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EffectofExogenousSalicylicAcidunderChangingEnvironment:AReview

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Environmental and Experimental Botany 68 (2010) 14–25

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journa l homepage: www.e lsev ier .com/ locate /envexpbot

eview

ffect of exogenous salicylic acid under changing environment: A review

aiser Hayata, Shamsul Hayata,∗, Mohd. Irfana, Aqil Ahmadb

Plant Physiology Section, Department of Botany, Aligarh Muslim University, Aligarh 202002, U.P., IndiaDepartment of Applied Sciences, Higher College of Technology, Al-Khuwair, Oman

r t i c l e i n f o

rticle history:eceived 30 April 2009eceived in revised form 17 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 ofmetabolic and physiological responses in plants thereby affecting their growth and development. In thepresent review, we have focused on various intrinsic biosynthetic pathways, interplay of SA and MeSA,

ccepted 18 August 2009

eywords:alicylic acidrowthtress

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 plantsexposed to various biotic and abiotic stresses has also been discussed.

© 2009 Elsevier B.V. All rights reserved.

hotosynthesisntioxidants

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142. Biosynthesis and metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153. Signaling and transport of salicylic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154. Effect of exogenous salicylic acid on growth and bio-productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165. Effect of exogenous SA on photosynthesis and plant water relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166. Effect of exogenous SA on Rhizobium-legume symbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177. Relationship of SA with antioxidant system and its impact on the plants exposed to stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

7.1. Biotic stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187.2. Abiotic stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

7.2.1. Effect of exogenous SA on plants exposed to heavy metal stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187.2.2. Effect of exogenous SA on plants grown under salinity stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197.2.3. Effect of exogenous SA on plants grown under temperature stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197.2.4. Effect of exogenous SA on the plants exposed to UV radiation or ozone stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207.2.5. Effect of exogenous SA on plants exposed to water stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

8. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219. Future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

. Introduction

Salicylic acid or ortho-hydroxy benzoic acid is ubiquitously dis-ributed in the whole plant kingdom and its history dates back to878, when it was world’s largest selling drug synthesized in Ger-any (Raskin et al., 1990). The word salicylic acid was derived from

∗ Corresponding author. Tel.: +91 9412328593.E-mail address: shayat@lycos.com (S. Hayat).

098-8472/$ – see front matter © 2009 Elsevier B.V. All rights reserved.oi:10.1016/j.envexpbot.2009.08.005

a latin word “salix” meaning willow tree and the name was givenby Rafacle Piria in 1938. SA has been characterized in 36 plants,belonging to diverse groups (Raskin et al., 1990). In the plants, suchas rice, crabgrass, barley and soybean the level of salicylic acid isapproximately 1 microgram g−1 fresh 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). Salicylicacid is considered to be a potent plant hormone (Raskin, 1992a)because of its diverse regulatory roles in plant metabolism (Popovaet al., 1997). Salicylic acid is an endogenous plant growth regulator

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f phenolic nature that possesses an aromatic ring with a hydroxylroup or its functional derivative. In free state, SA is found in a crys-alline powder state having a melting point of 157–159 ◦C and a pHf 2.4 (Raskin, 1992b). Salicylic acid has been found to play a key rolen the regulation of plant growth, development, interaction withther organisms and in the responses to environmental stressesRaskin, 1992a,b; Yalpani et al., 1994; Senaratna et al., 2000). Fur-her, its role is evident in seed germination, fruit yield, glycolysis,owering in thermogenic plants (Klessig and Malamy, 1994), ionptake and transport (Harper and Balke, 1981), photosynthetic rate,tomatal conductance and transpiration (Khan et al., 2003).

Salicylic acid is considered to be an important signalingolecule which is involved in local and endemic disease resis-

ance in plants in response to various pathogenic attacks (Enyedit al., 1992; Alverez, 2000). Besides providing disease resistanceo the plants, SA can modulate plant responses to a wide rangef oxidative stresses (Shirasu et al., 1997). Keeping in view theiverse physiological roles of SA in plants, and the necessary spaceonstraints, we restrict our coverage to its biosynthesis, transport,nvolvement in signaling and the effects of exogenous salicylic acidn bio-productivity, growth, activities of various enzyme and itsmpact on plants, exposed to various biotic and abiotic stresses.

. Biosynthesis and metabolism

In early 1960s, it was suggested that salicylic acid is synthe-ized in plants from cinnamic acid by two possible pathways.ne pathway involves the decarboxylation of the side chain ofinnamic acid to form benzoic acid, which inturn undergoes a 2-ydroxylation to form salicylic acid. Such biosynthetic pathway ofalicylic acid has been reported in tobacco (Yalpani et al., 1993)nd in rice (Silverman et al., 1995). The enzyme that catalyzes theransformation of cinnamic acid to benzoic acid has been identi-ed in Quercus pedunculata (Alibert and Ranjeva, 1971; Alibert andanjeva, 1972). However, other enzymes involved in the pathwayre yet to be explored. The other pathway proposed for the biosyn-hesis of salicylic acid involves a 2-hydroxylation of cinnamic acido o-coumaric acid which is then decarboxylated to salicylic acidnd the reaction is catalyzed by an enzyme trans-cinnamate-4-ydroxylate (Alibert and Ranjeva, 1971; Alibert and Ranjeva, 1972)hich was first detected in pea seedlings (Russell and Conn, 1967).owever, this enzyme was also identified in Q. pedunculata (Alibertnd Ranjeva, 1971; Alibert and Ranjeva, 1972) and in Melilotus albaGestetner and Conn, 1974). However, the exact mechanism of theathway is still an anomaly. Ellis and Amichein (1971) incorporatedadiolabeled benzoic acid or cinnamic acid and recovered the radi-labeled salicylic acid in Gaultheria procumbens. This observationurther strengthened the belief that salicylic acid is synthesizedrom cinnamic acid via the formation of benzoic acid. However,ecently, genetic studies in Arabidopsis have shown that salicyliccid was also produced when the pathways mentioned earlier wereither inhibited or the specific activity of radiolabeled SA in feedingxperiments was lower than expected. According to this pathway,alicylic acid is synthesized from chorismate by means of isocho-ismate synthase in chloroplasts and the salicylic acid synthesizedy this pathway is responsible for providing local and systemiccquired resistance in plants (Wildermuth et al., 2001)

SA has got a property of forming conjugates with a varietyf molecules (Ibrahim and Towers, 1959; Griffiths, 1959) eithery glycosylation or by esterification (Popova et al., 1997). The

onjugated form of SA as �-glucoside-SA was reported in suspen-ion cultures of Mellotus japonicus (Tanaka et al., 1990) and alson the roots of Avena sativa seedlings (Balke and Schulz, 1987;alpani et al., 1992). The enzyme that catalyzes the metabolismf salicylic acid to �-glucoside-SA was identified and named as SA-

rimental Botany 68 (2010) 14–25 15

glucosyltransferase (Gtase) (Balke and Schulz, 1987; Yalpani et al.,1992). SA may also be metabolized to 2,3-dihydrobenzoic acid or2,5-dihydrobenzoic acid as was identified in the leaves of Astilbesinensis 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 thatplay’s a key role in establishing and signaling a defense responseagainst various pathogenic infections (Malamy et al., 1990; Durneret al., 1997) and also induces systemic acquired resistance (SAR)in plants. The induction of SAR, after a localized infection, requiressome kind of long distance communication mediator. A survey ofliterature indicates that salicylic acid moves from infected organsof plants to the non-infected ones through phloem (Metraux et al.,1990; Rasmussen et al., 1991; Yalpani et al., 1991). These findingswere further confirmed by using radiolabeled SA or its analogues(Shulaev et al., 1995; Molders et al., 1996). Salicylic acid synthesizedin cells can move freely in and out of the cells, tissues and organs(Kawano et al., 2004) and this movement is finely regulated by ROSand Ca2+ (Chen and Kuc, 1999; Chen et al., 2001). Supplementationof tobacco cell suspension culture with higher concentration of sal-icylic acid resulted in a de novo induction of SA excretion across themembrane 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 salicylicacid did not require a de novo synthesis of proteins and was foundindependent 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 courseof leaf senescence in Arabidopsis. Salicylic acid acts as a signalingmolecule and regulates the biogenesis of chloroplasts (Uzunovaand Popova, 2000), photosynthetic activity (Fariduddin et al., 2003),gravitropism (Medvedev and Markova, 1991) and inhibition of fruitripening (Srivastava and Dwivedi, 2000).

Ohashi et al. (2004) reported that the radiolabeled salicylicacid was translocated at an unexpectedly rapid rate when appliedexogenously at cut end of petiole in tobacco plants. The results oftheir experiment revealed that the signal reached to 6 neighbor-ing upper leaves and three adjacent lower leaves with in a span of10 min and accumulated throughout the plant body within 50 minindicating that the transport of salicylic acid is rapid and smoothenough to allow a systemic distribution of SA signal throughoutthe plat body with in a short span of time, thereby providing tol-erance to infections. Further, it is also cited in the literature thatthe cuticle hardly allows the entry of surface applied salicylic acidin plants (Ohashi et al., 2004; Niederl et al., 1998). However, itwas further reported that salicylic acid can pass through the toughcuticular 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 tissuesthrough phloem. MeSA represents an inactive precursor of SAthat can be translocated and converted to salicylic acid wheneverrequired. Shulaev et al. (1997) reported that MeSA was producedfrom SA in tobacco plants, after infection and induced the defenseresponse by reverting back to SA. Further, MeSA levels in planttissues also parallel the increase in SA concentration locally andsystemically after viral or bacterial infections (Seskar et al., 1998).

These authors also reported that NahG mutants were unable torespond to MeSA, indicating that this compound has no direct effecton the induction of defense response. In tobacco, two enzymes con-trol the balance between SA and MeSA: the SA binding protein2 (SABP2), which converts biologically inactive MeSA into active

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A (Forouhar et al., 2005), and SA methyl transferase 1 (SAMT1),hich catalyses the formation of MeSA from SA (Ross et al., 1999).ecently the research on MeSA reached a breakthrough, when Parkt al. (2007) demonstrated that MeSA functions as a crucial longistance SAR signal in tobacco. The authors reported that MeSAsterase activity of enzyme SABP2 is essential for SAR signal percep-ion in the distal tissues. The fact was further confirmed by the usef SABP2 and/or SAMT1 silenced plants, where SAR was blocked.ark et al. (2009) confirmed the importance of SABP2 and MeSAor the development of SAR in tobacco. However, it still remainsnclear whether MeSA plays a similar role in other plant species.

. Effect of exogenous salicylic acid on growth andio-productivity

Salicylic acid and other salicylates are known to affect varioushysiological and biochemical activities of plants and may play aey role in regulating their growth and productivity (Arberg, 1981).A and its close analogues enhanced the leaf area and dry massroduction in corn and soybean (Khan et al., 2003). Enhanced ger-ination and seedling growth were recorded in wheat, when the

rains were subjected to pre-sowing seed-soaking treatment in sal-cylic acid (Shakirova, 2007). Fariduddin et al. (2003) reported thathe dry matter accumulation was significantly enhanced in Brassicauncea, when lower concentrations of salicylic acid were sprayed.owever, higher concentrations of SA had an inhibitory effect.

In another study, Hayat et al. (2005), the leaf number, freshnd dry mass per plant of wheat seedlings raised from the grainsoaked in lower concentration (10−5 M) of salicylic acid, increasedignificantly. Similar growth promoting response was generatedn barley seedlings sprayed with salicylic acid (Pancheva et al.,996). Khodary (2004) observed a significant increase in growthharacteristics, pigment contents and photosynthetic rate in maize,prayed with SA. The exogenous SA application also enhancedhe carbohydrate content in maize (Khodary, 2004). Hussein et al.2007) in their pot experiment sprayed salicylic acid to the foliage ofheat plants, irrigated with Mediterranean sea water and reported

n enhanced productivity due to an improvement in all growthharacteristics including plant height, number and area of greeneaves, stem diameter and dry weight of stem, leaves and of thelant as a whole. Moreover, the plants that received treatment withA had more proline content.

It is well documented that the plans on being exposed totressful environments such as high salinity, result in a declinen their metabolic activity, thereby leading to retarded overallrowth (Ramagopal, 1987). However, salinity induced retardationf growth in wheat was to a great extent alleviated by the appli-ation of salicylic acid (Shakirova, 2007). Eraslan et al. (2007) alsoarried out an experiment to elucidate the effect of exogenouslypplied salicylic acid on growth, physiology and antioxidant activ-ty of carrot plants grown under combined stress of salinity andoron toxicity. The results of their experiment revealed that sali-ylic acid significantly enhanced the overall growth, root dry mass,ulphur concentration, carotenoids and anthocyanin contents withconcomitant enhancement of total antioxidant activity of shoot

nd that of storage root. The SA application also regulated the pro-ine accumulation and decreased the toxic ion (Cl, B) accumulation,oth in shoot and storage root. However, Pancheva et al. (1996)eported a delayed leaf emergence and a decrease in the growthf leaves and roots of barley plants in a dose-dependent manner,hen salicylic acid was applied exogenously. A dose-dependent

nhibition in bud formation was also observed in Funaria hygro-atica when SA was supplied exogenously (Christianson and Duffy,

002). Further, exogenous application of SA has also been found tohift the nutrient status leading to a decreased uptake of phosphatend potassium by roots and this decrease was found to be depen-

rimental Botany 68 (2010) 14–25

dent on pH, suggesting a higher activity of protonated form of SA(Hayat and Ahmad, 2007).

The soil nutrient solution enters the plant body through its rootsand besides some other factors a healthy root system plays a keyrole in enhancing the growth and productivity of plants. Basu etal. (1969) observed that the rooting was enhanced in mungbeanplants, following the treatment of salicylates. In a study carriedout by Larque-Saavedra et al. (1975), treatment of bean explantswith aspirin, which is a close analogue of salicylic acid, enhancedrooting. Since then a lot of work was carried out to elucidate theeffect of exogenous SA and other salicylates on rooting and therebyproductivity in plants.

Lower concentrations of salicylic acid enhanced rooting in Tage-tus erecta (Sandoval-Yapiz, 2004) and these findings were strictlyin tune with the observations made by Gutierrez-Coronado etal. (1998), where foliar application of salicylic acid significantlyincreased the length of roots in soybean. This root growth pro-moting domain of salicylic acid has now made it one of the mostimportant, effective and cost beneficial phytohormone that has thepotential to enhance the root growth in economically importantvegetables and salads like Daucus carota, Raphanus sativus and Betavulgaris (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(Sandoval-Yapiz, 2004). Further, salicylic acid when applied exoge-nously to wheat seedlings increased the size and mass of plantletssignificantly, compared to the untreated control (Shakirova, 2007).

Flowering is another important parameter that is directlyrelated to yield and productivity of plants. Salicylic acid has beenreported to induce flowering in a number of plants, including Lemna(Cleland and Ajami, 1974). Different plant species including orna-mental plant Sinningia speciosa flowered much earlier as comparedto the untreated control, when they received an exogenous foliarspray of salicylic acid (Martin-Mex et al., 2003, 2005a). Promisingresults were obtained when plants of Carica papaya were treatedwith 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 inSpirodela (Khurana and Maheshwari, 1980) and Wolfia microscopica(Khurana and Maheshwari, 1987; Tomot et al., 1987). Moreover, inassociation with sucrose, SA enhanced flower opening in Oncidium(Hew, 1987). In cucumber and tomato, the fruit yield enhanced sig-nificantly when the plants were sprayed with lower concentrationsof salicylic acid (Larque-Saavedra and Martin-Mex, 2007). The foliarapplication of salicylic acid to soybean also enhanced the floweringand pod formation (Kumar et al., 1999). In a comparative analysis,Kumar et al. (2000), studied the cumulative effect of SA with thatof GA, Kinetin, NAA, ethral and chloro chloro chloride (CCC), andfound a synergistic effect of SA and GA on flowering compared toother combinations of hormones. However, the exact mechanismof flower inducing property of salicylic acid is yet to be explored.However, Oota (1975), hypothesized that o-hydroxyl of salicylicacid confers the metal chelating property that favours induction offlowering. The induction of flowering in Lamnaceae, following thetreatment of chelating agents (Seth et al., 1970; Oota, 1972), sup-ports this hypothesis. Thus, it may be concluded that salicylic acidacts as an endogenous regulator that potentially affects the growthand productivity in plants.

5. Effect of exogenous SA on photosynthesis and plantwater relations

It is a well-established fact that salicylic acid potentially gener-ates a wide array of metabolic responses in plants and also affects

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he photosynthetic parameters and plant water relations. Hayatt al. (2005) reported that the pigment content was significantlynhanced in wheat seedlings, raised from the grains pre-treatedith lower concentration (10−5 M) of salicylic acid, whereas, higher

oncentrations did not prove to be beneficial. Besides seed-soakingreatment, the foliar application of SA also proved to be equallyruitful in increasing the pigment contents in Brassica napus (Ghai etl., 2002). Similar results were obtained when the plants of B. junceaere sprayed with lower concentrations (10−5 M) of SA, where, the

hlorophyll content was significantly enhanced, whereas, higheroncentrations proved to be inhibitory (Fariduddin et al., 2003).owever, contrary to these observations, a reduction in chloro-hyll content was observed in plants pre-treated with salicylic acidAnandhi and Ramanujam, 1997; Pancheva et al., 1996). Moharekart al. (2003) reported that salicylic acid activated the synthesis ofarotenoids and xanthophylls and also enhanced the rate of de-poxidation with a concomitant decrease in chlorophyll pigmentsnd chlorophyll a/b ratio in wheat and moong. Exogenous appli-ation of SA was found to enhance the net photosynthetic rate,nternal CO2 concentration, water use efficiency, stomatal conduc-ance and transpiration rate in B. juncea (Fariduddin et al., 2003).urther, Khan et al. (2003) reported an increase in transpirationate and stomatal conductance in response to foliar application ofA and other salicylates in corn and soybean. In another study car-ied out in soybean, foliar application of salicylic acid enhancedhe water use efficiency, transpiration rate and internal CO2 con-entration (Kumar et al., 2000). However, contrary to these results,he transpiration rate decreased significantly in Phaseolus vulgarisnd Commelina communis after the foliar application of SA andhis decrease in transpiration rate was attributed to the fact thatalicylic acid induced the closure of stomata (Larque-Saavedra,978, 1979). The leaf carbonic anhydrase activity was significantlynhanced, when SA at lower concentration (10−5 M) was eitherprayed to the foliage of Brassica (Fariduddin et al., 2003) or sup-lied exogenously as pre-sowing seed-soaking treatment to wheatrains (Hayat et al., 2005). However, the treatment with higheroncentrations of SA decreased the activity of the enzyme. Such aecrease in the enzyme activity was also observed by Pancheva etl. (1996), where the activity of ribulose-1,5-biphosphate carboxy-ase/oxygenase (RuBPCO) in barley decreased with the increasingoncentration of SA and this decrease was accompanied by aoncomitant increase in the activity of phosphoenol pyruvate car-oxylase (PEPCase) resulting in a decline in photosynthetic ratehich was contrary to the results of Fariduddin et al. (2003) andayat et al. (2005).

. Effect of exogenous SA on Rhizobium-legume symbiosis

SA is reported to affect the early stages of Rhizobium-legumeymbiosis. The nod factors produced by the colonizing Rhizobian response to flavonoids released by the legume, changed thendogenous SA content of the host plant during the early stages ofodulation (Mabood and Smith, 2007). Exogenous SA inhibited therowth of Rhizobia and the production of nod factors by them andlso delayed the nodule formation, thereby decreasing the num-er of nodules per plant (Mabood and Smith, 2007). However, innother study, Martinez-Abarca et al. (1998), observed that the SAevel in the roots of Medicago sativa, inoculated with specific strainf Rhizobia, either decreased or remained close to the basal levels.owever, M. sativa plants when inoculated with an incompatible

train of Rhizobia, resulted in a marked accumulation of SA in theoots of host plant. It was therefore, concluded that the compati-le strains of Rhizobia produce certain signals (specific nod factors)hich are perceived by the host plant that suppress the accumula-

ion of SA in the roots (Martinez-Abarca et al., 1998).

rimental Botany 68 (2010) 14–25 17

Van Spronsen et al. (2003) reported that the exogenous applica-tion of SA at lower concentration strongly inhibited indeterminatenodule formation in Vicia sativa and pea thereby decreasing thenodulation, nitrogen fixation and ultimately growth of plants. How-ever, the same concentration of SA when sprayed to plants such as P.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 1 mM) of SA had aninhibitory effect on nodulation, thereby decreasing nodule numberand dry mass in soybean, thereby lowering the nitrogen fixationand photosynthesis. The nodule number, N2 fixation and proteincontent of Vigna mungo, raised from the seeds soaked in SA priorto inoculation with specific strain of Rhizobium, decreased signifi-cantly compared to unsoaked control (Ramanujan et al., 1998). Theaforesaid discussion clearly indicates that SA has crucial regulatoryrole in establishing early stages of nodulation and is provided by theinfestating Rhizobia. The relation is terminated under initial sup-ply of exogenous SA, particularly higher concentrations severelychecks the symbiotic relation. Once the establishment of symbio-sis is terminated the upcoming benefits of well known benefits ofnodulation viz. nitrogen fixation, protein content and photosynthe-sis are also hampered. However, SA did not affect the subsequentnodule development, if supplied after inoculation. This could beregarded as a good example of spatial and temporal regulation ofany growth regulator. Furthermore, there appears an adjustment orfine tuning of internal release of SA in response of exogenous supplylowering the overburden on tissue-specific metabolic machinery tosynthesize it especially under stress. Conversely, plant synthesizesit 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 toaffect the activities of the enzymes of nitrate/nitrogen metabolismas well. The activity of enzyme nitrate reductase (NR) was enhancedin 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 inNR activity was revived in the maize plants following the exoge-nous application of SA (Sinha et al., 1994). The total protein contentwas increased in soybean plants sprayed with SA and this increasemight be due to enhanced activity of NR following the SA treat-ment (Kumar et al., 1999). A significant increase in the activityof nitrate reductase was observed both in roots and leaves of theplants raised from the wheat grains soaked in lower concentration(10−5 M) of SA (Hayat et al., 2005). Such a lower concentration of SAwhen sprayed to the foliage of mustard plants enhanced their NRactivity (Fariduddin et al., 2003). However, at higher concentrations(10−3 or 10−4 M), SA proved to be inhibitory. The treatment of maizeplants with lower concentrations of SA also enhanced the uptake ofnitrogen and activity of enzyme NR, whereas, higher concentrationswere proved to be inhibitory (Jain and Srivastava, 1981).

7. Relationship of SA with antioxidant system and itsimpact on the plants exposed to stress

Stressful environments induce the generation of reactive oxy-gen species (ROS) such as superoxide radicals (O2

−), hydrogenperoxide (H2O2), hydroxyl radicals (OH−) etc. in plants thereby cre-ating a state of oxidative stress in them (Elstner, 1982; Halliwelland Gutteridge, 1988; Asada, 1994; Gille and Singler, 1995; Monket al., 1989; Prasad et al., 1999; Panda et al., 2003a,b). This increased

ROS level in plants cause oxidative damage to biomolecules suchas lipids, proteins and nucleic acids, thus altering the redox home-ostasis (Smirnoff, 1993; Gille and Singler, 1995). When appliedexogenously at suitable concentrations, SA was found to enhancethe efficiency of antioxidant system in plants (Knorzer et al., 1999).

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A treatment was found to alleviate the oxidative stress gener-ted by paraquat (one of the most widely used herbicides, whichs quick-acting and non-selective, killing green plant tissue on con-act) in tobacco and cucumber (Strobel and Kuc, 1995). Further,he treatment with salicylic acid resulted in temporary reductionf catalase (CAT) activity and increased H2O2 level (Janda et al.,003) which possibly played a key role in providing the SAR (Chent al., 1993) and tolerance against the oxidative stress (Gechevt al., 2002) in plants. SA was found to enhance the activities ofntioxidant enzymes, CAT, peroxidase (POX) and superoxide dis-utase (SOD), when sprayed exogenously to the drought stressed

lants of L. esculentum (Hayat et al., 2008) or to the salinity stressedlants of B. juncea (Yusuf et al., 2008). Krantev et al. (2008) reportedhe exogenous application of salicylic acid enhanced the activi-ies of antioxidant enzymes ascorbate peroxidase (APX) and SODith a concomitant decline in the activity of CAT in maize plants.

he priming of seeds with lower concentrations of SA, before sow-ng, lowered the elevated levels of ROS due to cadmium exposurend also enhanced the activities of various antioxidant enzymesCAT, guaiacol peroxidase, glutathione reductase and SOD) in Oryzaativa, thereby protecting the plants from oxidative burst (Pandand Patra, 2007). However, contrary to this observation, Choudhurynd Panda (2004) reported a decline in the activities of the antiox-dant enzymes CAT, POX, SOD and glutathione reductase in riceollowing the pre-sowing seed-soaking treatment with salicyliccid.

.1. Biotic stress

Plants continuously remain exposed to the challenging threatsf a variety of pathogenic attacks. However, in order to defendhemselves against these attacks, plants have evolved various con-titutive and inducible mechanisms, one such mechanism beinghe accumulation of large quantities of salicylic acid. This notions supported by the observations of Malamy et al. (1990), wherearge amounts of salicylic acid accumulated in the leaves of TMV-esistant tobacco variety Nicotiana tabaccum cv. Xanthi nc, uponnoculation with TMV. A similar increase in the endogenous SA level

as observed in the phloem sap of cucumber plants, infected witholletotrichum lagenarium, Pseudomonas syringae or tobacco necro-is virus (Metraux et al., 1990; Rasmussen et al., 1991; Smith et al.,991).

These findings open a new window for the role to exogenouspplication of salicylic acid in providing tolerance to the plantsgainst various pathogens. The involvement of exogenous SA inefense signaling has been characterized and well documented inany dicotyledonous plants. The exogenous application of salicylic

cid and acetyl salicylic acid was found to induce resistance againstobacco mosaic virus (TMV) in tobacco (Antoniw and White, 1980).urther, salicylic acid or acetyl salicylic acid when applied exoge-ously induced the expression of PR (pathogenesis related) genesnd also conferred resistance against various pathogens of viral,acterial, oomycete and fungal origin in a variety of dicot plantsMalamy and Klessig, 1992; Silverman et al., 1995; Ryals et al., 1996;hah and Klessig, 1999) and in monocot plants (Wasternack et al.,994; Kogel et al., 1994; Gorlach et al., 1996; Morris et al., 1998;asquer et al., 2005; Makandar et al., 2006).

Singh et al. (2004) reported that salicylic acid activated a cas-ade of events resulting in the inhibition of viral replication andheir cell-to-cell and long distance transmission in plants. Loweroncentrations of salicylic acid were found to enhance the depo-

ition of callose plugs in Arabidopsis which contributed to thelant defense system (Kohler et al., 2002). Lamb and Dixon (1997)eported that salicylic acid causes an increase in the accumula-ion of H2O2 in plant tissues which plays a key role in initiatingypersensitive responses and providing SAR against pathogenic

rimental Botany 68 (2010) 14–25

microbes. Salicylic acid is found to alter the activity of a mitochon-drial enzyme, alternative oxidase, which mediates the oxidation ofubiquinol/ubiquinone pool and reduction of oxygen to water, with-out the synthesis of ATP in mitochondria and this altered activity ofenzyme alternative oxidase affects the ROS levels in mitochondriaand in turn induces an antiviral defense response in plants (Singhet al., 2004).

Salicylic acid has an affinity to bind with the enzymes like CAT,APX, aconitase and carbonic anhydrase (Chen et al., 1993; Durnerand Klessig, 1995; Ruffer et al., 1999; Slaymaker et al., 2002) andsome of these enzymes are involved in ROS metabolism and inredox 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-tion, which plays a key role in initiating defense response (Andersonet al., 1998) and induction of SAR in plants when challenged withpathogens (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 metalstress

Among the naturally occurring elements, 53 are considered tobe heavy metals and a few of them have got some biological sig-nificance for plants (Weast, 1984). However, the heavy metalslike cadmium, if present in elevated levels in agricultural soils,are easily assimilated by plants and induce serious visible andmetabolic perturbations e.g. leaf roll, chlorosis, growth reductionin root and shoot, browning of leaf tips (Kahle, 1993), decrease innutrient uptake (Sandalio et al., 2001), altered nitrogen metabolism(Boussama et al., 1999), inhibition of stomatal opening (Barcelo andPoschenrieder, 1990), disruption of membrane composition andfluidity (Quariti et al., 1997), decrease photosynthetic rate (Stobortet al., 1985; Padmaja et al., 1990; Gadallah, 1995) and disruptionof ATPase activity (Fodor et al., 1995). In addition to these haz-ards Cd hinders the development of chloroplasts (Stoyanova andMerakchiiska-Nikolova, 1992; Stoyanova and Tchakalova, 1997)and also affects the activities of two main photosynthetic enzymesRubisco 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 inplants has been reported by many workers. Mishra and Choudhuri(1999) observed that SA pre-treatment alleviated the lead and mer-cury induced membrane disruptions in rice. Further, exogenoussalicylic acid was found to alleviate the toxic effects generated byCd 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 toxicitythat was mediated by an increase in citrate efflux in the roots ofthe treated plants (Yang et al., 2003). Similarly, exogenous salicylicacid protected barley plants from lipid peroxidation, induced by Cdstress, thereby increased the fresh mass of roots and shoots and thiseffect of SA was mediated by suppressing the cadmium-inducedup-regulation of H2O2 metabolizing 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 leadand mercury in rice (Mishra and Choudhuri, 1999). These authorsreported deterioration of the membranes in the leaves of rice dueto 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 ofM. sativa from oxidative damage induced by mercury. The authorsreported that this protection from oxidative damage was medi-ated by an increased activity of various antioxidant enzymes. A

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imilar ameliorative role of salicylic acid was observed in soybeaneedlings exposed to cadmium toxicity (Drazic and Mihailovic,005). In a study carried out by Drazic et al. (2006), the pre-sowingeed-soaking treatment with lower concentrations of salicylic acidnhanced the growth of root and shoot of alfalfa plants, which wasnhibited by cadmium exposure. Further, the treatment was foundo maintain the ionic homeostasis in the seedlings of M. sativaalfalfa). Pre-sowing seed treatment with salicylic acid alleviatedhe inhibitory effects of cadmium on the activities of enzymes RUBParboxylase and PEP carboxylase and also enhanced the activitiesf antioxidative enzymes APX and SOD with a concomitant reduc-ion in the activities of enzyme CAT in maize plants (Krantev etl., 2008). A significant improvement in growth parameters wasecorded with a concomitant reduction in the rate of cadmium-nduced lipid peroxidation and electrolyte leakage in maize plants,aised from the seeds soaked in salicylic acid (Krantev et al., 2008).imilarly, Choudhury and Panda (2004) investigated the ameliora-ive role of SA on cadmium-induced oxidative stress in roots of O.ativa. Their study revealed that Cd toxicity resulted in the loss oflongation growth and biomass of roots with a concomitant accu-ulation of cadmium in them, thereby, generating oxidative stress

n plants. However, the pre-sowing seed-soaking treatment withalicylic acid, decreased the toxic effects, generated by cadmiumnd was manifested in the form of lowered level of lipid peroxi-ation, lesser production of H2O2, reduction in the generation ofuperoxide radicals and maintaining the stability of membranes.hi and Zhu (2008) reported that exogenous SA alleviated the tox-city generated in Cucumis sativus by manganese exposure and theesponse was mediated by reduction in ROS level and lipid per-xidation. The antioxidant enzymes also showed varied responseollowing the SA treatment e.g. CAT and APX activities were reducedhereas, SOD, POX, dehydroascorbate reductase (DHAR) and GR

ctivities were enhanced.A decline in the activities of enzymes CAT, POX, SOD and glu-

athione reductase was observed in the plants treated with SAompared to the untreated plants of O. sativa (Choudhury andanda, 2004). However, contrary to this, higher activities of CAT,OD, glutathione reductase and guaiacol peroxidase were observedn the plants of O. sativa, raised from the seeds primed with sali-ylic acid. The treatment of salicylic acid also lowered the level ofhiobarbituric acid reactive substances (TBARS), H2O2 and O2

− inice, thereby provided additional tolerance to the plants againstxidative stress generated by cadmium exposure (Panda and Patra,007).

.2.2. Effect of exogenous SA on plants grown under salinity stressA high salinity induces serious metabolic perturbations in

lants, as it generates ROS which disturb the cellular redox systemn favour of oxidized forms thereby creating an oxidative stress that

ay damage DNA, inactivate enzymes and cause lipid peroxida-ion (Smirnoff, 1993). However, a large body of literature indicateshat exogenous application of salicylic acid to the stressed plantsan potentially alleviate the toxic effects, generated by salinity. Annhanced tolerance against salinity stress was observed in wheateedlings raised from the grains soaked in salicylic acid (Hamadand Al-Hakimi, 2001). Similar observations were also made inomato plants raised from the seeds soaked in salicylic acid and wasresumed to be due to the enhanced activation of some enzymesiz. aldose reductase and ascorbate peroxidase and to the accumu-ation of certain osmolytes such as proline (Tari et al., 2002, 2004;zepesi et al., 2005).

Accumulation of large amounts of osmolytes (proline) is andaptive response in plants exposed to stressful environmentsRai, 2002). Wheat seedlings accumulated large amounts of prolinender salinity stress which was further increased when salicyliccid was applied exogenously, thereby alleviating the deleterious

rimental Botany 68 (2010) 14–25 19

effects of salinity (Shakirova et al., 2003). The exogenous applica-tion of salicylic acid prevented the lowering of IAA and cytokininlevels in salinity stressed wheat plants resulting in the better-ment of cell division in root apical meristem, thereby increasinggrowth and productivity of plants (Shakirova et al., 2003). Theseauthors also reported that the pre-treatment with SA resulted inthe accumulation of ABA which might have contributed to thepre-adaptation of seedlings to salinity stress as ABA induces thesynthesis of a wide range of anti-stress proteins, thereby providingprotection to the plants. Further, the treatment also lowered thelevel of active oxygen species and therefore the activities of SODand POX were also lowered in the roots of young wheat seedlings(Shakirova et al., 2003). These findings indicate that the activities ofthese antioxidant enzymes are directly or indirectly regulated bysalicylic acid, thereby providing protection against salinity stress(Sakhabutdinova et al., 2004). Exogenous application of salicylicacid enhanced the photosynthetic rate and also maintained thestability of membranes, thereby improved the growth of salin-ity stressed barley plants (El Tayeb, 2005). The damaging effectsof salinity were also alleviated by exogenous application of SA inArabidopsis 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 (chlorophylla, b and carotenoids) in wheat seedlings, under both saline andnon-saline conditions. The loss of growth, photosynthetic parame-ters and the activities of enzymes (nitrate reductase and carbonicanhydrase) as a result of salinity stress in B. juncea was revivedwhen salicylic acid was sprayed to the foliage, at 30 days stage.Further the activities of various antioxidant enzymes (CAT, POX andSOD) were increased with a concomitant increase in proline con-tent as a result of salinity exposure and/or SA treatment, therebyproviding enhanced tolerance against salinity stress (Yusuf et al.,2008).

7.2.3. Effect of exogenous SA on plants grown under temperaturestress7.2.3.1. Heat stress. Deviation from optimum temperature result’sin serious perturbations in plant growth and development whichmay be due to membrane disruptions, metabolic alterations andgeneration of oxidative stress (Mittler, 2002; Posmyk and Janas,2007).

However, salicylic acid plays a key role in providing toleranceagainst temperature stress. A foliar spray of lower concentrationsof salicylic acid conferred heat tolerance to mustard. Further thistreatment, accompanied with hardening at 45 ◦C for 1 h enhancedthe H2O2 level and also reduced the CAT activity, thereby increasingthe potential of plants to withstand the heat stress (Dat et al., 1998).A similar response was observed in potato plantlets, raised fromthe cultures, supplemented with lower concentrations of acetylsalicylic acid (Lopez-Delgado et al., 1998). Larkindale and Huang(2004) pointed out that the enhanced heat tolerance in plants ofAgrostis stolonifera, pre-treated with salicylic acid was due to theprotection of plants from oxidative damage. These authors furtherreported that the pre-treatment with salicylic acid had no effecton POX activity, whereas, the CAT activity declined, compared tocontrol. However, the treatment enhanced the activity of enzymeascorbate peroxidase. Contrary to this, an enhanced activity of CATand SOD was observed in heat stressed plants of Poa pratensis, afterthe 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 Cicerarietinum which was significantly reduced by the application ofSA, compared to the heat acclimatized and untreated control. Thetreatment also enhanced the protein and proline contents signif-icantly with a concomitant induction of various stress enzymes

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.2.3.2. Cold stress. Besides providing tolerance to the plantsgainst heat shock, exogenous salicylic acid also generates resis-ance towards chilling or cold stress. Janda et al. (1997, 1999)eported an enhanced cold tolerance in maize plants, grown inydroponic solutions, supplemented with 0.5 mM of salicylic acid.he treatment positively affected various parameters of fluores-ence and lowered those associated with electrolyte leakage. Aecline in CAT activity with a concomitant enhancement in thectivities of glutathione reductase and guaiacol peroxidase waslso observed. Besides, salicylic acid, its analogues like benzalde-yde aspirin or coumaric acid also had a protective role againsthilling stress in maize plants (Janda et al., 1998, 2000; Horvatht al., 2002). However, it should be underlined here, that SA or itsnalogues may exert deleterious effects on plants under normalrowth conditions. A decline in net photosynthetic rate, stomatalonductance and transpiration rate was observed in maize plantsfter 1 day of SA, benzaldehyde (BA) or aspirin treatment underormal growth conditions (Janda et al., 1998, 2000). The chilling

njury manifested in the form of electrolyte leakage in leaves wasignificantly reduced following the application of lower concentra-ions of salicylic acid to maize, cucumber and rice plants (Kang andaltveit, 2002). However, the extent of electrolyte leakage from thexcised radicals of cold stressed maize seedlings was not alteredignificantly by SA pre-treatment. Other studies have shown thathe addition of salicylic acid to the hydroponic solution may causeevere damage to roots (Pal et al., 2002) indicating a toxic effectenerated by SA.

Exogenous salicylic acid potentially alleviates the damagingffects of low temperatures in rice and wheat (Szalai et al., 2002;asgin et al., 2003), bean (Senaratna et al., 2000) and banana (Kangt al., 2003a). Pre-treatment with salicylic acid activated variousntioxidant enzymes in maize (Janda et al., 1999, 2000) and bananaKang et al., 2003b) exposed to chilling stress. Further the increasen the activities of antioxidant enzymes, SOD, CAT and APX fol-owing SA treatment was related to H2O2 metabolism produced byhilling, thereby providing tolerance against the stress (Kang et al.,003b). Pre-treatment with salicylic acid or its analogues was foundo affect the seed germination as well. SA or acetyl salicylic acidnhanced the germination percentage of carrot seeds (Rajasekarant al., 2002) and in the seeds of Capsicum annum at low tempera-ures (Korkmaz, 2005). Tasgin et al. (2003) reported that exogenousA not only provided protection against heat and cold stresses,ut was equally beneficial in providing tolerance against freezingFrost) injury to winter wheat.

.2.4. Effect of exogenous SA on the plants exposed to UVadiation or ozone stress

The level of UV radiations in the environment is increasing dayy day and the plants, which use direct sunlight for photosynthe-is are unable to avoid UV radiations which imparts adverse effectsn photosynthesis and other physiological processes (Rajendirannd Ramanujam, 2003). Similarly, ozone is the other most dam-ging air pollutant generated through photochemical reactionsetween nitrogen oxides, carbon monoxide and hydrocarbons,eleased during the burning of fossil fuels in urban areas (Mauzerallnd Wang, 2001) and is responsible for tremendous loses to ourrops. Prolonged chronic exposure to ozone results in the inhi-ition of photosynthesis, premature senescence, altered biomass

artitioning ultimately reducing the growth and yield of plantsBlack et al., 2000; Pell et al., 1997; Saitanis and Karandinos, 2002;andermann, 1996). Therefore, the mechanisms which may pro-ect the plants from the harmful effects of UV-exposure or ozonetress are of particular concern. It has been reported earlier that

rimental Botany 68 (2010) 14–25

plants accumulated large amounts of salicylic acid when exposedto ozone or UV radiations (Yalpani et al., 1994; Sharma et al., 1996).The role of salicylic acid in counteracting the damaging effectsof ozone was best demonstrated in Arabidopsis thaliana, whereNahG mutants, deficient in SA biosynthesis were more sensitiveto the deteriorating effects of ozone (Sharma et al., 1996). Since,SA improved the activity of antioxidant enzyme system, therefore,lead to enhanced tolerance against ozone stress in NahG mutants ofArabidopsis (Rao and Davis, 1999). Like ozone, UV radiations werealso reported to induce the accumulation of SA in tobacco plantsand this increased accumulation of SA was probably due to higheractivity of the enzyme BAZ-hydroxylase, which is involved in SAbiosynthesis (Yalpani et al., 1994). In a study carried out by Ervinet al. (2004), the exogenous application of salicylic acid alleviatedthe damaging effects induced by UV-B radiation exposure in Ken-tuky blue grass and tall fescue sod. These studies revealed that thetreatment enhanced photochemical efficiency and the activities ofantioxidant enzymes CAT and SOD which were greatly reducedby UV-B exposure. The treatment also increased the anthocyaninand �-tocopherol contents in the UV-B stressed plants treated withsalicylic acid. Thus, it may be concluded that SA plays promotingrole in alleviating the damaging effects of ozone and/or ultravioletirradiance.

7.2.5. Effect of exogenous SA on plants exposed to water stressExposure of plants to water stress leads to serious physiolog-

ical and biochemical dysfunctions including reduction in turgor,growth, photosynthetic rate, stomatal conductance and damagesof cellular components (reviewed by Janda et al., 2007).

A survey of literature indicates that salicylic acid plays a keyrole in providing tolerance to the plants, exposed to water stress(drought or flooding). Hayat et al. (2008) studied the growth ofwater stressed L. esculentum (tomato) plants in response to exoge-nously applied salicylic acid. The results of their experimentsrevealed a significant decline in photosynthetic parameters, mem-brane stability index, leaf water potential, activities of the enzymesnitrate reductase and carbonic anhydrase, chlorophyll and rela-tive water contents with a concomitant increase in proline contentand 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 aforesaidparameters thereby improved tolerance of the plants to droughtstress. Higher tolerance to drought stress was also observed inthe plants raised from the grains soaked in aqueous solution ofacetyl 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 droughtin tomato and bean plants, whereas, higher concentrations did notshow fruitful results (Senaratna et al., 2000). Leaf senescence is ahighly regulated physiological process, allowing the remobilizationof stored food from the older leaves to the rest of the plant, duringstressful conditions and salicylic acid is involved in the promotionof drought-induced leaf senescence in Salvia officinalis plants grownunder drought stress in Mediterranean field conditions (Abreu andMunne-Bosch, 2008). However, the authors also pointed out thatSA regulates the leaf senescence in association with other phyto-hormones.

The results reported by Singh and Usha (2003) revealed thatthe wheat seedlings subjected to drought stress when treated withsalicylic 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-trol. Further, the treatment also provided a considerable protectionto the enzyme nitrate reductase thereby maintained the normallevel of various proteins in the leaves (Singh and Usha, 2003).

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xogenous application of salicylic acid also alleviated the damag-ng effects of water deficit on cell membranes of barley plants andoncomitantly increased the ABA content in leaves, which mightave contributed to the enhanced tolerance of plants to watercarcity (Bandurska and Stroinski, 2005). Besides providing toler-nce to plants against drought stress, the exogenous applicationf SA was also found to be effective in providing resistance to thelants against the excessive water stress as was observed in celluspensions prepared from the fully turgid leaves of Sporobcdustapfianus (Ghasempour et al., 2001).

. Conclusions

It may be concluded from the above discussion that salicylic acidcts as a potent plan growth regulator that can effectively modulatearious plant growth responses.

Exogenous application of salicylic acid enhances the growth andproductivity of plants.The flower inducing domain of salicylic acid makes it an importphytohormone that can enhance flowering in a variety of orna-mental plants.Exogenous application of salicylic acid induces the SAR in plants,thereby provides a considerable protection against various bioticstress.Besides providing protection against infections and pathogenattacks, SA imparts tolerance against various abiotic stresses tothe plants.SA effectively alleviated the toxic effects generated in plants dueto the exposure to various abiotic stresses viz. Heavy metals, tem-

perature, water, ozone, UV irradiance and salinity stress etc.Exogenous application of the lower concentrations of salicylicacid proved to be beneficial in enhancing the photosynthesisgrowth and various other physiological and biochemical char-acteristics of plants.

on the induction of biotic and abiotic stress tolerance.

• However, at higher concentrations, SA itself may cause a highlevel 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 nitratemetabolism under stressful environments.

• It interferes the indeterminate nodule formation in leguminousplants, whereas, subsequent nodule development is not hindered.

9. Future perspectives

Hence, it may be resolved from the survey of literature citedabove that salicylic acid play’s diverse physiological roles in plantsand potentially alleviates the devastating effects generated byvarious biotic and abiotic stresses. However, this recently intro-duced phytohormone still demands a lot of work to be carriedout to elucidate the exact pathways of its biosynthesis; weathermajor or minor, key regulatory points of biosynthesis, mecha-nism of action and other specific and collaborative regulatory rolesplayed by salicylic acid that have remained elusive till date. Thework is also needed on how this plant hormone interacts andbeing regulated by the cross-talk in harmony with other estab-lished phytohormones and plant growth regulators working at longrange (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 shortrange phytohormones mostly produced in-vicinity to biotic infes-tation and then transported systemically to play their role duringbroad range abiotic stresses. It is also worthwhile to elucidate therole of aforesaid phytohormone in tissue-specific differentiationand growth of plant parts during growth and development. Bio-

chemical inhibitors of key enzymes of pathways and mutant studymight incident some light on such aspects. Locating tissue-specificconcentrations during seedling development fusing with reportergenes or radioactive molecules could pave the way in this con-cern. In future, the exogenous application of this phytohormone

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ight act as a powerful tool in enhancing the growth, produc-ivity and also in combating the ill effects generated by variousbiotic stresses in plants (Fig. 1). The future applications of thislant hormone holds a great promise as a management tool forroviding tolerance to our agricultural crops against the aforesaidonstrains consequently aiding to accelerate potential crop yield inear future.

eferences

breu, M.E., Munne-Bosch, S., 2008. Salicylic acid may be involved in the regulationof drought-induced leaf senescence in perennials: a case study in field-grownSalvia officinalis L. plants. Environ. Exp. Bot. 64 (2), 105–112.

libert, G., Ranjeva, R., 1971. Recharches sur les enzymes catalysant la biosynthesedes acides phenoliques chez Quarcus pedunculata (Ehrn): I—formation des seriescinnamique et benzoique. FEBS Lett. 19, 11–14.

libert, G., Ranjeva, R., 1972. Recharches sur les enzymes catalysant la biosynthesesdes acid phenoliques chez Quarcus pedunculata (Ehrn): II—localization intercel-lulaire de la phenylalanin mmonique-lyase, de la cinnamate 4-hydroxylase, etde la “benzoote synthase” Biochem. Biophys. Acta 279, 282–289.

lverez, A.L., 2000. Salicylic acid in machinery of hypersensitive cell death and dis-ease resistance. Plant Mol. Biol. 44, 429–442.

nandhi, S., Ramanujam, M.P., 1997. Effect of salicylic acid on black gram (Vignamungo) cultivars. Ind. J. Plant Physiol. 2, 138–141.

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