K., Gong, Z. (2009). Overexpres-
sion of SOS (salt overly sensitive) genes increases salt tol-
erance in transgenic Arabidopsis. Mol. Plant 2, 22–31.
[92] Xue, Z.-Y., Zhi, D.-Y., Xue, G.-P., Zhang, H., Zhao, Y.-X.,
et al. (2004). Enhanced salt tolerance of transgenic wheat
(Tritivum aestivum L.) expressing a vacuolar Na+/H+
antiporter gene with improved grain yields in saline soils
in the field and a reduced level of leaf Na+. Plant Sci. 167,
849–859.
[93] Zhao, J., Zhi, D., Xue, Z., Liu, H., Xia, G. (2007). Enhanced
salt tolerance of transgenic progeny of tall fescue (Festuca
arundinacea) expressing a vacuolar Na+ /H+ antiporter gene
from Arabidopsis. J. Plant Physiol. 164, 1377–1383.
882 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
[94] Tian, L.M.H.C., Yu, R., Liang, R.F, Li, Z.L., Zhang, L.S.,
Wang, Y.Q., Zhang, X.H., Wu, Z.Y. (2006). Overexpression
AtNHX1 confers salt-tolerance of transgenic tall fescue.
Afr. J. Biotechnol. 5, 1041–1044.
[95] Verma, D., Singla-Pareek, S.L., Rajagopal, D., Reddy,
M.K., Sopory, S.K. (2007). Functional validation of a novel
isoform of Na+/H+ antiporter from Pennisetum glaucum
for enhancing salinity tolerance in rice. J. Biosci. (Banga-
lore) 32, 621–628.
[96] Wu, Y.-Y., Chen, Q.-J., Chen, M., Chen, J., Wang, X.-C.
(2005). Salt-tolerant transgenic perennial ryegrass (Lolium
perenne L.) obtained by Agrobacterium tumefaciens-
mediated transformation of the vacuolar Na+/H+ antiporter
gene. Plant Sci. 169, 65–73.
[97] An, B.-Y. (2008). Expression of a vacuolar Na+ /H+
antiporter gene of alfalfa enhances salinity tolerance in
transgenic Arabidopsis. Acta Agron. Sinica 34, 557–564.
[98] Zhang, G.-H., Su, Q., An, L.-J., Wu, S. (2008). Characteri-
zation and expression of a vacuolar Na+/H+ antiporter gene
from the monocot halophyte Aeluropus littoralis. Plant
Physiol. Biochem. 46, 117–126.
[99] Bao, A.-K., Wang, S.-M., Wu, G.-Q., Xi, J.-J., Zhang, J.-L.,
et al. (2009). Overexpression of the Arabidopsis H+ -PPase
enhanced resistance to salt and drought stress in transgenic
alfalfa (Medicago sativa L.). Plant Sci. 176, 232–240.
[100a] Tian, N., Wang, J., Xu, Z.Q. (2011). Overexpression
of Na+/H+ antiporter gene AtNHX1 from Arabidopsis
thaliana improves the salt tolerance of kiwifruit (Actinidia
deliciosa). S. Afr. J. Bot. 77, 160–169.
[100b] Li, W., Wang, D., Jin, T., Chang, Q., Yin, D., et al. (2010).
The vacuolar Na+ /H+ antiporter gene SsNHX1 from the
halophyte Salsola soda confers salt tolerance in transgenic
alfalfa (Medicago sativa L.). Plant Mol. Biol. Rep. 29, 278–
290.
[101] Li, Y., Zhang, Y., Feng, F., Liang, D., Cheng, L., et al.
(2010). Overexpression of a Malus vacuolar Na+/H+
antiporter gene (MdNHX1) in apple rootstock M.26 and its
influence on salt tolerance. Plant Cell Tissue Organ Cult.
102, 337–345.
[102] Asif, M.A., Zafar, Y., Iqbal, J., Iqbal, M.M., Rashid, U.,
et al. (2011). Enhanced expression of AtNHX1, in trans-
genic groundnut (Arachis hypogaea L.) improves salt and
drought tolerence. Mol. Biotechnol. 49, 250–256.
[103] Wei, Q., Guo, Y.J., Cao, H.M., Kuai, B.K. (2011).
Cloning and characterization of an AtNHX2 -like Na+/H+
antiporter gene from Ammopiptanthus mongolicus (Legu-
minosae) and its ectopic expression enhanced drought and
salt tolerance in Arabidopsis thaliana. Plant Cell Tissue
Organ Cult. 105, 309–316.
[104] Zhao, F., Guo, S., Zhang, H., Zhao, Y. (2006). Expression
of yeast SOD2 in transgenic rice results in increased salt
tolerance. Plant Sci. 170, 216–224.
[105] Gao, F., Gao, Q., Duan, X., Yue, G., Yang, A., et al. (2006).
Cloning of an H+-PPase gene from Thellungiella halophila
and its heterologous expression to improve tobacco salt
tolerance. J. Exp. Bot. 57, 3259–3270.
[106] Lv, S.-L., Lian, L.-J., Tao, P.-L., Li, Z.-X., Zhang, K.-W.,
et al. (2009). Overexpression of Thellungiella halophila
H+-PPase (TsVP) in cotton enhances drought stress resis-
tance of plants. Planta 229, 899–910.
[107] Pasapula, V., Shen, G., Kuppu, S., Paez-Valencia, J., Men-
doza, M., et al. (2011). Expression of an Arabidopsis vac-
uolar H+-pyrophosphatase gene (AVP1) in cotton improves
drought- and salt tolerance and increases fibre yield in the
field conditions: Using AVP1 to improve drought and salt
tolerance in cotton. Plant Biotechnol. J. 9, 88–99.
[108] Shi, H., Quintero, F.J., Pardo, J.M., Zhu, J.-K. (2002). The
putative plasma membrane Na+/H+ antiporter SOS1 con-
trols long-distance Na+ transport in plants. Plant Cell. 14,
465–477.
[109] Gao, X., Ren, Z., Zhao, Y., Zhang, H. (2003). Overexpres-
sion of SOD2 increases salt tolerance of Arabidopsis. Plant
Physiol. 133, 1873–1881.
[110] Huertas, R., Olı́as, R., Eljakaoui, Z., Gálvez, F.J., Li, J.,
et al. (2012). Overexpression of SlSOS2 (SlCIPK24) con-
fers salt tolerance to transgenic tomato. Plant Cell Environ.
35, 1467–1482.
[111] Ma, D.-M., Xu, W.-R., Li, H.-W., Jin, F.-X., Guo, L.-N.,
et al. (2013). Co-expression of the Arabidopsis SOS genes
enhances salt tolerance in transgenic tall fescue (Festuca
arundinacea Schreb.). Protoplasma 251, 219–231.
[112] Davenport, R.J., Munoz-Mayor, A., Jha, D., Essah, P.A.,
Rus, A., Tester, M. (2007). The Na+ transporter AtHKT1
controls retrieval of Na+ from the xylem in Arabidopsis.
Plant Cell Environ. 30, 497–507.
[113] Huang, S., Spielmeyer, W., Lagudah, E.S., James, R.A.,
Platten, J.D., Dennis, E.S., Munns, R. (2006). A sodium
transporter (HKT7) is a candidate for Nax1, a gene for
salt tolerance in durum wheat. Plant Physiol. 142, 1718–
1727.
[114] Horie, T., Costa, A., Kim, T.H., Han, M.J., Horie, R., Leung,
H.-Y., Miyao, A., Hirochika, H., An, G., Schroeder, J.I.
(2007). Rice OsHKT2 transporter mediates large Na+ influx
component into K+ starved roots for growth. EMBO J. 26,
3003–3014.
[115] Chérel, I. (2004). Regulation of K+ channel activities in
plants: from physiological to molecular aspects. J. Exp.
Bot. 55, 337–351.
[116] Carden, D.E., Walker, D.J., Flowers, T.J., Miller, A.J.
(2003). Single-cell measurements of the contributions of
cytosolic Na+ and K+ to salt tolerance. Plant Physiol. 131,
676–683.
[117] Neid, S.L., Biesboer, D.D. (2005). Alleviation of salt-
induced stress on seed emergence using soil additives in
a greenhouse. Plant Soil 268, 303–307.
[118] Zheng, Y., Jia, A., Ning, T., Xu, J., Li, Z., Jiang, G. (2008).
Potassium nitrate application alleviates sodium chloride
stress in winter wheat cultivars differing in salt tolerance.
J. Plant Physiol. 165, 1455–1465.
[119] Li, D., Ma, N.N., Wang, J.R., Yang, D.Y., Zhao, S.J., Meng,
Q.W. (2013). Over-expression of tomato enhancer of SOS3-
1 (LeENH1) in tobacco enhanced salinity tolerance by

excluding Na+ from the cytosol. Plant Physiol. Biochem.
70, 150–158.
[120] Hueras, R., Rubio, L., Cagdac, O., Garcia-Sanchez, M.J.,
Alche, J.D.D., Venema, K., Fernandez, J., Rodriguez-
Rosales, M.P. (2013). The K+ /H+ antiporter LeNHX2
increases salt tolerance by improving K+ homeostasis in
transgenic tomato. Plant Cell Environ. 36, 2135–2149.
[121] Leidi, E.O., Barragán, V., Rubio, L., El-Hamdaoui, A.,
Ruiz, M.T., Cubero, B., Fernández, J.A., Bressan, R.A.,
Hasegawa, P.M., Quintero, F.J. (2010). The AtNHX1
exchanger mediates potassium compartmentation in vac-
uoles of transgenic tomato. Plant J. 61(3), 495–506.
[122] Mittler, R. (2002). Oxidative stress, antioxidants and stress
tolerance. Trends Plant Sci. 7, 405–410.
[123] Ahmad, P., Jaleel, CA., Salem, M.A., Nabi, G., Sharma, S.
(2010). Roles of enzymatic and nonenzymatic antioxidants
in plants during abiotic stress. Crit. Rev. Biotechnol. 30,
161–175.
[124] Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G. (2012).
ROS and redox signalling in the response of plants to abiotic
stress. Plant Cell Environ. 35, 259–270.
[125] Hernández, J.A., Almansa, M.S. (2002). Short-term effects
of salt stress on antioxidant systems and leaf water relations
of pea leaves. Physiol. Plant 115, 251–257.
[126] Karpinski, S., Muhlenbock, P. (2007). Genetic, molecu-
lar and physiological mechanisms controlling cell death,
defenses, and antioxidant network in response to abiotic
and biotic stresses in plants. Compar. Biochem. Physiol. A:
Mol. Integr. Physiol. 146, S60.
[127] Abrol, E., Vyas, D., Koul, S. (2012). Metabolic shift
from secondary metabolite production to induction of anti-
oxidative enzymes during NaCl stress in Swertia chirata
Buch.-Ham. Acta Physiol. Plant 34, 541–546.
[128] Chen, S., Polle, A. (2010). Salinity tolerance of populus.
Plant Biol. 12, 317–333.
[129] Wang, Y., Ying, Y., Chen, J., Wang, X. (2004). Trans-
genic Arabidopsis overexpressing Mn-SOD enhanced salt-
tolerance. Plant Soi1 67, 671–677.
[130] Wang, Y., Wisniewski, M., Meilan, R., Uratsu, S., Cui, M.,
Dandekar, A., Fuchigami, L. (2007). Ectopic expression
of Mn-SOD in Lycopersicon esculentum leads to enhanced
tolerance to salt and oxidative stress. J. Appl. Hortic. 9, 3–8.
[131] Miller, G., Suzuki, N., Rizhsky, L., Hegie, A., Koussevitzky,
S., Mittler, R. (2007). Double mutants deficient in cytoso-
lic and thylakoid ascorbate peroxidase reveal a complex
mode of interaction between reactive oxygen species, plant
development, and response to abiotic 122] stresses. Plant
Physiol. 144, 1777–1785.
[132] Srivastava, A.K., Bhargava, P., Rai, L.C. (2005). Salin-
ity and copper-induced oxidative damage and changes in
the antioxidative defence systems of Anabaena doliolum.
World J. Microbiol. Biotechnol. 21, 1291–1298.
[133] Pan, Y., Wu, L.J., Yu, Z.L. (2006), Effect of salt and drought
stress on antioxidant enzymes activities and SOD isoen-
zymes of liquorice (Glycyrrhiza uralensis Fisch). Plant
Growth Regul. 49, 157–165.
REFERENCES 883
[134] Badawi Ghazi Hamid, K.N., Tamauchi, Y., Shimada, E.,
Sasaki, R., Kubo, A., Tanaka, K. (2004). Over-expression
of ascorbate peroxidase in tobacco chloroplasts enhances
the tolerance to salt stress and water deficit. Physiol. Plant.
121, 231–238.
[135] Wang, Y.W., Meilan, R., Cui, M., Webb, R., Fuchigami, L.
(2005). Overexpression of cytosolic ascorbate peroxidase
in tomato confers tolerance to chilling and salt stress. J. Am.
Soc. Hort. Sci. 130, 167–173.
[136] Ushimaru, T., Nakagawa, T., Fujioka, Y., Daicho, K., Naito,
M., et al. (2006). Transgenic Arabidopsis plants expressing
the rice dehydroascorbate reductase gene are resistant to
salt stress. J. Plant Physiol. 163, 1179–1184.
[137] Lu, Z., Liu, D., Liu, S. (2007). Two rice cytosolic ascorbate
peroxidases differentially improve salt tolerance in trans-
genic Arabidopsis. Plant Cell Rep. 26, 1909–1917.
[138] Lee, Y.P., Kim, S.H., Bang, J.W., Lee, H.S., Kwak, S.S.,
et al. (2007). Enhanced tolerance to oxidative stress in trans-
genic tobacco plants expressing three antioxidant enzymes
in chloroplasts. Plant Cell Rep. 26, 591–598.
[139] Eltayeb, A.E., Kawano, N., Badawi, G.H., Kaminaka, H.,
Sanekata, T., et al. (2007). Overexpression of monode-
hydroascorbate reductase in transgenic tobacco confers
enhanced tolerance to ozone, salt and polyethylene glycol
stresses. Planta 225, 1255–1264.
[140] Al-Taweel, K., Iwaki, T., Yabuta, Y., Shigeoka, S., Murata,
N., et al. (2007). A bacterial transgene for catalase protects
translation of d1 protein during exposure of salt-stressed
tobacco leaves to strong light. Plant Physiol. 145, 258–
265.
[141] Prashanth, S.R., Sadhasivam, V., Parida, A. (2008). Over-
expression of cytosolic copper/zinc superoxide dismutase
from a mangrove plant Avicennia marina in indica rice var
Pusa Basmati-1 confers abiotic stress tolerance. Transgenic
Res. 17, 281–291.
[142] Tsaftaris, A., Chatzidimitriadou, K., Nianiou-Obeidat, I.,
Madesis, P., Perl-Treves, R. (2009). Expression of SOD
transgene in pepper confer stress tolerance and improve
shoot regeneration. Electron. J. Biotechnol. 12, 78—95.
[143] Sun, W.H., Duan, M., Shu, D.F., Yang, S., Meng, Q.W.
(2010). Over-expression of StAPX in tobacco improves
seed germination and increases early seedling tolerance to
salinity and osmotic stresses. Plant Cell Rep. 29, 917–926.
[144] Qi, Y.C., Liu, W.Q., Qiu, L.Y., Zhang, S.M., Ma, L., et al.
(2010). Overexpression of glutathione S-transferase gene
increases salt tolerance of arabidopsis. Russ. J. Plant Phys-
iol. 57, 233–240.
[145] Kavitha, K., George, S., Venkataraman, G., Parida, A.
(2010). A salt-inducible chloroplastic monodehydroascor-
bate reductase from halophyte Avicennia marina confers
salt stress tolerance on transgenic plants. Biochimie 92,
1321–1329.
[146] Li, Y.J., Hai, R.L., Du, X.H., Jiang, X.N., Lu, H. (2009).
Over-expression of a Populus peroxisomal ascorbate per-
oxidase (PpAPX) gene in tobacco plants enhances stress
tolerance. Plant Breed. 128, 404–410.
884 PHYSIOLOGICAL AND MOLECULAR ASPECTS OF MECHANISMS INVOLVED IN PLANT RESPONSE TO SALT STRESS
[147] Lee, Y.P., Baek, K.H., Lee, H.S., Kwak, S.S., Bang, J.W.,
et al. (2010). Tobacco seeds simultaneously over-expressing
Cu/Zn-superoxide dismutase and ascorbate peroxidase dis-
play enhanced seed longevity and germination rates under
stress conditions. J. Exp. Bot. 61, 2499–2506.
[148] Zhai, C.-Z., Zhao, L., Yin, L.-J., Chen, M., Wang, Q.-
Y., et al. (2013). Two wheat glutathione peroxidase genes
whose products are located in chloroplasts improve salt and
H2 O2 tolerances in Arabidopsis. PLoS ONE 8, e73989.
[149] Diaz-Vivancos, P., Faize, M., Barba-Espin, G., Faize, L.,
Petri, C., et al. (2013). Ectopic expression of cytosolic
superoxide dismutase and ascorbate peroxidase leads to
salt stress tolerance in transgenic plums. Plant Biotechnol.
J. 11, 976-985.
[150] Lumbreras, V., Vilela, B., Irar, S., Solé, M., Capellades,
M., Valls, M., Coca, M. (2010). MAPK phosphatase MKP2
mediates disease responses in Arabidopsis and functionally
interacts with MPK3 and MPK6. Plant J. 63, 1017–1030.
[151] De Bruxelles, G., Peacock, W.J., Dennis, E.S., Dolferus, R.
(1996). Abscisic acid induces the alcohol dehydrogenase
gene in Arabidopsis. Plant Physiol. 111, 381–391.
[152] Popova, L.P., Stoinova, Z.G., Maslenkova, L.T. (1995).
Involvement of abscisic acid in photosynthetic process in
Hordeum vulgare L. during salinity stress. J. Plant Growth
Regul. 14, 211–218.
[153] Xiong, L., Zhu, J.K. (2001). Abiotic stress signal transduc-
tion in plants: Molecular and genetic perspectives. Physiol.
Plant 112, 152–166.
[154] Gilliham, M., Tester, M. (2005). The regulation of anion
loading to the maize root xylem. Plant Physiol. 137, 819–
828.
[155] Ohta, M., Guo, Y., Halfter, U., Zhu, J.K. (2003). A novel
domain in the protein kinase SOS2 mediates interaction
with the protein phosphatase 2C ABI2. Proc. Natl. Acad.
Sci. 100, 11771–11776.
[156] Hu, X., Jiang, M., Zhang, A., Lu, J. (2005). Abscisic
acid-induced apoplastic H2 O2 accumulation up-regulates
the activities of chloroplastic and cytosolic antioxidant
enzymes in maize leaves. Planta 223, 57–68.
[157] Zhang, A., Jiang, M., Zhang, J., Tan, M., Hu, X. (2006).
Mitogen-activated protein kinase is involved in abscisic
acid-induced antioxidant defense and acts downstream of
reactive oxygen species production in leaves of maize
plants. Plant Physiol. 141, 475–487.
[158] Zhang, A., Jiang, M., Zhang, J., Ding, H., Xu, S., Hu, X.,
Tan, M. (2007). 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.
[159] Ye, N., Zhu, G., Liu, Y., Li, Y., Zhang, J. (2011). ABA con-
trols H2 O2 accumulation through the induction of OsCATB
in rice leaves under water stress. Plant Cell Physiol. 52,
689–698.
[160] Miller, G., Suzuki, N., Ciftci-Yilmaz, S., Mittler, R. (2010).
Reactive oxygen species homeostasis and signalling during
drought and salinity stresses. Plant Cell Environ. 33, 453–
467.
[161] Zhang, H., Ni, L., Liu, Y., Wang, Y., Zhang, A., Tan,
M., Jiang, M. (2012). The C2 H2 -type zinc finger protein
ZFP182 is involved in abscisic acid–induced antioxidant
defense in RiceF. J. Integr. Plant Biol. 54, 500–510.
[162] Ibrahim, M.H., Jaafar, H.Z. (2013). Abscisic acid
induced changes in production of primary and secondary
metabolites, photosynthetic capacity, antioxidant capabil-
ity, antioxidant enzymes and lipoxygenase inhibitory activ-
ity of Orthosiphon stamineus Benth. Molecules 18, 7957–
7976.
[163] Idrees, M., Naeem, M., Aftab, T., Khan, M.M.A. (2011).
Salicylic acid mitigates salinity stress by improving antiox-
idant defence system and enhances vincristine and vin-
blastine alkaloids production in periwinkle [Catharan-
thus roseus (L.) G. Don]. Acta Physiol. Plant 33, 987–
999.
[164] Nazar, R., Iqbal, N., Syeed, S., Khan, N.A. (2011). Salicylic
acid alleviates decreases in photosynthesis under salt stress
by enhancing nitrogen and sulfur assimilation and antioxi-
dant metabolism differentially in two mungbean cultivars.
J. Plant Physiol. 168, 807–815.
[165] Shabala, S.N., Newman, I.A., Morris, J. (1997). Oscillations
in H+ and Ca2+ ion fluxes around the elongation region of
corn roots and effects of external pH. Plant Physiol. 113(1),
111–118.
[166] Jayakannan, M., Bose, J., Babourina, O., Rengel, Z., Sha-
bala, S. (2013). Salicylic acid improves salinity tolerance in
Arabidopsis by restoring membrane potential and prevent-
ing salt-induced K+ loss via a GORK channel. J. Exp. Bot.
64, 2255–2268.
[167] Horváth, E., Szalai, G., Janda, T. (2007). Induction of abi-
otic stress tolerance by salicylic acid signaling. J. Plant
Growth Regul. 2, 290–300.
[168] Gao, W., Bai, S., Li, Q., Gao, C., Liu, G., Li, G., Tan,
F. (2013). Overexpression of TaLEA gene from Tamarix
androssowii improves salt and drought tolerance in trans-
genic poplar (Populus simonii P. nigra). PloS ONE 8,
e67462.
[169] Scarpeci, T.E., Zanor, M.I., Mueller-Roeber, B., Valle, E.M.
(2013). Overexpression of AtWRKY30 enhances abiotic
stress tolerance during early growth stages in Arabidopsis
thaliana. Plant Mol. Biol. 1–13.
[170] Cheng, L., Li, X., Huang, X., Liang, Y., Ma, X., Peng, X.,
Jia, J., Chen, S., Chen, Y., Deng, B. (2013). Overexpression
of sheepgrass R1-MYB transcription factor LcMYB1 con-
fers salt tolerance in transgenic Arabidopsis. Plant Physiol.
Biochem. 70, 252–260.
[171] Dodd, I.C., Pérez-Alfocea, F. (2012). Microbial ameliora-
tion of crop salinity stress. J. Exp. Bot. 63, 3415–3428.