Salinidade e Seus Efeitos em Plantas

ARTICLE IN PRESS
Ecotoxicology and Environmental Safety 60 (2005) 324349

www.elsevier.com/locate/ecoenv
Salt tolerance and salinity effects on plants: a review

Asish Kumar Paridaa, Anath Bandhu Dasa,b,
a
National Institute for Plant Biodiversity Conservation and Research, Nayapalli, Bhubaneswar 751015, Orissa, India
b
Regional Plant Resource Centre, Nayapalli, Bhubaneswar 751015, Orissa, India
Received 18 September 2003; received in revised form 8 March 2004; accepted 8 June 2004
Available online 7 August 2004
Abstract
Plants exposed to salt stress undergo changes in their environment. The ability of plants to tolerate salt is determined by multiple
biochemical pathways that facilitate retention and/or acquisition of water, protect chloroplast functions, and maintain ion
homeostasis. Essential pathways include those that lead to synthesis of osmotically active metabolites, specic proteins, and certain
free radical scavenging enzymes that control ion and water ux and support scavenging of oxygen radicals or chaperones. The
ability of plants to detoxify radicals under conditions of salt stress is probably the most critical requirement. Many salt-tolerant
species accumulate methylated metabolites, which play crucial dual roles as osmoprotectants and as radical scavengers. Their
synthesis is correlated with stress-induced enhancement of photorespiration. In this paper, plant responses to salinity stress are
reviewed with emphasis on physiological, biochemical, and molecular mechanisms of salt tolerance. This review may help in
interdisciplinary studies to assess the ecological signicance of salt stress.
r 2004 Elsevier Inc. All rights reserved.
Keywords: Antioxidative enzymes; Compatible solutes; Ion homeostasis; Photosynthesis; Salt stress
1. Introduction
Salinity is the major environmental factor limiting
plant growth and productivity (Allakhverdiev et al.,
2000b). The detrimental effects of high salinity on plants
can be observed at the whole-plant level as the death of
plants and/or decreases in productivity. Many plants
develop mechanisms either to exclude salt from their
cells or to tolerate its presence within the cells. During
the onset and development of salt stress within a plant,
all the major processes such as photosynthesis, protein
synthesis, and energy and lipid metabolism are affected.
The earliest response is a reduction in the rate of leaf
surface expansion, followed by a cessation of expansion
as the stress intensies. Growth resumes when the stress
is relieved. Carbohydrates, which among other subCorresponding author. National Institute for Plant Biodiversity
Conservation and Research, Nayapalli, Bhubaneswar 751015, Orissa,
India. Fax: +91-674-2550274.
E-mail address: a_b_das@hotmail.com (A.B. Das).
0147-6513/$ - see front matter r 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.ecoenv.2004.06.010
strates are needed for cell growth, are supplied mainly

through the process of photosynthesis, and photosynthesis rates are usually lower in plants exposed to salinity
and especially to NaCl.
Salinity stress biology and plant responses to high
salinity have been discussed over two decades (Flowers
et al., 1977; Greenway and Munns, 1980; Ehret and
Plant, 1999; Hasegawa et al., 2000; Zhu, 2002) and it has
been over a decade since salinity tolerance in marine
algae has been covered (Kirst, 1989). These reviews
covered organismal, physiological, and the then-known
biochemical hallmarks of stress and the bewildering
complexity of plant stress responses. We summarize in
this review physiological, biochemical, and molecular
mechanisms of salt tolerance with the salient features of
salinity stress effects on plants. In this review, much
research information about cellular, metabolic, molecular, and genetic processes associated with the response to
salt stress, some of which presumably function to
mediate salt tolerance, has been gathered.
ARTICLE IN PRESS
A.K. Parida, A.B. Das / Ecotoxicology and Environmental Safety 60 (2005) 324349
2. Salt tolerance of plants

Salt tolerance is the ability of plants to grow and
complete their life cycle on a substrate that contains
high concentrations of soluble salt. Plants that can
survive on high concentrations of salt in the rhizosphere
and grow well are called halophytes. Depending on their
salt-tolerating capacity, halophytes are either obligate
and characterized by low morphological and taxonomical diversity with relative growth rates increasing up to
50% sea water or facultative and found in less saline
habitats along the border between saline and nonsaline
upland and characterized by broader physiological
diversity which enables them to cope with saline and
nonsaline conditions.
2.1. Mechanism of salt tolerance
Plants develop a plethora of biochemical and molecular mechanisms to cope with salt stress. Biochemical
pathways leading to products and processes that
improve salt tolerance are likely to act additively and
probably synergistically (Iyengar and Reddy, 1996).
Biochemical strategies include (i) selective accumulation
or exclusion of ions, (ii) control of ion uptake by roots
and transport into leaves, (iii) compartmentalization of
ions at the cellular and whole-plant levels, (iv) synthesis
325
of compatible solutes, (v) change in photosynthetic

pathway, (vi) alteration in membrane structure, (vii)
induction of antioxidative enzymes, and (viii) induction
of plant hormones (Fig. 1). These are discussed under
separate headings.
Salt tolerance mechanisms are either low-complexity
or high-complexity mechanisms. Low-complexity mechanisms appear to involve changes in many biochemical pathways. High-complexity mechanisms involve
changes that protect major processes such as photosynthesis and respiration, e.g., water use efciency, and
those that preserve such important features as cytoskeleton, cell wall, or plasma membranecell wall interactions (Botella et al., 1994) and chromosome and
chromatin structure changes, i.e., DNA methylation,
polyploidization, amplication of specic sequences, or
DNA elimination (Walbot and Cullis, 1985). It is
believed that for the protection of higher-order processes, low-complexity mechanisms are induced coordinately (Bohnert et al., 1995).
2.2. Ion regulation and compartmentalization
Ion uptake and compartmentalization are crucial not
only for normal growth but also for growth under saline
conditions (Adams et al., 1992b) because the stress
disturbs ion homeostasis. Plants, whether glycophyte or
Extracellular and cell-wall space Ion exclusion

Ion export
Cell-wall modification
Cytosol and organelle space

Osmotic adjustment
Radical scavenging
Ion-selectivity changes
Enhancement of proton pumping
Aquaporin-activity control
Plant growth regulator

sensitivity adjustment
Osmoprotection
Ion partitioning
Vacuolar space
Ion (sodium, calcium) storage
Ion (potassium) export
Osmotic adjustment
Proton-gradient maintenance
Fig. 1. Biochemical functions associated with tolerance to plant salt stress. The schematic presentation of a plant cell includes three compartments
that are dened by the plasma membrane and tonoplast (reproduced from Bohnert and Jensen, 1996).
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326
halophyte, cannot tolerate large amounts of salt in the

cytoplasm and therefore under saline conditions they
either restrict the excess salts in the vacuole or
compartmentalize the ions in different tissues to facilitate their metabolic functions (Reddy et al., 1992;
Iyengar and Reddy, 1996; Zhu, 2003). Glycophytes limit
sodium uptake or partition sodium in older tissues that
serve as storage compartments that are eventually
sacriced (Cheeseman, 1988).
Removal of sodium from the cytoplasm or compartmentalization in the vacuoles is done by a salt-inducible
enzyme Na+/H+ antiporter (Apse et al., 1999). Two
electrogenic H+ pumps, the vacuolar type H+-ATPase
(V-ATPase) and the vacuolar pyrophosphatase (VPPase), coexist at membranes of the secretory pathway
of plants (Dietz et al., 2001). The V-ATPase is the
dominant H+ pump at endomembranes of most plant
cells with regard to protein amount and, frequently,
activity. The V-ATPase is indispensable for plant
growth under normal conditions due to its roles in
energizing secondary transport, maintaining solute
homeostasis, and, possibly, facilitating vesicle fusion.
Under stress conditions such as salinity, drought, cold,
acid stress, anoxia, and excess heavy metals in the soil,
survival of the cells depends strongly on maintaining or
adjusting the activity of the V-ATPase. Regulation of
gene expression and activity are involved in adapting the
V-ATPase on long- and short-term bases (Dietz, et al.,
2001). Salt modulation of the tonoplast H+-pumping VATPase and H+-pyrophosphatase has been evaluated in
hypocotyls of Vigna unguiculata seedlings (Otoch et al.,
2001). Salt stress induces V-ATPase expression in V.
unguiculata with concomitant enhancement of its
activity as a homeostatic mechanism to cope with salt
stress, whereas under the same conditions V-PPase is
inhibited (Otoch et al., 2001). The main strategy of salt
tolerance in the halophyte Suaeda salsa seems to be an
up-regulation of V-ATPase activity, which is required to
energize the tonoplast for ion uptake into the vacuole,
while V-PPase plays only a minor role (Wang et al.,
2001).
When under salt stress, plants maintain high concentrations of K+ and low concentrations of Na+ in the
cytosol. They do this by regulating the expression and
activity of K+ and Na+ transporters and of H+ pumps
that generate the driving force for transport (Zhu et al.,
1993). Although salt-stress sensors remain elusive, some
of the intermediary signaling components have been
identied. Evidence suggests that a protein kinase
complex consisting of the myristoylated calcium-binding
protein SOS3 and the serine/threonine protein kinase
SOS2 is activated by a salt-stress-elicited calcium
signal. The protein kinase complex then phosphorylates
and activates various ion transporters, such as the
plasma membrane Na+/H+ antiporter SOS1 (Zhu
et al., 1993).
The Arabidopsis thaliana AtNHX1 gene encodes a

vacuolar Na+/H+ antiporter that is important in salt
tolerance. The tissue distribution and regulation of
AtNHX1 expression by salt stress and abscisic acid
(ABA) have been reported by Shi and Zhu (2002).
Experimental evidence shows that the steady state level
of AtNHX1 transcript is up-regulated by treatment with
NaCl, KCl, or ABA. AtNHX1 promoter (GUS) analysis
in transgenic Arabidopsis shows that AtNHX1 is
expressed in all tissues except the root tip. Strong
GUS expression was detected in guard cells, suggesting
that AtNHX1 may play a role in pH regulation and/or
K+ homeostasis in the specialized cells. AtNHX1
promoter activity is substantially up-regulated by NaCl,
KCl, or ABA, demonstrating that salt and ABA
regulation of AtNHX1 expression occurs at the transcriptional level. Strong induction of GUS activity in
root hair cells suggests a role of AtNHX1 in storing Na+
in the enlarged vacuoles in root hair cells. The upregulation of AtNHX1 transcript levels by NaCl is
reduced in abil-1, aba2-1, and aba3-1 but not in abi2-1,
sos1, sos2, or sos3 mutants of Arabidopsis. ABAinduced AtNHX1 expression is also decreased in abil-1
but not in abi2-1. This evidence suggests that salt stress
up-regulates AtNHX1 expression transcriptionally and
that the up-regulation is partially dependent on ABA
biosynthesis and ABA signaling through ABI1 (Shi and
Zhu, 2002).
With a homologous gene region a Na+/H+ antiporter gene has been isolated from a halophytic plant,
Atriplex gmelini, and named AgNHX1 (Hamada et al.,
2001). The isolated cDNA is 2607 bp in length and
contains one open reading frame, which comprises 555
amino acid residues with a predicted molecular mass of
61.9 kDa. The amino acid sequence of the AgNHX1
gene shows more than 75% identity with those of the
previously isolated NHX1 genes from the glycophytes A.
thaliana and Oryza sativa. The migration pattern of
AgNHX1 is shown to correlate with H+-pyrophosphatase and not with P-type H+-ATPase, suggesting
the localization of AgNHX1 in a vacuolar membrane.
Induction of the AgNHX1 gene has been observed by
salt stress at both mRNA and protein levels. The
expression of the AgNHX1 gene in the yeast mutant,
which lacks the vacuolar-type Na+/H+ antiporter gene
(NHX1) and has poor viability under the high-salt
conditions, shows partial complementation of the
NHX1 functions. It has been suggested that the
AgNHX1 products have important roles in salt tolerance (Hamada et al., 2001).
Experimental evidence implicates Ca2+ function in
salt adaptation. Externally supplied Ca2+ reduces the
toxic effects of NaCl, presumably by facilitating higher
K+/Na+ selectivity (Liu and Zhu, 1997; Lauchli and
Schubert, 1989). High salinity also results in increased
cytosolic Ca2+ that is transported from the apoplast
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and intracellular compartments (Knight et al., 1997).

The resultant transient Ca2+ increase potentiates stress
signal transduction and leads to salt adaptation
(Mendoza et al., 1994; Knight et al., 1997). A prolonged
elevated Ca2+ level may, however, also pose a stress; if
so, reestablishment of Ca2+ homeostasis is a requisite.
Other mechanisms of salt regulation are salt secretion
and selective salt accumulation or exclusion. Salt
secretion occurs through development of unique cellular
structures called salt glands. These salt glands secrete
salt (especially NaCl) from leaves and maintain internal
ion concentration at lower level (Hogarth, 1999). Salt
exclusion occurs through roots to regulate the salt
content of their leaves in many halophytes (Levitt,
1980). Selective accumulation of ions or solutes enables
the plants to make osmotic adjustments, which occur
through mass action, and results in increased water
retention and/or sodium exclusion.
2.3. Induced biosynthesis of compatible solutes
To accommodate the ionic balance in the vacuoles,
cytoplasm accumulates low-molecular-mass compounds
termed compatible solutes because they do not interfere
with normal biochemical reactions (Yancey et al., 1982;
Ford, 1984; Ashihara et al., 1997; Hasegawa et al., 2000;
Zhifang and Loescher, 2003); rather, they replace water
in biochemical reaction. With accumulation proportional to the change of external osmolarity within
species-specic limits, protection of structures and
osmotic balance supporting continued water inux (or
reduced efux) are accepted functions of osmolytes
(Hasegawa et al., 2000). These compatible solutes
include mainly proline (Khatkar and Kuhad, 2000;
Singh et al., 2000), glycine betaine (GB) (Rhodes and
Hanson, 1993; Khan et al., 2000a; Wang and Nil, 2000),
sugars (Kerepesi and Galiba, 2000; Bohnert and Jensen,
1996; Pilon-Smits et al., 1995), and polyols (Ford, 1984;
Popp et al., 1985; Orthen et al., 1994; Bohnert et al.,
1995).
Polyols make up a considerable percentage of all
assimilated CO2 and serve several functions: as compatible solutes, as low-molecular-weight chaperones, and
as scavengers of stress-induced oxygen radicals (Smirnoff and Cumbes, 1989; Bohnert et al., 1995). Polyols are
classied as acyclic (e.g., manitol) and cyclic (e.g.,
pinitol). Mannitol, a sugar alcohol that may serve as a
compatible solute to cope with salt stress, is synthesized
via the action of a mannose-6-phosphate reductase
(M6PR) in celery (Zhifang and Loescher, 2003). In
contrast to previous approaches that have used a
bacterial gene to engineer mannitol biosynthesis in
plants and other organisms, A. thaliana, a nonmannitol-producer, has been transformed with the
celery leaf M6PR gene under control of the CaMV
35S promotor. In all independent Arabidopsis M6PR
327
transformants, mannitol accumulates throughout the

plants in amounts ranging from 0.5 to 6 mmol g1 fresh
weight. A novel compound, not found in either celery or
Arabidopsis,
1-O-beta-D-glucopyranosyl-D-mannitol,
also accumulates in vegetative tissues of mature plants
in amounts up to 4 mmol g1 fresh weight but not in
owers and seeds. In the absence of NaCl, all
transformants are phenotypically the same as the wild
type; however, in the presence of NaCl, mature
transgenic plants shows a high level of salt tolerance,
i.e., growing, completing normal development, owering, and producing seeds in soil irrigated with 300 mM
NaCl in the nutrient solution. These results demonstrate
a major role in developing salt-tolerant plants by means
of introducing mannitol biosynthesis using M6PR
(Zhifang and Loescher, 2003). Pinitol is synthesized
from myo-inositol by the sequential catalysis of inositolo-methyltransferase and ononitol epimerase (Bohnert
and Jensen, 1996). Polyols function in two ways that are
difcult to separate mechanistically: osmotic adjustment
and osmoprotection. In osmotic adjustment, they act as
osmolytes facilitating the retention of water in the
cytoplasm and allowing sodium sequestration to the
vacuole or apoplast. These osmolytes protect cellular
structures by interacting with membranes, protein
complexes, or enzymes. These compounds have hydrogen-bonding characteristics that allow them to protect
macromolecules from the adverse effects of increasing
ionic strength in the surrounding media (Crowe et al.,
1992). By tight association with protein and membrane
components, they compensate for water loss during
stress (Yancey et al., 1982). Those polyols that are
nonreducing sugars may also store excess carbon under
environmental stress conditions (Vernon et al., 1993).
The cyanobacterium Synechocystis sp. PCC 6803
accumulates the compatible solute glucosylglycerol
(GG) and sucrose under salt stress (Hagemann and
Murata, 2003). The molecular mechanisms for GG
synthesis including regulation of the GG-phosphate
synthase (ggpS) gene, which encodes GgpS, has been
intensively investigated. Experimental evidences shows
that GG is important for salt tolerance and thus for the
proper division of cells under salt stress conditions in
Synechocystis (Hagemann and Murata, 2003). Accumulation of the polyol myo-inositol in leaf tissues of
Actidinia takes place under salt stress and accumulation
of myo-inositol is negatively correlated to fructose and
glucose (Klages et al., 1999). Severe salt stress
(4120 mM NaCl) led to a preferential accumulation
of D-pinitol in gametophytes of Acrostichum aureum,
whereas the sporophyte accumulates D-1-O-methylmuco-inositol (Sun et al., 1999).
Carbohydrates such as sugars (glucose, fructose,
sucrose, fructans) and starch accumulate under salt
stress (Parida et al., 2002). Their major functions are
osmoprotection, osmotic adjustment, carbon storage,
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328
and radical scavenging. Salt stress increases reducing

sugars (glucose, fructose), sucrose, and fructans in a
number of plants (Kerepesi and Galiba, 2000; Khatkar
and Kuhad, 2000; Singh et al., 2000). In Vicia faba
salinity decreases soluble and hydrolyzable sugars
(Gadallah, 1999). Sugar content increases in some
genotypes of rice but also decreases in some genotypes
(Alamgir and Ali, 1999). Under salinity, the starch
content in roots of rice plants declines and remains
unchanged in shoots. A decrease in starch content and
an increase in both reducing and nonreducing sugar
have been reported in leaves of Bruguiera parviflora
(Parida et al., 2002) (Fig. 2). The contents of reducing
and nonreducing sugars and the activity of sucrose
phosphate synthase increase under salt stress, whereas
starch phosphorylase activity decreases (Dubey and
Singh, 1999). In leaves of tomato the contents of soluble
sugars and total saccharides are signicantly increased,
but the starch content is not affected signicantly by
NaCl treatment (Khavarinejad and Mosto, 1998). Gao
et al. (1998) have reported that in tomato (Lycopersicon
esculentum L.) salinity enhances sucrose concentration
and activity of sucrose phosphate synthase (EC 2.3.1.14)
in leaves but decreases the activity of acid invertase (EC
2.3.1.14). It has also been reported that polyphenol level
M
66.0
43.0
29.0
increases in leaves of B. parviflora by salt stress (Fig. 4)

(Parida et al., 2002).
A number of nitrogen-containing compounds (NCC)
accumulate in plants exposed to saline stress. The most
frequently accumulating NCC include amino acids,
amides, imino acids, proteins, quaternary ammonium
compounds, and polyamines. The specic NCC that
accumulate in saline environments varies with plant
species. Osmotic adjustment, protection of cellular
macromolecules, storage of nitrogen, maintenance of
cellular pH, detoxication of the cells, and scavenging of
free radicals are proposed functions of these compounds
under stress conditions. NCC accumulation is usually
correlated with plant salt tolerance (Mansour, 2000).
There are several reports of accumulation of free amino
acids and other NCC under salt stress. Glycine betaine
content increases by salt stress in a number of plants
(Khan et al., 1998, 1999, 2000a; Saneoka et al., 1999;
Muthukumarasamy et al., 2000; Wang and Nil, 2000).
Khan et al. (2000a) have reported that glycine betaine
content increases in shoots and does not differ
signicantly in roots of Haloxylon recurvum under salt
stress. Many plants accumulate proline as a nontoxic
and protective osmolyte under saline conditions (Lee
and Liu, 1999; Khatkar and Kuhad, 2000; Muthukumarasamy et al., 2000; Singh et al., 2000; Jain et al.,
2001). It has been reported that proline levels increase
signicantly in leaves of nonsecretor mangrove B.
parviflora (Fig. 3) (Parida et al., 2002) and in saltsecretor mangrove Aegiceras corniculatum (Parida et al.,
unpublished data). The most abundant amino acids
(cysteine, arginine, methionine), constituting about 55%
of total free amino acid content, are reduced in NaCltreated plants of wheat, but valine, isoleucine, aspartic
acid, and proline increase in response to NaCl stress and
NaCl-treated wheat seedlings show 1.6-fold increase in
total free amino acids compared to the control
(Elshintinawy and Elshourbagy, 2001). In Zea mays,
20.1
14.3
Fig. 2. Changes in protein proe in leaf of B. parviflora after 7, 14, and

30 days recovery from salt stress. Lanes C and 1 represent proteins
extracted from control and 400 mM NaCl-treated (45 day) leaves.
Lanes 2, 3, and 4 represent proteins extracted from leaves after 7, 14
and 30 days of desalinization, respectively. Lane M represents the
molecular weight marker. The boldface arrow on the left indicates the
23-kDa polypeptide, which reappears after desalinization (from Parida
et al., 2004c).
Fig. 3. Effects of NaCl stress on proline level in B. parviflora measured

as a function of days of NaCl treatment. Values are mean7SE (from
Parida et al., 2002).
Table 1
Responses to salt-stress-accumulating products and their function(s) in conferring tolerance
Suggested function(s)
References
Ions
Sodium, chloride
Osmotic adjustment
Potassium exclusion/Export
Blumwald et al. (2000); Hasegawa et al. (2000); Nilu et al. (1995)

Koyro (2000)
Khan et al. (2000a, b)
Proteins
Osmotin
SOD/Catalase
Pathogenesis-related proteins
Osmoprotection
Radical detoxication
Singh et al. (1987); King et al. (1988)

Bohnert and Jensen (1996)
Bohnert and Jensen (1996); Allen et al (1997); Hernandez et al. (2000)
Amino acids
Proline
Ectoine
Osmotic adjustment
Osmoprotection
Khatkar and Kuhad (2000); Singh et al. (2000); Lin et al. (2002)
Lippert and Galinski (1992)
Sugars
Glucose, fructose, sucrose

Fructans
Osmotic adjustment
Osmoprotection, carbon storage
Kerepesi and Galiba (2000)

Bohnert and Jensen (1996); Pilon-Smits et al. (1995)
Polyols
Acyclic (e.g., manitol)

Cyclic (e.g., pinitol)
Carbon storage, osmotic adjustment

Osmoprotection, osmotic adjustment
Retention of photochemical efciency of PSII
Radical scavenging
Popp et al. (1985); Bohnert et al. (1995)

Ford (1984); Bohnert et al. (1995)
Sun et al (1999)
Smirnoff and Cumbes (1989); Orthen et al. (1994)
Polyamines
Spermine, spermidine
Ion balance, chromatin protection
Tiburico et al. (1993); SantaCruz et al. (1998)
Quaternary amines Glycine betaine

b-Alanine betaine,
Dimethyl-sulfonio propionate,
Choline-o-sulfate
Trigonelline
Pigments
Osmoprotection
Khan et al. (2000a); Wang and Nil (2000)
Preservation of thylakoid and plasma membrane integrity Rhodes and Hanson (1993)
Osmoprotection
Rhodes and Hanson (1993)
Osmoprotection
Hanson (1998); Trossat et al. (1998)
Osmoprotection
Nuccio et al. (1999)
Rajasekaran et al. (2001)
Carotenoids, anthocyanins, betalaines Protection against photoinhibition
Foyer et al. (1994); Adams et al. (1992a); Kennedy and De Fillippis (1999)
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Specic compound
Product group
329
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330
with increasing external salt concentration, amino acids

and quaternary ammonium compounds accumulate in
leaves and roots, with concentrations in leaves exceeding
those in roots (AbdElBaki et al., 2000). Proline
accumulates in leaves, stems, and roots of Pringlea
antiscorbutica (kerguelen cabbage) and this osmolyte
accumulate at a 23 higher concentration in the
cytoplasm than in the vacuole (Aubert et al., 1999).
Mattioni et al. (1997) have reported that most of the
amino acids show an increase with the induction of
water or salt stress in durum wheat (Triticum durum),
but proline increases more markedly than other amino
acids and the activity of the enzyme delta (1)-pyrroline5-carboxylate reductase (EC 1.5.1.2) involved in proline
biosynthesis is enhanced during both water and salt
stress, while the activity of proline dehydrogenase (EC
1.5.1.2) involved in proline catabolism is inhibited only
during salt stress. These results indicate that synthesis de
novo is the predominant mechanism in proline accumulation in durum wheat. In mulberry, free amino acids
increase at low salinity and decrease at high salinity and
glycine betaine accumulates more than proline (Agastian et al., 2000). Proline, quaternary ammonium, and
tertiary sulfonium osmolytes are zwitter ions at physiological pH. Although they are ionic, they have no net
charge. Their osmotic function is due to their unique
chemistry.
Experimental observations shows that transformation
of plants with the codA gene for choline oxidase
enhances tolerance of the transgenic plants to salt stress
at the reproductive stage as a result of the accumulation
of GB in the reproductive organs (Sulpice et al., 2003).
The compatible solute N-epsilon-acetyl-beta-lysine is
unique to methanogenic archaea and is produced under
salt stress only (Puger et al., 2003). However, the
molecular basis for the salt-dependent regulation of Nepsilon-acetyl-beta-lysine formation is unknown. Genes
potentially encoding lysine-2, 3-aminomutase (abl4) and
beta-lysine acetyltransferase (ablB), which are assumed
to catalyze N-epsilon-acetyl-beta-lysine formation from
alpha-lysine, have been identied on the chromosomes
of the methanogenic archaea Methanosarcina mazei Gol,
Methanosarcina acetivorans, Methanosarcina barkeri,
Methanococcus jannaschii, and Methanococcus maripaludis (Puger et al., 2003). Table 1 provides examples of
plant products whose action correlates with metabolic
functions that are known or assumed to enable plants to
cope with salt tolerance.
A common feature of compatible solutes is that these
compounds can accumulate to high levels without
disturbing intracellular biochemistry (Bohnert and
Jensen, 1996). Compatible solutes have the capacity to
preserve the activity of enzymes that are in saline
solutions. These compounds have minimal effect on pH
or charge balance of the cytosol or lumenal compartments of organelles. The synthesis of compatible
osmolytes is often achieved by diversion of basic

intermediary metabolites into unique biochemical reactions. Often, stress triggers this metabolic diversion. For
example, higher plants synthesize glycine betaine from
choline by two reactions that are catalyzed in sequence
by choline monooxygenase and betaine aldehyde dehydrogenase (Rhodes and Hanson, 1993).
2.4. Induction of antioxidative enzymes
Salt stress is complex and imposes a water decit
because of osmotic effects on a wide variety of metabolic
activities (Greenway and Munns, 1980; Cheeseman,
1988). This water decit leads to the formation of
reactive oxygen species (ROS) such as superoxide (Od
2 ),
hydrogen peroxide (H2O2), hydroxyl radical (dOH)
(Halliwell and Gutteridge, 1985), and singlet oxygen
(1O2) (Elstner, 1987). These cytotoxic activated oxygen
species can seriously disrupt normal metabolism through
oxidative damage to lipids (Fridovich, 1986; Wise and
Naylor, 1987) and to protein and nucleic acids (Fridovich, 1986; Imlay and Linn, 1988). Since internal O2
concentrations are high during photosynthesis (Steiger et
al., 1977), chloroplasts are especially prone to generate
activated oxygen species (Asada and Takahashi, 1987).
Once produced, Od
will rapidly dismutate, either
2
enzymatically or nonenzymatically, to yield H2O2 and
O2. In addition, H2O2 may interact in the presence of
certain metal ions or metal chelates to produce highly
reactive dOH (Imlay and Linn, 1988). In varying
degrees, present day plants possess a number of
antioxidants that protect against the potentially cytotoxic species of activated oxygen. The metalloenzyme
superoxide dismutase (SOD; EC 1.15.1.1) converts Od
2
to H2O2. Catalase and a variety of peroxidases (Chang et
al., 1984) catalyze the breakdown of H2O2. Although
catalase is apparently absent in the chloroplast, H2O2
can be detoxied in a reaction catalyzed by an ascorbatespecic peroxidase often present in high levels in this
organelle (Chen and Asada, 1989) through the ascorbateglutathione cycle (Halliwell and Gutteridge, 1986;
Asada, 1992). Both ascorbate and glutathione have been
reported in millimolar concentrations within the chloroplast (Halliwell, 1982). Ascorbate can also be oxidized
by direct reaction with Od
2 or by serving as a reductant
of the a-chromoxyl radical of oxidized a-tocopherol
(Foyer et al., 1991). The thylakoid membranes are rich in
a-tocopherol which disrupts lipid peroxidation reactions
not only by reacting with Od
but also by scavenging
2
hydroxyl, peroxyl, and alkoxyl radicals (Halliwell, 1987).
When plants are subjected to environmental stress
conditions such as high light intensity, temperature
extremes, drought, high salinity, herbicide treatment, or
mineral deciencies, the balance between the production
of reactive oxygen species and the quenching activity of
the antioxidants is upset, often resulting in oxidative
ARTICLE IN PRESS
damage (Harper and Harvey, 1978; Dhindsa and

Matowe, 1981; Wise and Naylor, 1987; Spychalla and
Desborough, 1990). Plants with high levels of antioxidants, either constitutive or induced, have been
reported to have greater resistance to this oxidative
damage (Harper and Harvey, 1978; Dhindsa and
Matowe, 1981; Wise and Naylor, 1987; Spychalla and
Desborough, 1990). The activities of the antioxidative
enzymes such as catalase (CAT), ascorbate peroxidase
(APX), guaicol peroxidase (POD), glutathione reductase
(GR), and superoxide dismutase increase under salt
stress in plants and a correlation of these enzyme levels
and salt tolerance exists (Gossett et al., 1994; Hernandez
et al., 1995, 2000; Sehmer et al., 1995; Kennedy and De
Fillippis, 1999; Sreenivasulu et al., 2000; Benavides et
al., 2000; Lee et al., 2001; Mittova et al., 2002, 2003). In
soybean root nodules ascorbate peroxidase, catalase,
and glutathione reductase activities decrease under salt
stress, while superoxide dismutase and reduced glutathione increase and malondialdehyde and total protein
remain unchanged (Comba et al., 1998).
Transgenic plants have been generated to probe the
effects of ROS scavenging on salinity stress tolerance,
based on observations of gene expression changes in
salt-stressed plants. A putative phospholipid hydroperoxide glutathione peroxidase (PHGPX) transcript increases during salt stress in Arabidopsis and citrus
(Gueta-Dahan et al., 1997; Sugimoto and Sakamoto,
1997); also in citrus, transcripts and enzyme activities of
Cu/Zn-SOD, glutathione peroxidase, and cytosolic APX
increase (Holland et al., 1993; Gueta-Dahan et al.,
1997). Catalase-decient (antisense) tobacco shows
enhanced sensitivity to oxidative stress under conditions
of light and salinity (Willkens et al., 1997). ROS
scavenging as an important component of abiotic stress
responses is documented by mutant analysis. The
ascorbic-acid-decient Arabidopsis semidominant soz1
accumulates only 30% of ascorbate compared with wild
type, and plants show signicantly higher sensitivity to
oxidative stress conditions (Conklin et al., 1996).
Further support comes from the study of transgenic
models, which have been generated to study antioxidant
defenses (Orr and Sohal, 1992; Creissen et al., 1996;
Allen et al., 1997; Noctor and Foyer, 1998; Smirnoff,
1998). Overexpression of genes leading to increased
amounts and activities of mitochondrial Mn-SOD, FeSOD, chloroplastic Cu/Zn-SOD, bacterial catalase, and
glutathione-S-transferase (GST)/glutathione peroxidase
(GPX) can increase the performance of plants under
stress (Bowler et al., 1991; Gupta et al., 1993a, b; Van
Camp et al., 1996; Shikanai et al., 1998; Roxas et al.,
2000). A cDNA clone encoding a cytosolic SOD has
been isolated from a cDNA library constructed from
poly(A)+ RNA from epicotyls of 5-day-old Cicer
arietinum, L. etiolated seedlings after a differential
screening to select clones whose expression decreases
331
with epicotyl growth (Hernandez et al., 2002). Analysis

of its deduced amino acid sequence shows all the typical
structural motifs of plant cytosolic SODs (EC 1.15.1.1.).
The expression of this clone is always higher in young
and growing tissues than in old and storage tissues and
diminishes throughout the development of the seedlings.
Cytosolic Cu/Zn-SOD activity is also higher in radicles
and younger internodes. Under stress conditions only
cold increases the gene expression whereas the activity is
clearly increased by a saline medium (Hernandez et al.,
2002). To analyze the potential of the active oxygenscavenging system of the cytosol in leaves of saltstressed mangrove B. gymnorrhiza, Takemura et al.
(2002) have isolated a full-length cDNA encoding a 153amino-acid sequence of cytosolic Cu/Zn-SOD and a
partial cDNA encoding catalase. Northern blot analyses
show that the transcript level of cytosolic Cu/Zn-SOD
increases after 1 and 5 days of NaCl treatment, but no
signicant change occurs in the expression of the
catalase gene. The transcript of cytosolic Cu/Zn-SOD
is also induced by mannitol treatment. This suggests
that the increase in cytosolic Cu/Zn-SOD 1 day after
NaCl treatment is a response to osmotic stress.
After 5 days of treatment with NaCl, the transcript
level of cytosolic Cu/Zn-SOD increases in young and
mature leaves but not in old leaves. Expression of the
cytosolic Cu/Zn-SOD gene is induced by exogenous
abscisic acid, while the catalase gene is induced by
application of 2-chloroethylphosphonic acid, which is a
generator of ethylene. The results from this study
suggest that salt stress leads to the generation of
superoxide in the cytosol and that the oxygen-scavenging system in the cytosol contributes to the salt
tolerance capacity of B. gymnorrhiza (Takemura et al.,
2002).
2.5. Induction of plant hormones
High salt concentration triggers an increase in levels
of plant hormones such as ABA and cytokinins
(Thomas et al., 1992; Aldesuquy, 1998; Vaidyanathan
et al., 1999). Abscisic acid is responsible for the
alteration of salt-stress-induced genes (de Bruxelles et
al., 1996). ABA-inducible genes are predicted to play an
important role in the mechanism of salt tolerance in rice
(Gupta et al., 1998). Salt stress results in increased levels
of ABA, aminocyclopropane-1-carboxylic acid, and
ethylene production in Citrus sinensis (GomezCadenas
et al., 1998). ABA has been found to alleviate the
inhibitory effect of NaCl on photosynthesis, growth and
translocation of assimilates (Popova et al., 1995). ABA
also promotes switch from C3 to crassulacean acid
metabolism (CAM) in Mesembryanthemum crystallinum
under salt stress (Thomas et al., 1992). ABA promotes
stomatal closure by rapidly altering ion uxes in guard
cells under stress conditions. Other ABA actions involve
ARTICLE IN PRESS
332
modications of gene expression, and the analysis of

ABA-responsive promoters has revealed diversity of
potential cis-acting regulatory elements. The nature of
the ABA receptors(s) remains unknown. In contrast,
combined biophysical, genetic, and molecular approaches have led to considerable progress in the
characterization of more downstream signaling elements. In particular, substantial evidence points to the
importance of reversible protein phosphorylation and
modication of cytosolic calcium levels and pH as
intermediates in ABA signal transduction (Leung and
Giraudat, 1998). Experimental evidence shows that the
increase of Ca2+ uptake is associated with the rise of
ABA under salt stress and thus contributes to membrane integrity maintainance, which enables plants to
regulate uptake and transport under high levels of
external salinity in the longer term (Chen et al., 2001). It
has been reported that ABA reduces ethylene release
and leaf abscission under salt stress in citrus probably by
decreasing the accumulation of toxic Cl ions in leaves
(GomezCadenas et al., 2002). Salt tolerance of facultatively halophytic Lophopyrum elongatum and the closely
related but less salt tolerant wheat T. aestivum L. is
enhanced when plants are allowed to gradually acclimate to salt stress in comparison to when they are
suddenly shocked (Noaman et al., 2002). This acclimation to salt stress is regulated by ABA; a pretreatment
with ABA substitutes for the acclimation and increases
tolerance of salt shock. The ABA-induced acclimation is
rapid and coincides with enhanced expression of the
early salt induced (ESI) genes in the roots. L. elongatum
tolerates salt shock better than wheat and its genome
confers greater tolerance of salt shock in their
amphiploid than wheat. The tolerance of salt shock is
principally controlled by chromosome 3E in the
L. elongatum genome. Wheat homologous chromosomes 3A and 3D also control salt shock response. It
is speculated that chromosome 3 in both species
mediates salt shock response via ABA (Noaman et al.,
2002).
Jasmonates also have important roles in salt tolerance. Experimental evidence shows that salt-tolerant
tomato cultivars have higher levels of jasmonates than
salt-sensitive cultivars (Hilda et al., 2003). Jasmonates
are generally considered to mediate signaling, such as
defense responses, owering, and senescence. However,
factors involved in the jasmonate signal-transduction
pathway remain unclear. To clarify the functions and
signaling mechanisms of jasmonates on a genomewide
level, Sasaki et al. (2000) have adopted a cDNA
macroarray technique. By analyzing the data from the
cDNA macroarray, many function-known and -unknown genes have been identied as MeJA-responsive
genes, and the proles of expression show good
agreement with Northern blot analysis (Sasaki et al.,
2000).
2.6. Change in photosynthetic pathway

Salt stress inhibits photosynthesis by reducing water
potential. So the main aim of salt tolerance is to increase
water use efciency under salinity. To this end,
facultative halophytic plants such as M. crystallinum
shift their C3 mode of photosynthesis to CAM (Cushman et al., 1989). This change allows the plant to reduce
water loss by opening stomata at night, thus decreasing
transpiratory water loss under prolonged salinity conditions. There is also a shift from the C3 to the C4
pathway in response to salinity in salt-tolerant plant
species such as Atriplex lentiformis (Zhu and Meinzer,
1999).
2.7. Molecular mechanism of salt tolerance
Physiologic or metabolic adaptations to salt stress at
the cellular level are the main responses amenable to
molecular analysis and have led to the identication of a
large number of genes induced by salt (Ingram and
Bartels, 1996; Bray, 1997; Shinozaki et al., 1998).
Selective examples of genes/proteins induced by salt
stress are given in Table 2. These genes can be classied
in functional groups (Table 3) related to their physiologic or metabolic function predicted from sequence
homology with known proteins. Salt tolerance is a
multigenic trait and a number of genes categorized into
different functional groups are responsible for encoding
salt-stress proteins: (i) genes for photosynthetic enzymes, (ii) genes for synthesis of compatible solutes, (iii)
genes for vacuolar-sequestering enzymes, and (iv) genes
for radical-scavenging enzymes. Most of the genes in the
functional groups have been identied as salt inducible
under stress conditions. Other genes have been detected
by a salt-hypersensitivity assay in Arabidopsis, which led
to the identication of mutants in potassium uptake as
being critical in salt sensitivity (Wu et al., 1996).
However, other physiological systems may be equally
limiting under stress conditions and mutants in these
physiological pathways could lead to increased salt
toxicity and would affect survival in a negative manner.
Transcript regulation in response to high salinity has
been investigated for salt-tolerant rice (var Pokkali) with
microarrays including 1728 cDNAs from libraries of
salt-stressed roots (Kawasaki et al., 2001). NaCl at
150 mM reduces photosynthesis to one-tenth of the prestress value within minutes. Hybridizations of RNA to
microarray slides were probed for changes in transcripts
from 15 min to 1 week after salt shock. Beginning 15 min
after the shock, Pokkali shows up-regulation of
transcripts. Approximately 10% of the transcripts in
Pokkali are signicantly up- or down-regulated within
1 h of salt stress. The initial differences between control
and stressed plants continue for hours but become less
pronounced as the plants adapted over time. The
Table 2
Selective examples of genes/proteins induced by salt stress
Characteristic feature(s)
Reference
Arabidopsis thaliana
Sal 1
Quintero et al. (1996)
Brassica napus
Bnd 22
Citrus cinensis
Dunaliella salina
Hordeum ulgare
Salt associated 23 to 25 kDa protein

P 150
26 and 27 kDa proteins (salt-induced
polypeptides SIP S1S4)
hva 1
TAS-12
le-16 gene
ppc-1 and ppc-2
Induced by salt stress, overexpression in Arabidopsis or yeast overcomes

Na+ and Li+ toxicity, homologous to hal 1 of yeast
22 kDa protein, level increased by progessive or rapid water stress and
salinity
Induced by salt stress, ABA, and water stress
150 kDa protein, induced by salt stress, de novo synthesized protein
Salt stress induced S1S4 polypeptides but water decit did not induce S2
polypeptides
Induced by ABA, drought, NaCl, cold, and heat treatment
Salt and water stress induced lipid transfer protein
Induced by drought, PEG, salinity, cold, and heat stress
Encodes PEP carboxylase, induced by salt and water stress, exogenous
ABA is a poor substitute for NaCl to induce it
Lycopersicom esculantum
Mesembryanthemum
crystallinum
Isogenes
lmt 1
Inps 1
Nicotiana tabacum
26- and 43-kDa polypeptides

58-, 37-, 35.5-, 34-, 26-, 21-, 19.5-, and
18-kDa polypeptides
30-kDa polypeptide
Vitronectin and bronectin-like
proteins
Osmotin
O. sativa
RAB21
salT
em
Reviron et al. (1992)

Benhayyim et al. (1993)
Sadaka et al. (1991)
Hurkman and Tanaka (1988)
Hong et al. (1992)
Torres-Schumann et al. (1992)
Plant et al. (1991)
Cushman et al. (1989)
Encodes myo-inositol o-methyl transferase 1; induced by NaCl and

osmotic stress
Encodes myo-inositol 1-phosphate synthase; shows signicant
homology to corresponding genes in plants and yeast
Levels increase in both NaCl, and PEG-induced water stress adapted
cells but are not detected in unadapted
Increased levels with increased NaCl tolerance
Vernon and Bohnert (1992)
Heat shock at 38 1C induces cross tolerance to salt stress

Found in membranes and cell wall of NaCl-adapted cells
Harrington and Alm (1988)

Zhu et al. (1993)
26-kDa protein, protein level enhanced in both NaCl- and PEG-induced

water stress adapted cells but not in unadapted cells
Induced when plants are subjected to water stress, rab21 mRNA and
protein accumulate in rice embryos, leaves, roots, and callus derived
suspension cells upon treatment with NaCl and/or ABA
mRNA accumulates rapidly in shoots and roots of mature seedlings
with ABA salts, PEG, NaCl, and KCl; no induction in leaf lamina
Induced by ABA and salt stress, salt interacts synergistically with ABA
Singh et al. (1987)
Ishitani et al. (1996)

Singh et al. (1985)
Singh et al. (1985)
Mundy et al. (1990)
Claes et al. (1990)

Bostock and Quatrano (1992)
The names of various genes and proteins have been by and large reproduced here as per the original publications of the authors.
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Salt responsive genes/proteins
Plant species
333
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334
Table 3
Functional groups of genes/proteins activated in salt stress with
potential for providing tolerance (reproduced from Winicov, 1998)
Table 4
Differences between halophytes and glycophytes with respect to salt
tolerance mechanism
1
2
3
4
5
6
7
8
9
Halophytes
Glycophytes
1.
1. Higher.
Carbon metabolism and energy production/photosynthesis

Cell wall/membrane structural components
Water channel proteins
Ion transport
Oxidative stress defenses
Detoxifying enzymes
Proteinases
Proteins involved in signaling
Transcription factors
2.
3.
4.
5.
6.
interpretation of an adaptive process is supported by the

similar analysis of salinity-sensitive rice (var IR29), in
which the immediate response exhibited by Pokkali is
delayed and later results in down-regulation of transcription and death. The up-regulated functions observed with Pokkali at different time points during stress
adaptation change over time. Increased protein synthesis and protein turnover are observed at early time
points, followed by the induction of known stressresponsive transcripts within hours and the induction of
transcripts for defense-related functions later. After 1
week, the nature of up-regulated transcripts (e.g.,
aquaporins) indicates recovery (Kawasaki et al., 2001).
Acclimation of microorganisms to environmental
stress is closely related to the expression of various
genes (Kanesaki et al., 2002). It has been reported that
salt stress and hyperosmotic stress have different effects
on the cytoplasmic volume and gene expression in
Synechocystis sp. PCC 6803 (Kanesaki et al., 2002).
DNA microarray analysis indicates that salt stress
strongly induces the genes for some ribosomal proteins.
Hyperosmotic stress strongly induces the genes for 3ketoacyl-acyl carrier protein reductase and rare lipoprotein A. Genes whose expression is induced both by
salt stress and by hyperosmotic stress include those for
heat shock proteins and the enzymes for the synthesis of
glucosylglycerol. It has also been reported by Kanesaki
et al. (2002) that each kind of stress induces a number of
genes for proteins of unknown function. Findings of
Kanesaki et al. (2002) suggests that Synechocystis sp.
recognizes salt stress and hyperosmotic stress as
different stimuli, although mechanisms common to the
responses to each form of stress might also contribute to
gene expression.
2.8. Salinity effect: halophytes vs. glycophytes
The salt tolerance mechanism is a multigenic trait and
therefore biochemical pathways leading to products or
processes that improve salt tolerance are likely to act
additively and probably synergistically. So the advantage of halophytes over glycophytes can be through
more efcient performance of a new basic biochemical
Salinity has a smaller effect

upon the extent to which
stomata limit photosynthesis.
High water use efciency.
Low internal CO2
concentration.
Low light saturated
photosynthetic rate.
Efcient accumulating solutes.
Low level of Na+ and Cl ions
in the cytoplasm and
chloroplast.
2. Comparatively less.
3. Comparatively less.
4. It is less.
5. Less efcient.
6. It is higher.
tolerance mechanism. Table 4 summarizes differences in

halophytes and glycophytes with respect to salt tolerance mechanism.
3. Salinity effects on plants

Salinity of soil and water is caused by the presence of
excessive amounts of salts. Most commonly, high Na+
and Cl cause the salt stress. Salt stress has threefold
effects; viz. it reduces water potential and causes ion
imbalance or disturbances in ion homeostasis and
toxicity. This altered water status leads to initial growth
reduction and limitation of plant productivity. Since salt
stress involves both osmotic and ionic stress (Hagemann
and Erdmann, 1997; Hayashi and Murata, 1998),
growth suppression is directly related to total concentration of soluble salts or osmotic potential of soil water
(Flowers et al., 1977; Greenway and Munns, 1980). The
detrimental effect is observed at the whole-plant level as
death of plants or decrease in productivity. Suppression
of growth occurs in all plants, but their tolerance levels
and rates of growth reduction at lethal concentrations of
salt vary widely among different plant species. Although
the change in water status is the cause of growth
suppression, the contribution of subsequent processes to
inhibition of cell division and expansion and acceleration of cell death has not been well documented
(Hasegawa et al., 2000). Salt stress affects all the major
processes such as growth, photosynthesis, protein
synthesis, and energy and lipid metabolism. These are
discussed under separate headings.
3.1. Effects of salinity on growth
Salinity stress results in a clear stunting of plants
(Hernandez et al., 1995; Cherian et al., 1999; Takemura
et al., 2000). The immediate response of salt stress is
reduction in the rate of leaf surface expansion leading to
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cessation of expansion as salt concentration increases

(Wang and Nil, 2000). Salt stress also results in a
considerable decrease in the fresh and dry weights of
leaves, stems, and roots (Hernandez et al., 1995;
AliDinar et al., 1999; Chartzoulakis and Klapaki,
2000). The optimum growth of plants is obtained at
50% seawater and declines with further increases in
salinity in Rhizophora mucronata (Aziz and Khan, 2001).
Fresh and dry weights of plants increase with an
increase in salinity in Salicornia rubra while the optimal
growth occurrs at 200 mM NaCl and the growth
declines with a further increase in salinity (Khan,
2001). In Raphanus sativus (radish) total plant dry
weight decreases at higher salinities and about 80% of
the growth reduction at high salinity can be attributed to
reduction of leaf area expansion and hence to reduction
of light interception. The remaining 20% of the salinity
effect on growth is most likely explained by a decrease in
stomatal conductance. The small leaf area at high
salinity is related to a reduced specic leaf area and
increased tuber/shoot weight ratio and the latter can be
attributed to tuber formation starting at a smaller plant
size at high salinity (Marcelis and VanHooijdonk, 1999).
Kurban et al. (1999) have reported that in Alhagi
pseudoalhagi (a leguminous plant), total plant weight
increases at low salinity (50 mM NaCl) but decreases at
high salinity (100 and 200 mM NaCl). Khan et al. (1999)
have reported that when Halopyrum mucronatum (a
perennial grass found on the coastal dunes of Karachi,
Pakistan) is treated with 0, 90, 180, and 360 mM NaCl in
sand culture, fresh and dry mass of roots and shoots
peaks at 90 mM NaCl, a further increase in salinity
inhibits plant growth, ultimately resulting in plant death
at 360 mM NaCl, and maximum succulence is noted at
90 mM NaCl. Experimental evidence shows that in a salt
nonsecretor mangrove B. parviflora the plant growth is
optimal at 100 mM NaCl under hydroponic culture,
whereas further increase in NaCl concentration retards
plant growth (Table 5) and 500 mM NaCl is found to be
lethal in this species (Parida et al., 2004a). On the other
hand a salt secretor mangrove Aegiceras corniculatum
can tolerate upto 250 mM NaCl and 300 mM is found
lethal in this case (Mishra and Das, 2003). Increasing
salinity is accompanied by signicant reductions in
335
shoot weight, plant height, number of leaves per plant,

root length, and root surface area per plant in tomato
(Mohammad et al., 1998). Increased NaCl levels results
in a signicant decrease in root, shoot, and leaf growth
biomass and increase in root/shoot ratio in cotton
(Meloni et al., 2001).
3.2. Effects of salinity on water relations
Water potential and osmotic potential of plants
become more negative with an increase in salinity,
whereas turgor pressure increases with increasing
salinity (Morales et al., 1998; Hernandez et al., 1999;
Khan et al., 1999; Meloni et al., 2001; Khan, 2001;
Romeroaranda et al., 2001). Leaf water and osmotic
potentials and xylem tension increase with an increase in
media salinity in R. mucronata (Aziz and Khan, 2001).
Leaf osmotic potentials decrease with increases in NaCl
in Chrysanthemum and sea aster (Matsumura et al.,
1998). Relative water content, leaf water potential,
water uptake, transpiration rate, water retention, and
water use efciency decrease under short-term NaCl
stress in jute (Chaudhuri and Choudhuri, 1997). Water
potential, osmotic potential, and stomatal conductance
become more negative with an increase in salinity, while
pressure potential decreases with increasing salinity in
the halophytic perennial grass Urochondra setulosa
(Trip.) (Gulzar et al., 2003). With increasing salt
concentration, leaf water potential and evaporation rate
decrease signicantly in the halophyte S. salsa while
there are no changes in leaf relative water content (Lu et
al., 2002). Leaf water potential and osmotic potential
decline depending on the osmotic potential of the
rooting medium and the mode of stress imposition. A
greater decline in osmotic potential compared with the
total water potential led to turgor maintenance in plants
under progressive or prolonged NaCl stress (Rajasekaran et al., 2001).
3.3. Effects of salinity on leaf anatomy
Salinity causes increases in epidermal thickness,
mesophyll thickness, palisade cell length, palisade
diameter, and spongy cell diameter in leaves of bean,
Table 5
Growth of B. parviflora after 45 days in nutrient solution containing 0400 mM NaCl
[NaCl] (mM)
Plant height
(cm/plant)
Leaf area (cm2/

plant)
Fresh matter of
plant (g/plant)
Dry matter of
plant (g/plant)
Water content per unit leaf

area (gm2)
0
100
200
400
24.070.62a
25.570.82a
23.270.55a
22.570.91a
54.970.35a
58.970.90b
46.270.62c
44.670.55c
8.3870.51a
8.7270.35a
8.1170.25a
7.0270.20a
1.9470.05a
2.0470.04a
1.7770.04a
1.3470.05a
301.175.51a
302.072.70a
319.372.35b
324.471.85c
Values are mean7SE of three independent experiments. Different letters next to values indicate statistically different means at Pp0:05 (Source:
Parida et al., 2004a).
ARTICLE IN PRESS
336
cotton, and Atriplex (Longstreth and Nobel, 1979). In

contrast both epidermal and mesophyll thickness and
intercellular spaces decrease signicantly in NaCltreated leaves of the mangrove B. parviflora (Parida et
al., 2004a). Salinity also reduces intercellular spaces in
leaves (Delphine et al., 1998). Salt stress causes (1)
vacuolation development and partial swelling of endoplasmic reticulum, (2) decrease in mitochondrial
cristase and swelling of mitochondria, (3) vesiculation
and fragmentation of tonoplast, and (4) degradation of
cytoplasm by the mixture of cytoplasmic and vacuolar
matrices in leaves of sweet potato (Mitsuya et al., 2000)
(Fig. 4). In leaves of potato salt stress causes rounding of
cells, smaller intercellular spaces, and a reduction in
chloroplast number (Bruns and HechtBuchholz, 1990).
In tomato plants salinity causes reduction of plant leaf
area and stomatal density (Romeroaranda et al., 2001).
3.4. Effects of salinity on photosynthetic pigments and

proteins
The chlorophyll and total carotenoid contents of
leaves decrease in general under salt stress. The oldest
leaves start to develop chlorosis and fall with prolonged
period of salt stress (Hernandez et al., 1995, 1999;
Gadallah, 1999; Agastian et al., 2000). However, Wang
and Nil (2000) have reported that chlorophyll content
increases under conditions of salinity in Amaranthus. In
Grevilea, protochlorophyll, chlorophylls, and carote-
Fig. 4. Effects of NaCl stress on polyphenol level in B. parviflora

measured as a function of days of NaCl treatment. Values are
mean7SE (from Parida et al., 2002).
noids are signicantly reduced under NaCl stress, but

the rate of decline of protochlorophyll and chlorophyll
is greater than that of Chl-a and carotenoids. The
anthocyanin pigments on the other hand signicantly
increase in this case with salt stress (Kennedy and De
Fillippis, 1999). In leaves of tomato, the contents of
total chlorophyll (Chl-a+b), Chl-a, and b carotene
decrease by NaCl stress (Khavarinejad and Mosto,
1998). Under salinity stress, leaf pigments studied in
nine genotypes of rice reduce in general, but relatively
high pigment levels are found in six genotypes (Alamgir
and Ali, 1999). In the cyanobacterium Spirulina platensis
a decrease in the phycocyanin/chlorophyll ratio and no
signicant change in the carotenoid/chlorophyll ratio
are observed under salt stress (Lu and Vonshak, 1999).
Salinity causes signicant decreases in Chl-a, Chl-b, and
carotenoid in leaves of B. parviflora (Table 6; Parida et
al., 2002).
Soluble protein contents of leaves decrease in
response to salinity (Alamgir and Ali, 1999; Gadallah,
1999; Wang and Nil, 2000; Muthukumarasamy et al.,
2000; Parida et al., 2002). Agastian et al. (2000) have
reported that soluble protein increases at low salinity
and decreases at high salinity in mulberry. In Rhizobium
certain outer membrane proteins of molecular weight
22, 38, 40, 42, 62, and 68 kDa markedly decrease in the
presence of salt (Unni and Rao, 2001). SDSPAGE
analysis of proteins in peanut (Arachis hypogaea L.)
reveals that plants grown under NaCl show induction
(127 and 52 kDa) or repression (260 and 38 kDa) in the
synthesis of a few polypeptides (Hassanein, 1999).
Salinity induces six new proteins in roots of barley,
which are of low molecular weight, 24 to 27 kDa, with
an isoelectric point of 6.1 to 7.6. In contrast to roots, ve
new shoot proteins are induced whose molecular weights
and isoelectric points fall within the range of 2024 kDa
and 6.37.2, respectively. In addition, salinity also
inhibits the synthesis of a majority of shoot proteins
(Ramagopal, 1987). In radish (R. sativus L.) salt stress
causes accumulation of a 22-kDa protein (pI of 7.5) and
its mRNA in the leaves (Lopez et al., 1994). A
signicant increase in the amount of a protein, whose
migration in two-dimensional (2D) gel electrophoresis
corresponds to an apparent molecular weight of
2325 kDa and a pI of 6.1, is observed under NaCl
stress in cultured cells derived from Shamuti orange
Table 6
Effects of NaCl stress on photosynthetic pigments in leaves of B. parviflora
[NaCl] (mM)
Chl a (mg cm2)
Chl b (mg cm2)
Total Chl
Chl a/b
Total carotenoids (mg cm2)
0
100
200
400
65.4871.2
67.9971.6
40.0671.0
35.5371.3
17.9671.1
20.6571.8
12.0671.3
11.0371.4
83.4471.8
88.6471.5
52.1271.4
46.5671.1
3.64
3.29
3.32
3.20
23.2071.5
23.6571.4
16.5571.1
13.6871.0
4th pair of leaves from shoot top were sampled after 45 days NaCl treatment. The values are mean7SE (n 6) (Source: Parida et al., 2004a).
ARTICLE IN PRESS
(Citrus sinensis L. Osbeck) ovular callus cells (Benhayyim et al., 1993). Yen et al. (1997) have reported the
accumulation of ve polypeptides with estimated
molecular masses of 40, 34, 32, 29, and 14 kDa by
SDS and 2D-PAGE in calli of M. crystallinum under
NaCl stress and these polypeptides are classied into
two distinct groups according to their course of
induction: early responsive (40-, 34-, and 29-kDa) and
late responsive (32- and 14-kDa) proteins. The disappearance of a 60-kDa polypeptide in response to salinity
has been observed in Prosopsis (Munoz et al., 1997). In
wheat, the content of a 26-kDa protein increases in
NaCl-treated plants, stimulation is more pronounced in
roots than in shoots, and, in contrast, the contents of 13and 20-kDa proteins decrease and the 24-kDa protein
disappears with NaCl treatment (Elshintinawy and
Elshourbagy, 2001). NaCl induces accumulation of four
polypeptides with molecular masses of 61, 51, 39, and
29 kDa in maize roots (Tamas et al., 2001). Fractionation of cells followed by SDSPAGE and 2D-PAGE
reveals an increase in the levels of membrane proteins of
39 and 50 kDa and a decrease in the level of a membrane
protein of 52 kDa with increasing levels of external
NaCl in Rhodobacter sphaeroides. The proteins have
been isolated and sequenced, the polypeptide of 50 kDa
in the inner membrane is assigned to an ATP synthase
beta chain and that of 52 kDa in the outer membrane to
a agellar lament protein, and, as the N terminus of the
39 kDa protein in the outer membrane is blocked,
partial proteolysis was carried out and four peptides
were sequenced. Each sequence exhibits no signicant
homology with those available in databases, suggesting
that the polypeptide of 39 kDa (named SspA) is a novel
salt-stress-induced protein (Xu et al., 2001). It has been
reported that salinity causes a decrease in intensity of
several protein bands of molecular weight 17, 23, 32, 33,
and 34 kDa in B. parviflora (Parida et al., 2004b) and the
degree of decrease of these protein bands seems to be
roughly proportional to the external NaCl concentration. The most obvious change concerns a 23-kDa
polypeptide, which disappears after 45 days of treatment
in 400 mM NaCl (Fig. 2). Moreover, the 23-kDa
polypeptide, which disappears in B. parviflora under
salinity stress, reappears when these salinized seedlings
are desalinized (Fig. 2) and these observations suggest
the possible involvement of these polypeptides for
osmotic adjustment under salt stress in this species
(Parida et al., 2004c).
3.5. Effects of salinity on lipids
Lipids are the most effective sources of storage
energy, they function as insulators of delicate internal
organs and hormones, and they play important roles as
the structural constituents of most of the cellular
membranes (Singh et al., 2002). They also have vital
337
roles in the tolerance to several physiological stressors in

a variety of organisms including cyanobacteria. The
mechanism of desiccation tolerance relies on phospholipid bilayers, which are stabilized during water stress by
sugars, especially by trehalose. Unsaturation of fatty
acids also counteracts water or salt stress. Hydrogen
atoms adjacent to olenic bonds are susceptible to
oxidative attack. Lipids are rich in these bonds and are a
primary target for oxidative reactions. Lipid oxidation is
problematic as enzymes do not control many oxidative
chemical reactions and some of the products of the
attack are highly reactive species that modify proteins
and DNA (Singh et al., 2002). The lipid content in
peanut (A. hypogaea L.) increases at low concentration
of NaCl (up to 45 mM) and decreases at higher
concentrations (Hassanein, 1999). Wu et al. (1998) have
analyzed the changes in lipid composition by NaCl
stress in root plasma membrane of salt marsh grass
(Spartina patens) and reported that molar percentages of
sterols (including free sterols) and phospholipid decreases with increasing salinity, but the sterol/phospholipid ratio is unaffected by NaCl. However, glycolipid
shows a statistically signicant increase in the total lipid
as salinity in the medium is increased and the content of
plasma membrane phosphatidylcholine (PC) and phosphatidylethalomine (PE) decrease by salinity, but the
PC/PE ratios are not affected by salinity. Plasma
membrane vesicles isolated from calli of tomato tolerant
to 100 mM NaCl exhibit higher phospholipid and sterol
content and lower phospholipid/free sterol ratio and
lower double bond index of phospholipid fatty acids
(Kerkeb et al., 2001).
3.6. Effects of salinity on ion levels
High salt (NaCl) uptake competes with the uptake of
other nutrient ions, especially K+, leading to K+
deciency. Increased treatment of NaCl induces increase
in Na+ and Cl and decrease in Ca2+, K+, and Mg2+
levels in a number of plants (Khan et al., 1999, 2000a;
Khan, 2001). Salinity enhances the content of Na+,
Ca2+, and Cl in Vicia faba and the ratio of K+/Na+
decreases (Gadallah, 1999). In A. pseudoalhagi (a
leguminous plant), the leaf Na+ concentration in
200 mM NaCl-treated plants increases to 45 times that
of the control and the plants do not die but continue to
grow at such a high leaf Na+ concentration (Kurban et
al., 1999). In Ulva fasciata, a marine green macro alga,
the contents of Na+, K+, and Cl accumulate linearly
with increasing salinity. An increase in Na+ and Cl
content induces proline accumulation but decreases
both the activity of proline dehydrogenase (PDH EC
1.4.3.1; a catabolic enzyme of proline) and the total
and water-soluble Ca2+ contents. These results suggest
that in U. fasciata a loss of cellular Ca2+ is associated
with NaCl induction of proline accumulation via
ARTICLE IN PRESS
338
Table 7
Effects of salt stress on ion levels in leaves, stems, and root of B. parviflora treated with different concentrations of NaCl for a period of 45 days
Plant parts
[NaCl] (mM)
Na
Ca
Mg
Fe
Cu
Mn
Cl
Leaf
0
100
200
400
14.4770.7
33.5470.3
38.6370.4
42.1370.2
11.0270.1
12.2670.7
10.8370.6
11.8170.2
12.3170.3
11.4170.2
9.9970.5
7.8170.6
155.9471.9
162.4971.6
145.4671.2
117.1471.4
325.2171.4
309.0771.8
254.1171.5
295.7571.3
31.5070.3
28.5070.2
20.4170.5
18.3770.64
103.1071.6
97.4170.8
53.0670.6
7.1070.6
13.1170.1
38.5370.6
40.2170.4
43.4970.4
Stem
0
100
200
400
9.4870.5
15.8170.7
16.7070.1
21.6770.2
6.0070.5
7.8670.7
3.8170.3
2.7170.2
2.4970.9
2.9170.6
2.2670.7
3.6370.5
65.4170.7
61.5470.3
88.3470.5
298.4170.3
137.171.8
187.070.8
190.570.5
220.471.5
4.3570.7
5.6970.3
2.3970.5
1.4870.9
17.0570.9
21.0770.4
14.0170.7
12.6370.5
7.2870.1
21.9170.3
26.7070.6
38.5470.8
Root
0
100
200
400
7.2170.5
14.4770.3
17.2570.5
26.9670.8
25.4570.4
17.7870.1
15.0370.9
11.2070.5
2.7470.6
2.8970.3
2.4570.8
2.3870.3
205.6870.8
159.5570.4
142.8770.5
116.7870.6
632.171.8
970.971.1
383.970.9
277.870.6
65.9070.9
51.1070.5
28.1071.2
14.5270.7
28.4070.5
37.0070.5
33.0770.3
11.9670.7
6.8570.7
18.3770.3
24.9570.5
31.4770.3
Na, K, Ca, Mg, and Cl content are expressed as mg g d wt1, whereas Fe, Cu, and Mn content are expressed as mg g dwt1. Values are mean7S.E
(n 6) (Source: Parida et al., 2004a).
an inhibition of PDH activity (Lee and Liu, 1999).

Salinity stress causes an increase in levels of Na+ and
Cl in guava and the highest ion accumulation is found
in the leaves followed by the roots; the Ca2+ levels are
stable in the roots but decrease in stems and leaves and
the K+ content is reduced with increased levels of
salinity, particularly in the leaves. On the other hand,
Mg2+ levels are not affected by salinity in stems and
roots but decrease in the leaves of guava. There is a
positive relationship between Na+ and Cl and a
negative relationship between Na+ and K+ concentration in roots and leaves. Mg2+ concentration in leaves
and roots does not vary with the concentration of Na+,
and the concentration of Ca2+ does not vary with that
of Na2+ in the leaves but shows an inverse relationship
in the roots (Ferreira et al., 2001). We have reported a
signicant increase in Na+ and Cl content in leaves,
stem, and root of the mangrove B. parviflora (Table 7)
without any signicant alteration of the endogenous
level of K+ and Fe2+ in leaves (Parida et al., 2004a).
Decreases of Ca2+ and Mg2+ content of leaves have
also been reported upon salt accumulation in this
species, suggesting increasing membrane stability and
decreased chlorophyll content, respectively (Parida
et al., 2004a).
3.7. Effects of salinity on antioxidative enzymes and
antioxidants
Salt stress causes water decit as a result of osmotic
effects on a wide variety of metabolic activities of plants
and this water decit results in oxidative stress because
of the formation of reactive oxygen species such as
superoxides and hydroxy and peroxy radicals. The
reactive oxygen species that are by-products of hyperosmotic and ionic stresses cause membrane disfunction
and cell death (Bohnert and Jensen, 1996). The plants
defend against these reactive oxygen species by induction of activities of certain antioxidative enzymes such
as catalase, peroxidase, glutathione reductase, and
superoxide dismutase, which scavenge reactive oxygen
species. There are several reports of increasing activity
of antioxidative enzymes. Activities of antioxidative
enzymes such as ascorbate peroxidase, glutathione
reductase,
monodehydroascorbate
reductase
(MDHAR), dehydroascorbate reductase (DHAR), and
Mn-SOD increase under salt stress in wheat, while Cu/
Zn-SOD remains constant and total ascorbate and
glutathione content decrease (Hernandez et al., 2000). In
wheat, activities of APX, MDHAR, DHAR, and GR
increase in the shoots and decrease in the roots
(Meneguzzo and Navarilzzo, 1999). Gossett et al.
(1994) have reported that in cotton (Gossypium hirsutum
L.) NaCl stress increases the activities of SOD, guaicol
peroxidase, and glutathione reductase and decreases the
activities of catalase and ascorbate peroxidase. Salt
stress also causes decrease in total ascorbate, total
glutathione, and a-tocopherol levels in this case. In
leaves of rice plant, salt stress preferentially enhances the
content of H2O2 and the activities of SOD, APX, and
GPX, whereas it decreases catalase activity (Lee et al.,
2001). On the other hand, salt stress has little effect on
the activity levels of glutathione reductase (Lee et al.,
2001). Lechno et al. (1997) have reported that NaCl
treatment increases the activities of the antioxidative
enzymes catalase and glutathione reductase and the
content of the antioxidants ascorbic acid and reduced
glutathione but does not affect the activity of SOD in
cucumber plants. In radish NaCl stress decreases proline
oxidase activity and increases protease, gamma-glutamyl kinase, and ATPase activities (Muthukumarasamy
et al., 2000). SOD activity in plant leaves of barley and
H+ ATPase activity in plant roots increase by salinity,
whereas malondialdehyde (MDA) concentration in
ARTICLE IN PRESS
CAT (Umg-1 protein)
30
25
a
a
ab
c
20
15
0mM
100mM
200mM
400mM
10
5
0
0
APX (Umg-1 protein)
(A)
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
GR(U mg-1 protein)
14
21
30
0mM
100mM
200mM
400mM
45
b
b
a
a
(B)
0.5
0.45
0.4
0.35
0.3
0.25
0.2
0.15
0.1
0.05
0
14
21
30
45
c
b
a
a
0mM
100mM
200mM
400mM
14
21
30
45
Duration of exposure (days)
(C)
20
SOD(Umg-1 protein)
plant leaves decreases (Liang, 1999). The higher

lipoxygenase and antioxidant enzyme activities such as
SOD, catalase, ascorbate peroxidase, glutathione reductase, and GST are observed in tomato under NaCl
stress (RodriguezRosales et al., 1999). In Grevia
ilicifolia, the levels of MDA signicantly decline as a
result of salt exposure, and this is accompanied by
signicant increases in both acid protease and neutral
protease activities. Four other key enzymes involved in
oxdative stress as tissue degradation (catalase, polyphenol oxidase, SOD, and lypoxygenase) are also
signicantly increased as a result of NaCl treatment
(Kennedy and De Fillippis, 1999). Hernandez et al.
(1999) have reported that in pea (Pisum sativum cv.
Puget) higher concentrations of NaCl (110130 mM)
enhance the activities of cytosolic CuZn-SOD II,
chloroplastic CuZn-SOD II, and mitochondrial and/or
peroxisomal Mn-SOD. These inductions are matched by
increases in the activity of APX and MDHAR. The
activities of GR and DHAR are induced only under
severe NaCl stress (130160 mM) and are accompanied
by losses in the ascorbate and glutathione pools and
ASC/DHA and GSH/GSSG ratios and by increases in
GSSG (Hernandez et al., 1999). Salinity induces
enhancement of activities of the chloroplast form of Lmyo-inositol 1-phosphate synthase (EC 5.5.4.1) in rice
(Raychaudhuri and Majumder, 1996). Experimental
evidence shows that salinity causes increases in APX,
GPX, GR, and SOD activity and decreases in catalase
activity in leaves of B. parviflora (Fig. 5; Parida et al.,
2004c). A preferential enhancement of Mn-SOD has
also been reported in this species (Parida et al., 2004c).
The response of the chloroplastic antioxidant system of
the cultivated tomato L. esculentum (Lem) and the wild
salt-tolerant related species L. pennellii (Lpa) to NaCl
stress has been reported by Mittova et al. (2002). An
increase in H2O2 level and membrane lipid peroxidation
is observed in chloroplasts of salt-stressed Lem. In
contrast, a decrease in these indicators of oxidative
stress is characterized by chloroplasts of salt-stressed
Lpa plants. This differential response of Lem and Lpa to
salinity correlates with the activities of the antioxidative
enzymes in their chloroplasts. Increased activities of
total superoxide dismutase, ascorbate peroxidase,
MDHAR, GST, PHGPX, and several isoforms of
nonspecic peroxidases are found in chloroplasts of
salt-treated Lpa plants. In these chloroplasts, in
contrast, activity of lipoxygenase decreases while in
those of salt-stressed Lem it increases. Although total
SOD activity slightly increases in chloroplasts of salttreated Lem plants, differentiation between SOD types
reveals that only stromal Cu/Zn-SOD activity increases.
In contrast, in chloroplasts of salt-treated Lpa plants
Fe-SOD activity increases while Cu/Zn-SOD activity
remains unchange. These data indicate that the saltdependent oxidative stress and damage suffered by Lem
339
c
c
0mM
100mM
200mM
400mM
15
10
a
5
0
0
(D)
7
14
21
30
Duration of exposure (days)
45
Fig. 5. Effects of different concentrations of NaCl on activity of

catalase (A), ascorbate peroxidase (B), glutathione reductase (C), and
superoxide dismutase (D) in leaves of B. parviflora measured as
function of days of NaCl treatment. Enzyme activity is expressed as
unit per mg protein. Values are mean7SE. Different letters next to the
symbols indicate statistically different means as Pp0:01 (from Parida
et al., 2004b).
chloroplasts is effectively alleviated in Lpa chloroplasts

by the selective up-regulation of a set of antioxidative
enzymes (Mittova et al., 2002). The effects of salinity
(100 mM NaCl) and different nitrogen sources [NaNO3/
(NH4)2SO4] on the activities and spatial distributions of
antioxidative enzymes (glutathione reductase, superoxide dismutase, guaicol peroxidase, and catalase) and
GST have been investigated in maize and sunower
seedlings (RiosGonzalez et al., 2002). The antioxidant
ARTICLE IN PRESS
340
enzymes exhibit higher activities in salinity-treated

plants. Changes in antioxidant enzyme activities caused
by different N sources differ in the two species.
Ammonium-fed plants show higher CAT activity in
both plant species and higher GR activity in maize and
sunower leaves, with the highest GST activity in maize.
POD and SOD activities are lower in both maize and
sunower seedlings and lower GR activity has been
observed in maize roots. SOD and POD activities are
higher in the mature sections of the root than in the tips.
GR activity is higher in the younger parts of the nitratefed plant roots. The antioxidant enzyme activities are
higher in the cortex than in the stele of the nodal roots
(RiosGonzalez et al., 2002). The response of the
antioxidative systems of leaf cell mitochondria and
peroxisomes of the cultivated tomato L. esculentum and
the wild salt-tolerant related species L. pennellii to NaCl
stress has also been investigated (Mittova et al., 2003).
Salt-dependent oxidative stress is evident in Lem
mitochondria as indicated by their raised levels of lipid
peroxidation and H2O2 content whereas their reduced
ascorbate and reduced glutathione contents decrease.
Concomitantly, SOD activity decreases whereas APX
and GPX activities remain at control level. In contrast,
the mitochondria of salt-treated Lpa do not exhibit saltinduced oxidative stress. In their case salinity induces an
increase in the activities of superoxide dismutase,
ascorbate peroxidase, MDHAR, dehydroascorbate reductase, and glutathione-dependent peroxidase. Lpa
peroxisomes exhibit increased SOD, APX, MDHAR,
and catalase activity and their lipid peroxidation and
H2O2 levels are not affected by the salt treatment. The
activities of all these enzymes remain at control level in
peroxisomes of salt-treated Lem plants. The saltinduced increase in the antioxidant enzyme activities in
the Lpa plants confer cross-tolerance toward enhanced
mitochondrial and peroxisomal reactive oxygen species
production imposed by salicylhydroxamic acid and 3amino-1,2,4-triazole, respectively (Mittova et al., 2003).
3.8. Effects of salinity on nitrogen metabolism
Nitrate reductase activity (NRA) of leaves decreases
in many plants under salt stress (AbdElBaki et al., 2000;
Flores et al., 2000). The primary cause of a reduction of
NRA in the leaves is a specic effect associated with the
presence of Cl salts in the external medium. This effect
of Cl seems to be due to a reduction in NO
3 uptake
and consequently a lower NO
3 concentration in the
leaves, although a direct effect of Clon the activity of
the enzyme cannot be discarded (Cram, 1973; Smith,
1973; Deane-Drummond and Glauss, 1982; Flores et al.,
2000). In Zea mays the nitrate content of leaves
decreases, but it increases in roots under NaCl stress
and NRA of leaves also decreases under salinity
(AbdElBaki et al., 2000). Soussi et al. (1999) have
reported that salinity inhibits nitrogen xation by

reducing nodulation and nitrogenase activity in chickpea (C. arietinum L.). Considerable inhibition of
nodulation and N2 xation has also been reported by
other workers (Bekki et al., 1987). Severe salt stress
reduces the leg hemoglobinn content and nitrogenase
activity in soybean root nodules (Comba et al., 1998).
The exposure of nodulated roots of legumes such as
soybean, common bean, and alfalfa to NaCl results in a
rapid decrease in plant growth associated with a shortterm inhibition of both nodule growth and nitrogenase
activity (Serraz et al., 1998). Khan et al. (1998) have
reported that salinity inhibits nitrate content and uptake
and NRA in leaves of maize plants. Nitrogenase activity
measured with regard to acetylene reduction (C2H2)
decreases in common bean by short-term exposure to
salinity (Serraz et al., 2001). Decrease in NRA activity
and in total nitrogen and nitrate uptake have been
reported in leaves of B. parviflora (Parida and Das,
2004).
NADP-specic isocitrate dehydrogenase (ICDH) is a
key cytosolic enzyme that links C and N metabolism by
supplying C skeletons for primary N assimilation in
plants. The characterization of the transcript McICDH1 encoding an NADP-dependent isocitrate dehydrogenase (NADP-ICDH; EC 1.1.1.42) has been reported from the facultative halophyte M. crystallinum
L., focusing on salt-dependent regulation of the enzyme
(Popova et al., 2002). The activity of NADP-ICDH in
plants adapted to high salinity increases in leaves and
decreases in roots. By transcript analyses and Westerntype hybridizations, expression of Mc-ICDH1 is found
to be stimulated in leaves in salt-adapted M. crystallinum. By immunocytological analyses, NADP-ICDH
proteins are localized to most cell types with strongest
expression in epidermal cells and in the vascular tissue.
In leaves of salt-adapted plants, signal intensities
increases in mesophyll cells. In contrast to Mc-ICDH1,
the activity and transcript abundance of ferredoxindependent glutamate synthase (EC 1.4.7.1), which is the
key enzyme of N assimilation and biosynthesis of amino
acids, decreases in leaves in response to salt stress
(Popova et al., 2002).
3.9. Effects of salinity on malate metabolism
NADP-malate dehydrogenase (NADP-MDH; EC
1.1.1.82) is responsible for the reduction of oxaloacetate
to malate in the chloroplasts of higher plants. In M.
crystallinum, steady state transcript levels for chloroplast NADP-MDH decrease transiently in the leaves
after salt stress and then increase to levels greater than
two fold higher than levels in unstressed plants, whereas
transcript levels in roots are extremely low and are
unaffected by salt-stress treatment and the salt-stressinduced expression pattern of this enzyme suggests that
ARTICLE IN PRESS
3.10. Effects of salinity on chloroplast ultrastructure

Electron microscopy shows that the thylakoidal
structure of the chloroplasts becomes disorganized, the
number and size of plastoglobuli increases, and their
starch content decreases in plants treated with NaCl
(Hernandez et al., 1995, 1999). In the mesophyll of sweet
potato leaves, thylakoid membranes of chloroplast are
swollen and most are lost under severe salt stress
(Mitsuya et al., 2000). In potato, salt stress reduces the
numbers and depth of the grana stacks and causes a
swelling of the thylakoid and starch grains become
larger in the chloroplasts (Bruns and Hecht-Buchholz,
1990). In leaves of NaCl-treated plants of tomato the
transmission electron microscopy shows that the chloroplasts are aggregated, the cell membranes are distorted
and wrinkled, and there are no signs of grana or
thylakoid structures in chloroplasts (Khavarinejad and
Mosto, 1998). Chloroplast ultrastructural changes
under salt stress are apparent in Eucalyptus microcorys;
these include the presence of large starch grains, the
dilation of the thylakoid membranes, the near absence
of grana, and the presence of enlarged mesophyll cells
(Keiper et al., 1998). We have also reported a notable
disorganization of the thylakoid structure of chloroplasts in leaves of B. parviflora by salt stress (Parida et
al., 2003).
3.11. Mechanism of salinity effects on photosynthesis
Plant growth is the result of integrated and regulated
physiological processes. Physiological processes are
affected by number of environmental factors and they
determine the response of plants to stress. Limitation of
plant growth by environmental factors cannot be
assigned to a single physiological process. The dominant
physiological process is photosynthesis. Plant growth as
biomass production is a measure of net photosynthesis
and, therefore, environmental stresses affecting growth
also affect photosynthesis. Salt stress causes either shortor long-term effects on photosynthesis. The short-term
effect occurs after a few hours or within 1 or 2 days of
the onset of exposure and this response is important, as
there is complete cessation of carbon assimilation within

hours. The long-term effect occurs after several days of
exposure to salt and reduction in carbon assimilation is
due to the salt accumulation in developing leaves
(Munns and Termatt, 1986). Although there are reports
of suppression of photosynthesis upon salt stress
(Chaudhuri and Choudhuri, 1997; Soussi et al., 1998;
AliDinar et al., 1999; Romeroaranda et al., 2001; Kao et
al., 2001), there are also reports that photosynthesis is
not slowed down by salinity and is even stimulated by
low salt concentration (Rajesh et al., 1998; Kurban et
al., 1999). In A. pseudoalhagi (a leguminous plant), the
leaf CO2 assimilation rate increases at low salinity
(50 mM NaCl) but is not affected signicantly by
100 mM NaCl, while it is reduced to about 60% of the
control in 200 mM NaCl. Similarly stomatal conductance is consistent with the CO2 assimilation rate
regardless of the treatments, and intercellular CO2
concentration is lower in the NaCl-treated plants than
in the control (Kurban et al., 1999). In mulberry, net
CO2 assimilation rate (PN), stomatal conductance (gs),
and transpiration rate (E) decline under salt stress,
whereas intercellular CO2 concentration (Ci) increases
(Agastian et al., 2000). In B. parviflora net CO2 PN
increases at low salinity (mM) and decreases at high
salinity (Fig. 6), whereas gs remains the same as in
control at low salinity and decreases at high salinity
(Fig. 7) (Parida et al., 2004a). NaCl stress decreases the
chlorophyll content and net photosynthetic rate and
increases the rate of respiration and CO2 compensation
concentration and there are no signicant changes in the
carotenoid contents in leaves of alfalfa plants (Khavarinejad and Chaparzadeh, 1998). In A. lentiformis,
net CO2 assimilation rate and the ratio of ribulose
18
16
14
PN (molm-2 s-1)
it may participate in the CO2 xation pathway during

CAM (Cushman, 1993). When Eucalyptus citridora
plants are treated with NaCl, an increased Na+ level
is observed in shoots 3 weeks after treatment, and at this
stage of treatment the growth of plants is not reduced
but the malate metabolism is modied. The malate
content decreases in leaves while the specic activities of
NAD and NADP-malic enzymes increase. The stimulation in enzyme activity is more pronounced for NADPmalic enzyme but, for both enzymes, enzyme activity
diminishes as early as 5 weeks after treatment (DeAragao et al., 1997).
341
12
10
8
0 mM
100 mM
200 mM
2
400 mM
0
7
14
30
45
Duration of NaCl treatment (d)

Fig. 6. Effect of NaCl treatment on photosynthetic rate (PN) in B.
parviflora measured as a function of days of NaCl treatment. Values
are mean7SE (from Parida et al., 2004a).
ARTICLE IN PRESS
342
biphosphate carboxylase (Rubisco) activity to that of

phosphoenol pyruvate carboxylase (PEPC) decrease
under salinity because PEPC activity on a leaf area
basis increases linearly with salinity, while Rubisco
activity remains relatively constant (Zhu and Meinzer,
1999). In the cyanobacterium S. platensis salt stress
inhibits the apparent quantum efciency of photosynthesis and photosystem II (PSII) activity while stimulating
photosystem I (PSI) activity and dark respiration
signicantly. Salt stress also results in a decrease in
overall activity of the electron transport chain, which
cannot be restored by diphenyl carbazide, an articial
electron donor to PSII (Lu and Vonshak, 1999).
Experimental evidence shows that PSII mediated
electron transport activity increases at low salinity
(100 mM) and decreases at high salinity in B. parviflora
(Table 8; Parida et al., 2003). A signicant reduction in
CO2 assimilation rate and stomatal conductance by salt
treatment is registered in horsegram (Macrotyloma
800
700
gs (mmolm-2 s -1)
600
500
400
0 mM
300
100 mM
200
200 mM
100
400 mM
0
7
14
30
45
Duration of NaCl treatment (d)

Fig. 7. Effect of NaCl treatment on stomatal conductance (gs) in B.
parviflora measured as a function of days of NaCl treatment. Values
are mean7SE (from Parida et al., 2004a).
uniflorum) and salinity inhibits the photosynthetic electron transport and the activity of enzymes of the Calvin
cycle, ribulose-1,5-biphosphate carboxylase (E.C.4.1.1.39),
ribulose-5-phosphate kinase (E.C.2.7.1.19), ribulose-5phosphate isomerase (E.C.5.3.16), and NADP-glyceraldehyde-3-phosphate dehydrogenase (E.C.1.2.13) (Reddy et
al., 1992). In four cultivars of rice (Oryza sativa L.),
gradual decreases in the activities of PSI, PSII, and
chlorophyll uorescence transients and emission at 688 nm
are observed with increase in NaCl concentration and a
drastic decrease in net photosynthetic rate is found
(Tiwari et al., 1997). Mishra et al. (1991) have reported
that in wheat (T. aesivum L.) salt stress has no direct effect
on electron transport activity and F(v)/F(m) ratio,
suggesting that the efciency of the photochemistry of
PSII is not affected and decrease in F(m) due to salt stress
may inuence reduction of Q(A). These results on
uorescence indicate that salt stress predisposes photoinhibition of plants and reduces their ability to recover
from photoinhibition.
Light stress and salt stress are major environmental
factors that limit the efciency of photosynthesis.
However, Allakhverdiev et al. (2002) have reported that
the effects of light and salt stress on PSII in the
cyanobacterium Synecchocystis sp. PCC 6803 are
completely different. Strong light induces photodamage
to PS II, whereas salt stress inhibits the repair of
photodamaged PSII and does not accelearate damage to
PSII directly. The combination of light and salt stress
appears to inactivate PSII very rapidly as a consequence
of their synergistic effects. Radioactive labeling of cells
reveals that salt stress inhibits the synthesis of proteins
de novo and, in particular, the synthesis of the D1
protein of PSII. Northern and Western blotting analyses
by Allakhverdiev et al. (2002) demonstrate that salt
stress inhibits the transcription and the translation of
psbA genes, which encode D1 protein. DNA microarray
analysis indicates that the light-induced expression of
various genes is suppressed by salt stress. It has been
suggested that salt stress inhibits the repair of PSII via
Table 8
Effects of NaCl (mM) on PSII-mediated electron transport activity (mmol mg chl1 h1) in B. parviflora as monitored with regard to DCPIP
photoreduction
[NaCl] (mM)
H2O-DCPIP
0
100
200
400
DPC-DCPIP
0
100
200
400
0 days
72.9772.5
72.977 2.7
72.9772.0
72.9772.3
113.4072.7
113.8972.0
112.5772.0
112.8071.5
15 days
30 days
45 days
71.1271.3
75.1071.5
70.5271.5
68.2772.0
71.8672.0
75.3571.3
65.6371.7
60.8271.0
70.6871.7
75.8171.5
61.2871.0
54.8172.5
111.6271.3
113.5171.8
110.7071.5
104.8272.0
111.5871.0
115.5472.3
106.7372.5
85.8172.4
110.5571.8
114.6272.5
93.4772.3
78.6571.7
The rate was measured at different days after NaCl treatment in a reaction mixture at pH 7.0 as H2O-DCPIP without any uncoupler and inhibitors
or as DPC-DCPIP. The values are mean7SE (n 6) (Source: Parida et al., 2003).
ARTICLE IN PRESS
suppression of the activities of the transcriptional and

translational machinery (Allakhverdiev et al., 2002).
Photosynthesis involves a long chain of mechanisms,
enzymes, and intermediate products and is regulated by
several external and internal factors. Photosynthetic
efciency depends on the sequence of metabolic events
such as photochemical reactions, on the enzymes
involved in carbon assimilation, on the structure of the
photosynthetic apparatus, and on the transport of
photosynthetic intermediates between subcellular compartments.
Photosynthetic rate is lower in salt-treated plants, but
the photosynthetic potential is not greatly affected when
rates are expressed with regard to chlorophyll or leaf
area. Decreases in photosynthetic rate are due to several
factors: (1) dehydration of cell membranes which reduce
their permeability to CO2, (2) salt toxicity, (3) reduction
of CO2 supply because of hydroactive closure of
stomata, (4) enhanced senescence induced by salinity,
(5) changes of enzyme activity induced by changes in
cytoplasmic structure, and (6) negative feedback by
reduced sink activity (Iyengar and Reddy, 1996).
Photosynthetic activity decreases as water potential of
leaves decreases (Iyengar and Reddy, 1996). The
reduction in photosynthetic activity depends on two
aspects of salinization, i.e., the total concentration of
salt and their ionic composition. High salt concentration
in soil and water create high osmotic potential, which
reduces the availability of water to plants. Decrease in
water potential causes osmotic stress, which reversibly
inactivates photosynthetic electron transport via shrinkage of intercellular space which is due to efux of water
through water channels in the plasma membrane
(Allakhverdiev et al., 2000a). Increase in osmotic
potential under high salt conditions causes Na+ ions
to leak into the cytosol (Papageorgiou et al., 1998) and
inactivate both photosynthetic and respiratory electron
transport (Allakhverdiev et al., 1999).
High salt (NaCl) uptake competes with the uptake of
other nutrient ions, especially K+, leading to K+
deciency (Ball et al., 1987). Under such conditions of
high salinity and K+ deciency, a reduction in quantum
yield of oxygen evolution due to malfunctioning of
photosystem II occurs (Ball et al., 1987).
The reduction in photosynthetic rate is also due to the
reduction in stomatal conductance resulting in restricted
availability of CO2 for carboxylation reactions (Brugnoli and Bjorkman, 1992). Stomatal closure minimizes loss
of water by transpiration and this affects chloroplast
light-harvesting and energy-conversion systems thus
leading to alteration in chloroplast activity (Iyengar
and Reddy, 1996). The extent to which stomatal closure
affects photosynthetic capacity depends on the magnitude of partial pressure of CO2 inside the leaf. There are
also reports of nonstomatal inhibition of photosynthesis
under salt stress. This nonstomatal inhibition is due to
343
increased resistance to CO2 diffusion in the liquid phase

from the mesophyll wall to the site of CO2 reduction in
the chloroplast and reduced efciency of RUBPCase
(Iyengar and Reddy, 1996).
Reduction in photosynthetic capacity is also a
consequence of inhibition of certain carbon metabolism
processes by feedback from other salt-induced reactions
(Greenway and Munns, 1980). Under reduced water
potential, stromal levels of the substrate fructose-1,6bisphosphate (FBP) accumulate and the FBPase
product fructose-6-phosphate is reduced so that
FBPase becomes rate limiting to photosynthesis (Heuer,
1996).
To cope with salt stress plants respond with physiological and biochemical changes that aim at the
retention of water despite high external osmoticum
and the maintenance of photosynthetic activity and
these enable plants to become tolerant. An understanding of the mechanisms by which salinity affects
photosynthesis would aid the improvement of growth
conditions and crop yield and would provide useful
tools for future genetic engineering.
4. Conclusion
Salinity effects and problems with regard to tolerance
and ecological performance are discussed briey in this
review. This review provides information on physiological, biochemical, and molecular bases of salt tolerance.
Efforts have been made to compare the relative
sensitivity of various plant species to salt, and uptake
and transport of NaCl are considered with regard to
phytotoxicity and their interactions with nutrients.
Present knowledge offers some ways for increasing salt
tolerance.
In conclusion, salinity is the most serious threat to
agriculture and to the environment in many parts of the
world and key molecular factors that can be used for
genetic engineering of salt-tolerant plants include overexpression of specic transcription factors, characterization of dehydrin proteins, overproduction of
osmoprotectants, expression of water channel proteins
and ion transporters, and expression and characterization of molecular chaperones.
Acknowledgments
We are grateful to Professor P. Mohanty, Visiting
Professor, Regional Plant Resource Centre, Bhubaneswar for his valuable suggestions during the course of
studies. The nancial assistance from CSIR (Grant No.
38(983)/EMR-II), New Delhi is gratefully acknowledged.
ARTICLE IN PRESS
344
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Salinidade e Seus Efeitos em Plantas

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ARTICLE IN PRESS

Ecotoxicology and Environmental Safety 60 (2005) 324349

Salt tolerance and salinity effects on plants: a review

strates are needed for cell growth, are supplied mainly

2. Salt tolerance of plants

of compatible solutes, (v) change in photosynthetic

Extracellular and cell-wall space Ion exclusion

Cytosol and organelle space

Plant growth regulator

halophyte, cannot tolerate large amounts of salt in the

The Arabidopsis thaliana AtNHX1 gene encodes a

and intracellular compartments (Knight et al., 1997).

transformants, mannitol accumulates throughout the

and radical scavenging. Salt stress increases reducing

increases in leaves of B. parviflora by salt stress (Fig. 4)

Fig. 2. Changes in protein proe in leaf of B. parviflora after 7, 14, and

Fig. 3. Effects of NaCl stress on proline level in B. parviflora measured

Blumwald et al. (2000); Hasegawa et al. (2000); Nilu et al. (1995)

Singh et al. (1987); King et al. (1988)

Glucose, fructose, sucrose

Kerepesi and Galiba (2000)

Acyclic (e.g., manitol)

Carbon storage, osmotic adjustment

Popp et al. (1985); Bohnert et al. (1995)

Ion balance, chromatin protection

Tiburico et al. (1993); SantaCruz et al. (1998)

Quaternary amines Glycine betaine

Carotenoids, anthocyanins, betalaines Protection against photoinhibition

with increasing external salt concentration, amino acids

osmolytes is often achieved by diversion of basic

damage (Harper and Harvey, 1978; Dhindsa and

with epicotyl growth (Hernandez et al., 2002). Analysis

modications of gene expression, and the analysis of

2.6. Change in photosynthetic pathway

Quintero et al. (1996)

Salt associated 23 to 25 kDa protein

Induced by salt stress, overexpression in Arabidopsis or yeast overcomes

26- and 43-kDa polypeptides

Reviron et al. (1992)

Encodes myo-inositol o-methyl transferase 1; induced by NaCl and

Vernon and Bohnert (1992)

Heat shock at 38 1C induces cross tolerance to salt stress

Harrington and Alm (1988)

26-kDa protein, protein level enhanced in both NaCl- and PEG-induced

Singh et al. (1987)

Ishitani et al. (1996)

Mundy et al. (1990)

Claes et al. (1990)

Salt responsive genes/proteins

Carbon metabolism and energy production/photosynthesis

interpretation of an adaptive process is supported by the

Salinity has a smaller effect

tolerance mechanism. Table 4 summarizes differences in

3. Salinity effects on plants

cessation of expansion as salt concentration increases

shoot weight, plant height, number of leaves per plant,

Leaf area (cm2/

Water content per unit leaf

cotton, and Atriplex (Longstreth and Nobel, 1979). In

3.4. Effects of salinity on photosynthetic pigments and

Fig. 4. Effects of NaCl stress on polyphenol level in B. parviflora

noids are signicantly reduced under NaCl stress, but

Chl a (mg cm2)