Environmental and Experimental Botany 68 (2010) 14–25
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Environmental and Experimental Botany
journal homepage: www.elsevier.com/locate/envexpbot
Effect of exogenous salicylic acid under changing environment: A review
Qaiser Hayata, Shamsul Hayata,∗, Mohd. Irfana, Aqil Ahmadb
aPlant Physiology Section, Department of Botany, Aligarh Muslim University, Aligarh 202002, U.P., India
bDepartment of Applied Sciences, Higher College of Technology, Al-Khuwair, Oman
a r t i c l ei n f o
Received 30 April 2009
Received in revised form 17 August 2009
Accepted 18 August 2009
a b s t r a c t
Salicylic acid (SA), an endogenous plant growth regulator has been found to generate a wide range of
metabolic and physiological responses in plants thereby affecting their growth and development. In the
present review, we have focused on various intrinsic biosynthetic pathways, interplay of SA and MeSA,
its long distance transport and signaling. The effect of exogenous application of SA on bio-productivity,
growth, photosynthesis, plant water relations, various enzyme activities and its effect on the plants
exposed to various biotic and abiotic stresses has also been discussed.
© 2009 Elsevier B.V. All rights reserved.
Biosynthesis and metabolism........................................................................................................................
Signaling and transport of salicylic acid .............................................................................................................
Effect of exogenous salicylic acid on growth and bio-productivity .................................................................................
Effect of exogenous SA on photosynthesis and plant water relations ..............................................................................
Effect of exogenous SA on Rhizobium-legume symbiosis............................................................................................
Relationship of SA with antioxidant system and its impact on the plants exposed to stress.......................................................
7.2.Abiotic stress .................................................................................................................................
7.2.1.Effect of exogenous SA on plants exposed to heavy metal stress..................................................................
7.2.2.Effect of exogenous SA on plants grown under salinity stress.....................................................................
7.2.3. Effect of exogenous SA on plants grown under temperature stress ...............................................................
7.2.4.Effect of exogenous SA on the plants exposed to UV radiation or ozone stress ...................................................
7.2.5.Effect of exogenous SA on plants exposed to water stress.........................................................................
Future perspectives ..................................................................................................................................
Salicylic acid or ortho-hydroxy benzoic acid is ubiquitously dis-
tributed in the whole plant kingdom and its history dates back to
1878, when it was world’s largest selling drug synthesized in Ger-
∗Corresponding author. Tel.: +91 9412328593.
E-mail address: email@example.com (S. Hayat).
a latin word “salix” meaning willow tree and the name was given
by Rafacle Piria in 1938. SA has been characterized in 36 plants,
belonging to diverse groups (Raskin et al., 1990). In the plants, such
as rice, crabgrass, barley and soybean the level of salicylic acid is
approximately 1 microgram g−1fresh mass. Floral parts of seven
species and the leaves of 27 thermogenic species exhibited sub-
stantial variation in the level of SA (Raskin et al., 1990). Salicylic
acid is considered to be a potent plant hormone (Raskin, 1992a)
because of its diverse regulatory roles in plant metabolism (Popova
et al., 1997). Salicylic acid is an endogenous plant growth regulator
0098-8472/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
of phenolic nature that possesses an aromatic ring with a hydroxyl
talline powder state having a melting point of 157–159◦C and a pH
in the regulation of plant growth, development, interaction with
other organisms and in the responses to environmental stresses
(Raskin, 1992a,b; Yalpani et al., 1994; Senaratna et al., 2000). Fur-
ther, its role is evident in seed germination, fruit yield, glycolysis,
flowering in thermogenic plants (Klessig and Malamy, 1994), ion
stomatal conductance and transpiration (Khan et al., 2003).
Salicylic acid is considered to be an important signaling
molecule which is involved in local and endemic disease resis-
tance in plants in response to various pathogenic attacks (Enyedi
et al., 1992; Alverez, 2000). Besides providing disease resistance
to the plants, SA can modulate plant responses to a wide range
of oxidative stresses (Shirasu et al., 1997). Keeping in view the
diverse physiological roles of SA in plants, and the necessary space
constraints, we restrict our coverage to its biosynthesis, transport,
involvement in signaling and the effects of exogenous salicylic acid
on bio-productivity, growth, activities of various enzyme and its
impact on plants, exposed to various biotic and abiotic stresses.
2. Biosynthesis and metabolism
In early 1960s, it was suggested that salicylic acid is synthe-
sized in plants from cinnamic acid by two possible pathways.
One pathway involves the decarboxylation of the side chain of
cinnamic acid to form benzoic acid, which inturn undergoes a 2-
hydroxylation to form salicylic acid. Such biosynthetic pathway of
salicylic acid has been reported in tobacco (Yalpani et al., 1993)
and in rice (Silverman et al., 1995). The enzyme that catalyzes the
transformation of cinnamic acid to benzoic acid has been identi-
fied in Quercus pedunculata (Alibert and Ranjeva, 1971; Alibert and
Ranjeva, 1972). However, other enzymes involved in the pathway
are yet to be explored. The other pathway proposed for the biosyn-
thesis of salicylic acid involves a 2-hydroxylation of cinnamic acid
to o-coumaric acid which is then decarboxylated to salicylic acid
and the reaction is catalyzed by an enzyme trans-cinnamate-4-
hydroxylate (Alibert and Ranjeva, 1971; Alibert and Ranjeva, 1972)
which was first detected in pea seedlings (Russell and Conn, 1967).
and Ranjeva, 1971; Alibert and Ranjeva, 1972) and in Melilotus alba
(Gestetner and Conn, 1974). However, the exact mechanism of the
radiolabeled benzoic acid or cinnamic acid and recovered the radi-
olabeled salicylic acid in Gaultheria procumbens. This observation
further strengthened the belief that salicylic acid is synthesized
from cinnamic acid via the formation of benzoic acid. However,
recently, genetic studies in Arabidopsis have shown that salicylic
experiments was lower than expected. According to this pathway,
salicylic acid is synthesized from chorismate by means of isocho-
rismate synthase in chloroplasts and the salicylic acid synthesized
by this pathway is responsible for providing local and systemic
acquired resistance in plants (Wildermuth et al., 2001)
SA has got a property of forming conjugates with a variety
of molecules (Ibrahim and Towers, 1959; Griffiths, 1959) either
by glycosylation or by esterification (Popova et al., 1997). The
conjugated form of SA as ?-glucoside-SA was reported in suspen-
sion cultures of Mellotus japonicus (Tanaka et al., 1990) and also
in the roots of Avena sativa seedlings (Balke and Schulz, 1987;
Yalpani et al., 1992). The enzyme that catalyzes the metabolism
of salicylic acid to ?-glucoside-SA was identified and named as SA-
glucosyltransferase (Gtase) (Balke and Schulz, 1987; Yalpani et al.,
1992). SA may also be metabolized to 2,3-dihydrobenzoic acid or
2,5-dihydrobenzoic acid as was identified in the leaves of Astilbe
sinensis and Lycopersicon esculentum after administering the radio-
labeled cinnamic acid or benzoic acid (Billek and Schmook, 1967).
3. Signaling and transport of salicylic acid
SA is well known naturally occurring signaling molecule that
play’s a key role in establishing and signaling a defense response
against various pathogenic infections (Malamy et al., 1990; Durner
et al., 1997) and also induces systemic acquired resistance (SAR)
in plants. The induction of SAR, after a localized infection, requires
some kind of long distance communication mediator. A survey of
literature indicates that salicylic acid moves from infected organs
of plants to the non-infected ones through phloem (Metraux et al.,
1990; Rasmussen et al., 1991; Yalpani et al., 1991). These findings
were further confirmed by using radiolabeled SA or its analogues
in cells can move freely in and out of the cells, tissues and organs
(Kawano et al., 2004) and this movement is finely regulated by ROS
and Ca2+(Chen and Kuc, 1999; Chen et al., 2001). Supplementation
of tobacco cell suspension culture with higher concentration of sal-
icylic acid resulted in a de novo induction of SA excretion across the
membrane which was mediated by the generation of ROS and acti-
vation of a cascade of Ca2+signaling and protein phosphorylation.
However, exogenous supply of lower concentrations of salicylic
acid did not require a de novo synthesis of proteins and was found
independent of ROS, Ca2+and protein kinases (Chen et al., 2001).
It has also been reported by Morris et al. (2000) that SA partici-
pated in signaling and regulation of gene expression in the course
of leaf senescence in Arabidopsis. Salicylic acid acts as a signaling
molecule and regulates the biogenesis of chloroplasts (Uzunova
ripening (Srivastava and Dwivedi, 2000).
Ohashi et al. (2004) reported that the radiolabeled salicylic
acid was translocated at an unexpectedly rapid rate when applied
exogenously at cut end of petiole in tobacco plants. The results of
their experiment revealed that the signal reached to 6 neighbor-
ing upper leaves and three adjacent lower leaves with in a span of
10min and accumulated throughout the plant body within 50min
indicating that the transport of salicylic acid is rapid and smooth
enough to allow a systemic distribution of SA signal throughout
the plat body with in a short span of time, thereby providing tol-
erance to infections. Further, it is also cited in the literature that
the cuticle hardly allows the entry of surface applied salicylic acid
in plants (Ohashi et al., 2004; Niederl et al., 1998). However, it
was further reported that salicylic acid can pass through the tough
cuticular layer in its methylated (MeSA) form which makes it capa-
ble of diffusing across cuticle independent of pH (Niederl et al.,
1998). Methyl salicylate (MeSA) is a volatile long distance signal-
ing molecule that moves from infected to the non-infected tissues
through phloem. MeSA represents an inactive precursor of SA
that can be translocated and converted to salicylic acid whenever
required. Shulaev et al. (1997) reported that MeSA was produced
from SA in tobacco plants, after infection and induced the defense
response by reverting back to SA. Further, MeSA levels in plant
tissues also parallel the increase in SA concentration locally and
systemically after viral or bacterial infections (Seskar et al., 1998).
These authors also reported that NahG mutants were unable to
trol the balance between SA and MeSA: the SA binding protein
2 (SABP2), which converts biologically inactive MeSA into active
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
SA (Forouhar et al., 2005), and SA methyl transferase 1 (SAMT1),
which catalyses the formation of MeSA from SA (Ross et al., 1999).
Recently the research on MeSA reached a breakthrough, when Park
et al. (2007) demonstrated that MeSA functions as a crucial long
distance SAR signal in tobacco. The authors reported that MeSA
tion in the distal tissues. The fact was further confirmed by the use
of SABP2 and/or SAMT1 silenced plants, where SAR was blocked.
Park et al. (2009) confirmed the importance of SABP2 and MeSA
for the development of SAR in tobacco. However, it still remains
unclear whether MeSA plays a similar role in other plant species.
4. Effect of exogenous salicylic acid on growth and
Salicylic acid and other salicylates are known to affect various
physiological and biochemical activities of plants and may play a
SA and its close analogues enhanced the leaf area and dry mass
production in corn and soybean (Khan et al., 2003). Enhanced ger-
mination and seedling growth were recorded in wheat, when the
icylic acid (Shakirova, 2007). Fariduddin et al. (2003) reported that
juncea, when lower concentrations of salicylic acid were sprayed.
However, higher concentrations of SA had an inhibitory effect.
In another study, Hayat et al. (2005), the leaf number, fresh
and dry mass per plant of wheat seedlings raised from the grains
soaked in lower concentration (10−5M) of salicylic acid, increased
significantly. Similar growth promoting response was generated
in barley seedlings sprayed with salicylic acid (Pancheva et al.,
1996). Khodary (2004) observed a significant increase in growth
sprayed with SA. The exogenous SA application also enhanced
the carbohydrate content in maize (Khodary, 2004). Hussein et al.
an enhanced productivity due to an improvement in all growth
characteristics including plant height, number and area of green
leaves, stem diameter and dry weight of stem, leaves and of the
SA had more proline content.
It is well documented that the plans on being exposed to
stressful environments such as high salinity, result in a decline
in their metabolic activity, thereby leading to retarded overall
growth (Ramagopal, 1987). However, salinity induced retardation
of growth in wheat was to a great extent alleviated by the appli-
cation of salicylic acid (Shakirova, 2007). Eraslan et al. (2007) also
carried out an experiment to elucidate the effect of exogenously
applied salicylic acid on growth, physiology and antioxidant activ-
ity of carrot plants grown under combined stress of salinity and
boron toxicity. The results of their experiment revealed that sali-
cylic acid significantly enhanced the overall growth, root dry mass,
sulphur concentration, carotenoids and anthocyanin contents with
a concomitant enhancement of total antioxidant activity of shoot
and that of storage root. The SA application also regulated the pro-
line accumulation and decreased the toxic ion (Cl, B) accumulation,
both in shoot and storage root. However, Pancheva et al. (1996)
reported a delayed leaf emergence and a decrease in the growth
of leaves and roots of barley plants in a dose-dependent manner,
when salicylic acid was applied exogenously. A dose-dependent
inhibition in bud formation was also observed in Funaria hygro-
2002). Further, exogenous application of SA has also been found to
and potassium by roots and this decrease was found to be depen-
dent on pH, suggesting a higher activity of protonated form of SA
(Hayat and Ahmad, 2007).
and besides some other factors a healthy root system plays a key
role in enhancing the growth and productivity of plants. Basu et
al. (1969) observed that the rooting was enhanced in mungbean
plants, following the treatment of salicylates. In a study carried
out by Larque-Saavedra et al. (1975), treatment of bean explants
with aspirin, which is a close analogue of salicylic acid, enhanced
rooting. Since then a lot of work was carried out to elucidate the
effect of exogenous SA and other salicylates on rooting and thereby
productivity in plants.
Lower concentrations of salicylic acid enhanced rooting inTage-
tus erecta (Sandoval-Yapiz, 2004) and these findings were strictly
in tune with the observations made by Gutierrez-Coronado et
al. (1998), where foliar application of salicylic acid significantly
increased the length of roots in soybean. This root growth pro-
moting domain of salicylic acid has now made it one of the most
important, effective and cost beneficial phytohormone that has the
potential to enhance the root growth in economically important
vegetables and salads like Daucus carota, Raphanus sativus and Beta
vulgaris (Aristeo-Cortes, 1998).
A similar promotion was generated in shoot system as well,
when the plants of T. erecta were treated with lower concentra-
tions of salicylic acid, thereby enhancing the productivity of plants
nously to wheat seedlings increased the size and mass of plantlets
significantly, compared to the untreated control (Shakirova, 2007).
Flowering is another important parameter that is directly
related to yield and productivity of plants. Salicylic acid has been
(Cleland and Ajami, 1974). Different plant species including orna-
mental plant Sinningia speciosa flowered much earlier as compared
to the untreated control, when they received an exogenous foliar
spray of salicylic acid (Martin-Mex et al., 2003, 2005a). Promising
results were obtained when plants of Carica papaya were treated
with salicylic acid which showed a significantly higher fruit setting
(Herrera-Tuz, 2004; Martin-Mex et al., 2005b). Exogenous appli-
cation of aspirin (a close analogue of SA) enhanced flowering in
(Khurana and Maheshwari, 1987; Tomot et al., 1987). Moreover, in
association with sucrose, SA enhanced flower opening in Oncidium
(Hew, 1987). In cucumber and tomato, the fruit yield enhanced sig-
application of salicylic acid to soybean also enhanced the flowering
and pod formation (Kumar et al., 1999). In a comparative analysis,
Kumar et al. (2000), studied the cumulative effect of SA with that
of GA, Kinetin, NAA, ethral and chloro chloro chloride (CCC), and
found a synergistic effect of SA and GA on flowering compared to
other combinations of hormones. However, the exact mechanism
of flower inducing property of salicylic acid is yet to be explored.
However, Oota (1975), hypothesized that o-hydroxyl of salicylic
acid confers the metal chelating property that favours induction of
flowering. The induction of flowering in Lamnaceae, following the
treatment of chelating agents (Seth et al., 1970; Oota, 1972), sup-
ports this hypothesis. Thus, it may be concluded that salicylic acid
acts as an endogenous regulator that potentially affects the growth
and productivity in plants.
5. Effect of exogenous SA on photosynthesis and plant
It is a well-established fact that salicylic acid potentially gener-
ates a wide array of metabolic responses in plants and also affects
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
the photosynthetic parameters and plant water relations. Hayat
et al. (2005) reported that the pigment content was significantly
enhanced in wheat seedlings, raised from the grains pre-treated
concentrations did not prove to be beneficial. Besides seed-soaking
treatment, the foliar application of SA also proved to be equally
chlorophyll content was significantly enhanced, whereas, higher
concentrations proved to be inhibitory (Fariduddin et al., 2003).
However, contrary to these observations, a reduction in chloro-
phyll content was observed in plants pre-treated with salicylic acid
et al. (2003) reported that salicylic acid activated the synthesis of
carotenoids and xanthophylls and also enhanced the rate of de-
epoxidation with a concomitant decrease in chlorophyll pigments
and chlorophyll a/b ratio in wheat and moong. Exogenous appli-
cation of SA was found to enhance the net photosynthetic rate,
internal CO2concentration, water use efficiency, stomatal conduc-
tance and transpiration rate in B. juncea (Fariduddin et al., 2003).
Further, Khan et al. (2003) reported an increase in transpiration
rate and stomatal conductance in response to foliar application of
SA and other salicylates in corn and soybean. In another study car-
ried out in soybean, foliar application of salicylic acid enhanced
the water use efficiency, transpiration rate and internal CO2con-
centration (Kumar et al., 2000). However, contrary to these results,
the transpiration rate decreased significantly in Phaseolus vulgaris
and Commelina communis after the foliar application of SA and
this decrease in transpiration rate was attributed to the fact that
salicylic acid induced the closure of stomata (Larque-Saavedra,
1978, 1979). The leaf carbonic anhydrase activity was significantly
enhanced, when SA at lower concentration (10−5M) was either
sprayed to the foliage of Brassica (Fariduddin et al., 2003) or sup-
plied exogenously as pre-sowing seed-soaking treatment to wheat
grains (Hayat et al., 2005). However, the treatment with higher
concentrations of SA decreased the activity of the enzyme. Such a
decrease in the enzyme activity was also observed by Pancheva et
al. (1996), where the activity of ribulose-1,5-biphosphate carboxy-
lase/oxygenase (RuBPCO) in barley decreased with the increasing
concentration of SA and this decrease was accompanied by a
concomitant increase in the activity of phosphoenol pyruvate car-
boxylase (PEPCase) resulting in a decline in photosynthetic rate
which was contrary to the results of Fariduddin et al. (2003) and
Hayat et al. (2005).
6. Effect of exogenous SA on Rhizobium-legume symbiosis
SA is reported to affect the early stages of Rhizobium-legume
symbiosis. The nod factors produced by the colonizing Rhizobia
in response to flavonoids released by the legume, changed the
endogenous SA content of the host plant during the early stages of
nodulation (Mabood and Smith, 2007). Exogenous SA inhibited the
growth of Rhizobia and the production of nod factors by them and
also delayed the nodule formation, thereby decreasing the num-
ber of nodules per plant (Mabood and Smith, 2007). However, in
another study, Martinez-Abarca et al. (1998), observed that the SA
level in the roots of Medicago sativa, inoculated with specific strain
of Rhizobia, either decreased or remained close to the basal levels.
However, M. sativa plants when inoculated with an incompatible
strain of Rhizobia, resulted in a marked accumulation of SA in the
roots of host plant. It was therefore, concluded that the compati-
ble strains of Rhizobia produce certain signals (specific nod factors)
which are perceived by the host plant that suppress the accumula-
tion of SA in the roots (Martinez-Abarca et al., 1998).
Van Spronsen et al. (2003) reported that the exogenous applica-
tion of SA at lower concentration strongly inhibited indeterminate
nodule formation in Vicia sativa and pea thereby decreasing the
vulgaris, Lotus japonicus and soybean, producing determinate nod-
ules, did not inhibit nodulation. The results of Lian et al. (2000)
revealed that higher concentrations (5 and 1mM) of SA had an
inhibitory effect on nodulation, thereby decreasing nodule number
and dry mass in soybean, thereby lowering the nitrogen fixation
and photosynthesis. The nodule number, N2fixation and protein
content of Vigna mungo, raised from the seeds soaked in SA prior
to inoculation with specific strain of Rhizobium, decreased signifi-
cantly compared to unsoaked control (Ramanujan et al., 1998). The
aforesaid discussion clearly indicates that SA has crucial regulatory
infestating Rhizobia. The relation is terminated under initial sup-
ply of exogenous SA, particularly higher concentrations severely
checks the symbiotic relation. Once the establishment of symbio-
sis is terminated the upcoming benefits of well known benefits of
sis are also hampered. However, SA did not affect the subsequent
nodule development, if supplied after inoculation. This could be
regarded as a good example of spatial and temporal regulation of
synthesize it especially under stress. Conversely, plant synthesizes
it endogenously as in case of inoculation with incompatible strain.
Nitrogen metabolism is an important aspect of legume-
Rhizobium symbiosis and exogenous application of SA was found to
affect the activities of the enzymes of nitrate/nitrogen metabolism
in the leaves of wheat following the exogenous application of SA.
The treatment also protected the enzyme from the action of pro-
teinases and trypsin (Rane et al., 1995). Lead induced decline in
NR activity was revived in the maize plants following the exoge-
nous application of SA (Sinha et al., 1994). The total protein content
was increased in soybean plants sprayed with SA and this increase
might be due to enhanced activity of NR following the SA treat-
ment (Kumar et al., 1999). A significant increase in the activity
of nitrate reductase was observed both in roots and leaves of the
plants raised from the wheat grains soaked in lower concentration
when sprayed to the foliage of mustard plants enhanced their NR
were proved to be inhibitory (Jain and Srivastava, 1981).
7. Relationship of SA with antioxidant system and its
impact on the plants exposed to stress
Stressful environments induce the generation of reactive oxy-
gen species (ROS) such as superoxide radicals (O2−), hydrogen
ating a state of oxidative stress in them (Elstner, 1982; Halliwell
and Gutteridge, 1988; Asada, 1994; Gille and Singler, 1995; Monk
ROS level in plants cause oxidative damage to biomolecules such
as lipids, proteins and nucleic acids, thus altering the redox home-
ostasis (Smirnoff, 1993; Gille and Singler, 1995). When applied
exogenously at suitable concentrations, SA was found to enhance
the efficiency of antioxidant system in plants (Knorzer et al., 1999).
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
SA treatment was found to alleviate the oxidative stress gener-
ated by paraquat (one of the most widely used herbicides, which
is quick-acting and non-selective, killing green plant tissue on con-
tact) in tobacco and cucumber (Strobel and Kuc, 1995). Further,
the treatment with salicylic acid resulted in temporary reduction
of catalase (CAT) activity and increased H2O2level (Janda et al.,
2003) which possibly played a key role in providing the SAR (Chen
et al., 1993) and tolerance against the oxidative stress (Gechev
et al., 2002) in plants. SA was found to enhance the activities of
antioxidant enzymes, CAT, peroxidase (POX) and superoxide dis-
mutase (SOD), when sprayed exogenously to the drought stressed
plants of L. esculentum (Hayat et al., 2008) or to the salinity stressed
the exogenous application of salicylic acid enhanced the activi-
ties of antioxidant enzymes ascorbate peroxidase (APX) and SOD
with a concomitant decline in the activity of CAT in maize plants.
The priming of seeds with lower concentrations of SA, before sow-
ing, lowered the elevated levels of ROS due to cadmium exposure
and also enhanced the activities of various antioxidant enzymes
sativa, thereby protecting the plants from oxidative burst (Panda
and Panda (2004) reported a decline in the activities of the antiox-
idant enzymes CAT, POX, SOD and glutathione reductase in rice
following the pre-sowing seed-soaking treatment with salicylic
7.1. Biotic stress
Plants continuously remain exposed to the challenging threats
of a variety of pathogenic attacks. However, in order to defend
themselves against these attacks, plants have evolved various con-
stitutive and inducible mechanisms, one such mechanism being
the accumulation of large quantities of salicylic acid. This notion
is supported by the observations of Malamy et al. (1990), where
large amounts of salicylic acid accumulated in the leaves of TMV-
resistant tobacco variety Nicotiana tabaccum cv. Xanthi nc, upon
was observed in the phloem sap of cucumber plants, infected with
Colletotrichum lagenarium, Pseudomonas syringae or tobacco necro-
sis virus (Metraux et al., 1990; Rasmussen et al., 1991; Smith et al.,
These findings open a new window for the role to exogenous
application of salicylic acid in providing tolerance to the plants
against various pathogens. The involvement of exogenous SA in
defense signaling has been characterized and well documented in
acid and acetyl salicylic acid was found to induce resistance against
tobacco mosaic virus (TMV) in tobacco (Antoniw and White, 1980).
Further, salicylic acid or acetyl salicylic acid when applied exoge-
nously induced the expression of PR (pathogenesis related) genes
and also conferred resistance against various pathogens of viral,
bacterial, oomycete and fungal origin in a variety of dicot plants
Shah and Klessig, 1999) and in monocot plants (Wasternack et al.,
1994; Kogel et al., 1994; Gorlach et al., 1996; Morris et al., 1998;
Pasquer et al., 2005; Makandar et al., 2006).
Singh et al. (2004) reported that salicylic acid activated a cas-
cade of events resulting in the inhibition of viral replication and
their cell-to-cell and long distance transmission in plants. Lower
concentrations of salicylic acid were found to enhance the depo-
sition of callose plugs in Arabidopsis which contributed to the
plant defense system (Kohler et al., 2002). Lamb and Dixon (1997)
reported that salicylic acid causes an increase in the accumula-
tion of H2O2in plant tissues which plays a key role in initiating
hypersensitive responses and providing SAR against pathogenic
microbes. Salicylic acid is found to alter the activity of a mitochon-
drial enzyme, alternative oxidase, which mediates the oxidation of
out the synthesis of ATP in mitochondria and this altered activity of
enzyme alternative oxidase affects the ROS levels in mitochondria
and in turn induces an antiviral defense response in plants (Singh
et al., 2004).
Salicylic acid has an affinity to bind with the enzymes like CAT,
APX, aconitase and carbonic anhydrase (Chen et al., 1993; Durner
and Klessig, 1995; Ruffer et al., 1999; Slaymaker et al., 2002) and
some of these enzymes are involved in ROS metabolism and in
redox homeostasis. Alteration in this homeostasis leads to induc-
tion of a defense response in plants (Mittler, 2002; Torres et al.,
2002; Durrant and Dong, 2004). SA also affects the lipid peroxida-
et al., 1998) and induction of SAR in plants when challenged with
pathogens (Maldonado et al., 2002; Nandi et al., 2004; Shah, 2005).
7.2. Abiotic stress
7.2.1. Effect of exogenous SA on plants exposed to heavy metal
Among the naturally occurring elements, 53 are considered to
be heavy metals and a few of them have got some biological sig-
nificance for plants (Weast, 1984). However, the heavy metals
like cadmium, if present in elevated levels in agricultural soils,
are easily assimilated by plants and induce serious visible and
metabolic perturbations e.g. leaf roll, chlorosis, growth reduction
in root and shoot, browning of leaf tips (Kahle, 1993), decrease in
Poschenrieder, 1990), disruption of membrane composition and
fluidity (Quariti et al., 1997), decrease photosynthetic rate (Stobort
et al., 1985; Padmaja et al., 1990; Gadallah, 1995) and disruption
of ATPase activity (Fodor et al., 1995). In addition to these haz-
ards Cd hinders the development of chloroplasts (Stoyanova and
Merakchiiska-Nikolova, 1992; Stoyanova and Tchakalova, 1997)
and also affects the activities of two main photosynthetic enzymes
Rubisco and phosphoenol pyruvate carboxylase (Siedlecka et al.,
1998; Stiborova, 1998; Malik et al., 1992).
A role of salicylic acid in alleviating the heavy metal toxicity in
plants has been reported by many workers. Mishra and Choudhuri
cury induced membrane disruptions in rice. Further, exogenous
salicylic acid was found to alleviate the toxic effects generated by
Cd in barley (Metwally et al., 2003) and in maize plants (Pal et al.,
2002). The application of Salicylic acid exogenously, conferred alu-
minium tolerance to the plants of Cassia tora, exposed to Al toxicity
that was mediated by an increase in citrate efflux in the roots of
the treated plants (Yang et al., 2003). Similarly, exogenous salicylic
acid protected barley plants from lipid peroxidation, induced by Cd
effect of SA was mediated by suppressing the cadmium-induced
up-regulation of H2O2metabolizing enzymes such as CAT and APX
(Metwally et al., 2003).
Exogenous application of salicylic acid was also found to alle-
viate the ill effects generated by other heavy metals like lead
and mercury in rice (Mishra and Choudhuri, 1999). These authors
reported deterioration of the membranes in the leaves of rice due
to an increased lipoxigenase activity, induced by lead and mer-
cury toxicity which was mitigated by exogenous SA. In a more
recent study, Zhou et al. (2009) reported that salicylic acid allevi-
ated the toxicity generated by mercury and protected the roots of
M. sativa from oxidative damage induced by mercury. The authors
reported that this protection from oxidative damage was medi-
ated by an increased activity of various antioxidant enzymes. A
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
similar ameliorative role of salicylic acid was observed in soybean
seedlings exposed to cadmium toxicity (Drazic and Mihailovic,
2005). In a study carried out by Drazic et al. (2006), the pre-sowing
seed-soaking treatment with lower concentrations of salicylic acid
enhanced the growth of root and shoot of alfalfa plants, which was
inhibited by cadmium exposure. Further, the treatment was found
to maintain the ionic homeostasis in the seedlings of M. sativa
(alfalfa). Pre-sowing seed treatment with salicylic acid alleviated
carboxylase and PEP carboxylase and also enhanced the activities
of antioxidative enzymes APX and SOD with a concomitant reduc-
tion in the activities of enzyme CAT in maize plants (Krantev et
al., 2008). A significant improvement in growth parameters was
recorded with a concomitant reduction in the rate of cadmium-
induced lipid peroxidation and electrolyte leakage in maize plants,
raised from the seeds soaked in salicylic acid (Krantev et al., 2008).
Similarly, Choudhury and Panda (2004) investigated the ameliora-
tive role of SA on cadmium-induced oxidative stress in roots of O.
sativa. Their study revealed that Cd toxicity resulted in the loss of
elongation growth and biomass of roots with a concomitant accu-
mulation of cadmium in them, thereby, generating oxidative stress
in plants. However, the pre-sowing seed-soaking treatment with
salicylic acid, decreased the toxic effects, generated by cadmium
and was manifested in the form of lowered level of lipid peroxi-
dation, lesser production of H2O2, reduction in the generation of
superoxide radicals and maintaining the stability of membranes.
Shi and Zhu (2008) reported that exogenous SA alleviated the tox-
icity generated in Cucumis sativus by manganese exposure and the
response was mediated by reduction in ROS level and lipid per-
oxidation. The antioxidant enzymes also showed varied response
whereas, SOD, POX, dehydroascorbate reductase (DHAR) and GR
activities were enhanced.
A decline in the activities of enzymes CAT, POX, SOD and glu-
tathione reductase was observed in the plants treated with SA
compared to the untreated plants of O. sativa (Choudhury and
Panda, 2004). However, contrary to this, higher activities of CAT,
in the plants of O. sativa, raised from the seeds primed with sali-
cylic acid. The treatment of salicylic acid also lowered the level of
thiobarbituric acid reactive substances (TBARS), H2O2and O2−in
rice, thereby provided additional tolerance to the plants against
oxidative stress generated by cadmium exposure (Panda and Patra,
7.2.2. Effect of exogenous SA on plants grown under salinity stress
A high salinity induces serious metabolic perturbations in
plants, as it generates ROS which disturb the cellular redox system
may damage DNA, inactivate enzymes and cause lipid peroxida-
tion (Smirnoff, 1993). However, a large body of literature indicates
that exogenous application of salicylic acid to the stressed plants
can potentially alleviate the toxic effects, generated by salinity. An
enhanced tolerance against salinity stress was observed in wheat
seedlings raised from the grains soaked in salicylic acid (Hamada
and Al-Hakimi, 2001). Similar observations were also made in
presumed to be due to the enhanced activation of some enzymes
viz. aldose reductase and ascorbate peroxidase and to the accumu-
lation of certain osmolytes such as proline (Tari et al., 2002, 2004;
Szepesi et al., 2005).
Accumulation of large amounts of osmolytes (proline) is an
adaptive response in plants exposed to stressful environments
(Rai, 2002). Wheat seedlings accumulated large amounts of proline
under salinity stress which was further increased when salicylic
acid was applied exogenously, thereby alleviating the deleterious
effects of salinity (Shakirova et al., 2003). The exogenous applica-
tion of salicylic acid prevented the lowering of IAA and cytokinin
levels in salinity stressed wheat plants resulting in the better-
ment of cell division in root apical meristem, thereby increasing
growth and productivity of plants (Shakirova et al., 2003). These
authors also reported that the pre-treatment with SA resulted in
the accumulation of ABA which might have contributed to the
pre-adaptation of seedlings to salinity stress as ABA induces the
synthesis of a wide range of anti-stress proteins, thereby providing
protection to the plants. Further, the treatment also lowered the
level of active oxygen species and therefore the activities of SOD
and POX were also lowered in the roots of young wheat seedlings
these antioxidant enzymes are directly or indirectly regulated by
salicylic acid, thereby providing protection against salinity stress
(Sakhabutdinova et al., 2004). Exogenous application of salicylic
acid enhanced the photosynthetic rate and also maintained the
stability of membranes, thereby improved the growth of salin-
ity stressed barley plants (El Tayeb, 2005). The damaging effects
of salinity were also alleviated by exogenous application of SA in
Arabidopsis seedlings (Borsani et al., 2001). Kaydan et al. (2007)
observed that pre-sowing soaking treatment of seeds with SA pos-
itively affected the osmotic potential, shoot and root dry mass,
K+/Na+ratio and contents of photosynthetic pigments (chlorophyll
a, b and carotenoids) in wheat seedlings, under both saline and
non-saline conditions. The loss of growth, photosynthetic parame-
ters and the activities of enzymes (nitrate reductase and carbonic
anhydrase) as a result of salinity stress in B. juncea was revived
when salicylic acid was sprayed to the foliage, at 30 days stage.
SOD) were increased with a concomitant increase in proline con-
tent as a result of salinity exposure and/or SA treatment, thereby
providing enhanced tolerance against salinity stress (Yusuf et al.,
7.2.3. Effect of exogenous SA on plants grown under temperature
22.214.171.124. Heat stress. Deviation from optimum temperature result’s
in serious perturbations in plant growth and development which
may be due to membrane disruptions, metabolic alterations and
generation of oxidative stress (Mittler, 2002; Posmyk and Janas,
However, salicylic acid plays a key role in providing tolerance
against temperature stress. A foliar spray of lower concentrations
of salicylic acid conferred heat tolerance to mustard. Further this
treatment, accompanied with hardening at 45◦C for 1h enhanced
A similar response was observed in potato plantlets, raised from
the cultures, supplemented with lower concentrations of acetyl
salicylic acid (Lopez-Delgado et al., 1998). Larkindale and Huang
(2004) pointed out that the enhanced heat tolerance in plants of
Agrostis stolonifera, pre-treated with salicylic acid was due to the
protection of plants from oxidative damage. These authors further
reported that the pre-treatment with salicylic acid had no effect
on POX activity, whereas, the CAT activity declined, compared to
control. However, the treatment enhanced the activity of enzyme
ascorbate peroxidase. Contrary to this, an enhanced activity of CAT
and SOD was observed in heat stressed plants of Poa pratensis, after
the treatment with salicylic acid (He et al., 2005). In a study car-
ried out by Chakraborty and Tongden (2005), it was reported that
the heat stress induced membrane injury in the plants of Cicer
arietinum which was significantly reduced by the application of
SA, compared to the heat acclimatized and untreated control. The
treatment also enhanced the protein and proline contents signif-
icantly with a concomitant induction of various stress enzymes
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
viz. POX and APX. However, the CAT activity was found to be
126.96.36.199. Cold stress. Besides providing tolerance to the plants
against heat shock, exogenous salicylic acid also generates resis-
tance towards chilling or cold stress. Janda et al. (1997, 1999)
reported an enhanced cold tolerance in maize plants, grown in
hydroponic solutions, supplemented with 0.5mM of salicylic acid.
The treatment positively affected various parameters of fluores-
cence and lowered those associated with electrolyte leakage. A
decline in CAT activity with a concomitant enhancement in the
activities of glutathione reductase and guaiacol peroxidase was
also observed. Besides, salicylic acid, its analogues like benzalde-
hyde aspirin or coumaric acid also had a protective role against
chilling stress in maize plants (Janda et al., 1998, 2000; Horvath
et al., 2002). However, it should be underlined here, that SA or its
analogues may exert deleterious effects on plants under normal
growth conditions. A decline in net photosynthetic rate, stomatal
conductance and transpiration rate was observed in maize plants
after 1 day of SA, benzaldehyde (BA) or aspirin treatment under
normal growth conditions (Janda et al., 1998, 2000). The chilling
injury manifested in the form of electrolyte leakage in leaves was
significantly reduced following the application of lower concentra-
tions of salicylic acid to maize, cucumber and rice plants (Kang and
Saltveit, 2002). However, the extent of electrolyte leakage from the
excised radicals of cold stressed maize seedlings was not altered
significantly by SA pre-treatment. Other studies have shown that
the addition of salicylic acid to the hydroponic solution may cause
severe damage to roots (Pal et al., 2002) indicating a toxic effect
generated by SA.
Exogenous salicylic acid potentially alleviates the damaging
effects of low temperatures in rice and wheat (Szalai et al., 2002;
Tasgin et al., 2003), bean (Senaratna et al., 2000) and banana (Kang
et al., 2003a). Pre-treatment with salicylic acid activated various
(Kang et al., 2003b) exposed to chilling stress. Further the increase
in the activities of antioxidant enzymes, SOD, CAT and APX fol-
lowing SA treatment was related to H2O2metabolism produced by
chilling, thereby providing tolerance against the stress (Kang et al.,
to affect the seed germination as well. SA or acetyl salicylic acid
enhanced the germination percentage of carrot seeds (Rajasekaran
et al., 2002) and in the seeds of Capsicum annum at low tempera-
SA not only provided protection against heat and cold stresses,
but was equally beneficial in providing tolerance against freezing
(Frost) injury to winter wheat.
7.2.4. Effect of exogenous SA on the plants exposed to UV
radiation or ozone stress
The level of UV radiations in the environment is increasing day
by day and the plants, which use direct sunlight for photosynthe-
sis are unable to avoid UV radiations which imparts adverse effects
on photosynthesis and other physiological processes (Rajendiran
and Ramanujam, 2003). Similarly, ozone is the other most dam-
aging air pollutant generated through photochemical reactions
between nitrogen oxides, carbon monoxide and hydrocarbons,
and Wang, 2001) and is responsible for tremendous loses to our
crops. Prolonged chronic exposure to ozone results in the inhi-
bition of photosynthesis, premature senescence, altered biomass
partitioning ultimately reducing the growth and yield of plants
(Black et al., 2000; Pell et al., 1997; Saitanis and Karandinos, 2002;
Sandermann, 1996). Therefore, the mechanisms which may pro-
tect the plants from the harmful effects of UV-exposure or ozone
stress are of particular concern. It has been reported earlier that
plants accumulated large amounts of salicylic acid when exposed
to ozone or UV radiations (Yalpani et al., 1994; Sharma et al., 1996).
The role of salicylic acid in counteracting the damaging effects
of ozone was best demonstrated in Arabidopsis thaliana, where
NahG mutants, deficient in SA biosynthesis were more sensitive
to the deteriorating effects of ozone (Sharma et al., 1996). Since,
SA improved the activity of antioxidant enzyme system, therefore,
Arabidopsis (Rao and Davis, 1999). Like ozone, UV radiations were
also reported to induce the accumulation of SA in tobacco plants
and this increased accumulation of SA was probably due to higher
activity of the enzyme BAZ-hydroxylase, which is involved in SA
biosynthesis (Yalpani et al., 1994). In a study carried out by Ervin
et al. (2004), the exogenous application of salicylic acid alleviated
the damaging effects induced by UV-B radiation exposure in Ken-
tuky blue grass and tall fescue sod. These studies revealed that the
treatment enhanced photochemical efficiency and the activities of
antioxidant enzymes CAT and SOD which were greatly reduced
by UV-B exposure. The treatment also increased the anthocyanin
salicylic acid. Thus, it may be concluded that SA plays promoting
role in alleviating the damaging effects of ozone and/or ultraviolet
7.2.5. Effect of exogenous SA on plants exposed to water stress
Exposure of plants to water stress leads to serious physiolog-
ical and biochemical dysfunctions including reduction in turgor,
growth, photosynthetic rate, stomatal conductance and damages
of cellular components (reviewed by Janda et al., 2007).
A survey of literature indicates that salicylic acid plays a key
role in providing tolerance to the plants, exposed to water stress
(drought or flooding). Hayat et al. (2008) studied the growth of
water stressed L. esculentum (tomato) plants in response to exoge-
nously applied salicylic acid. The results of their experiments
revealed a significant decline in photosynthetic parameters, mem-
brane stability index, leaf water potential, activities of the enzymes
nitrate reductase and carbonic anhydrase, chlorophyll and rela-
tive water contents with a concomitant increase in proline content
and the activities of antioxidant enzymes (CAT, POX and SOD).
However, the treatment of these stressed plants with lower con-
centrations of salicylic acid significantly enhanced the aforesaid
parameters thereby improved tolerance of the plants to drought
stress. Higher tolerance to drought stress was also observed in
the plants raised from the grains soaked in aqueous solution of
acetyl salicylic acid and the treatment also enhanced dry mat-
ter accumulation (Hamada, 1998; Hamada and Al-Hakimi, 2001).
The lower concentrations of salicylic acid, when applied exoge-
nously provided tolerance against the damaging effects of drought
in tomato and bean plants, whereas, higher concentrations did not
show fruitful results (Senaratna et al., 2000). Leaf senescence is a
of stored food from the older leaves to the rest of the plant, during
stressful conditions and salicylic acid is involved in the promotion
under drought stress in Mediterranean field conditions (Abreu and
Munne-Bosch, 2008). However, the authors also pointed out that
SA regulates the leaf senescence in association with other phyto-
The results reported by Singh and Usha (2003) revealed that
the wheat seedlings subjected to drought stress when treated with
salicylic acid, generally exhibited higher moisture content and also
higher dry matter accumulation, carboxylase activity of Rubisco,
SOD and total chlorophyll content compared to the untreated con-
to the enzyme nitrate reductase thereby maintained the normal
level of various proteins in the leaves (Singh and Usha, 2003).
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
Fig. 1. Model of the biosynthesis and action of salicylic acid on the induction of biotic and abiotic stress tolerance.
Exogenous application of salicylic acid also alleviated the damag-
ing effects of water deficit on cell membranes of barley plants and
concomitantly increased the ABA content in leaves, which might
have contributed to the enhanced tolerance of plants to water
scarcity (Bandurska and Stroinski, 2005). Besides providing toler-
ance to plants against drought stress, the exogenous application
of SA was also found to be effective in providing resistance to the
plants against the excessive water stress as was observed in cell
suspensions prepared from the fully turgid leaves of Sporobcdus
stapfianus (Ghasempour et al., 2001).
various plant growth responses.
•Exogenous application of salicylic acid enhances the growth and
productivity of plants.
•The flower inducing domain of salicylic acid makes it an import
phytohormone that can enhance flowering in a variety of orna-
•Exogenous application of salicylic acid induces the SAR in plants,
thereby provides a considerable protection against various biotic
•Besides providing protection against infections and pathogen
attacks, SA imparts tolerance against various abiotic stresses to
•SA effectively alleviated the toxic effects generated in plants due
perature, water, ozone, UV irradiance and salinity stress etc.
•Exogenous application of the lower concentrations of salicylic
acid proved to be beneficial in enhancing the photosynthesis
growth and various other physiological and biochemical char-
acteristics of plants.
•However, at higher concentrations, SA itself may cause a high
level of stress in plants.
•Exogenous application of SA enhances the activities of antioxi-
dants enzyme system.
•Exogenous SA can protect and enhance the enzymes of nitrate
metabolism under stressful environments.
•It interferes the indeterminate nodule formation in leguminous
9. Future perspectives
Hence, it may be resolved from the survey of literature cited
above that salicylic acid play’s diverse physiological roles in plants
and potentially alleviates the devastating effects generated by
various biotic and abiotic stresses. However, this recently intro-
duced phytohormone still demands a lot of work to be carried
out to elucidate the exact pathways of its biosynthesis; weather
major or minor, key regulatory points of biosynthesis, mecha-
nism of action and other specific and collaborative regulatory roles
played by salicylic acid that have remained elusive till date. The
work is also needed on how this plant hormone interacts and
being regulated by the cross-talk in harmony with other estab-
range (auxins, cytokinins, gibberellins, ethylene etc.), short range
(NO, jasmonates, brassinosteroids etc.) and very short range (ROS,
H2O2). One could also argue how the regulated doses of these short
range phytohormones mostly produced in-vicinity to biotic infes-
tation and then transported systemically to play their role during
broad range abiotic stresses. It is also worthwhile to elucidate the
role of aforesaid phytohormone in tissue-specific differentiation
and growth of plant parts during growth and development. Bio-
chemical inhibitors of key enzymes of pathways and mutant study
might incident some light on such aspects. Locating tissue-specific
concentrations during seedling development fusing with reporter
genes or radioactive molecules could pave the way in this con-
cern. In future, the exogenous application of this phytohormone
Q. Hayat et al. / Environmental and Experimental Botany 68 (2010) 14–25
might act as a powerful tool in enhancing the growth, produc-
tivity and also in combating the ill effects generated by various
abiotic stresses in plants (Fig. 1). The future applications of this
plant hormone holds a great promise as a management tool for
providing tolerance to our agricultural crops against the aforesaid
constrains consequently aiding to accelerate potential crop yield in
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