Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants

17 Pages·2015·2.17 MB·English

by  Naser A. Anjum

REVIEW
published:30June2015
doi:10.3389/fpls.2015.00462
Salicylic acid-induced abiotic stress
tolerance and underlying
mechanisms in plants
M.IqbalR.Khan1,MeharFatma1,TasirS.Per1,NaserA.Anjum2*andNafeesA.Khan1
1DepartmentofBotany,AligarhMuslimUniversity,Aligarh,India,2CentreforEnvironmentalandMarineStudies,Department
ofChemistry,UniversityofAveiro,Aveiro,Portugal
Abiotic stresses (such as metals/metalloids, salinity, ozone, UV-B radiation,
extreme temperatures, and drought) are among the most challenging threats
to agricultural system and economic yield of crop plants. These stresses (in
isolation and/or combination) induce numerous adverse effects in plants, impair
biochemical/physiological and molecular processes, and eventually cause severe
reductions in plant growth, development and overall productivity. Phytohormones
Editedby:
have been recognized as a strong tool for sustainably alleviating adverse effects
ZuhuaHe,
of abiotic stresses in crop plants. In particular, the significance of salicylic acid
ShanghaiInstituteforBiological
Sciences–ChineseAcademy (SA) has been increasingly recognized in improved plant abiotic stress-tolerance
ofSciences,China
via SA-mediated control of major plant-metabolic processes. However, the basic
Reviewedby:
biochemical/physiological and molecular mechanisms that potentially underpin SA-
VasileiosFotopoulos,
CyprusUniversityofTechnology, induced plant-tolerance to major abiotic stresses remain least discussed. Based on
Cyprus recent reports, this paper: (a) overviews historical background and biosynthesis of SA
FangChen,
underboth optimal and stressful environments in plants;(b) critically appraises therole
YaleUniversity,USA
*Correspondence: ofSAinplantsexposed tomajor abioticstresses; (c)cross-talks potentialmechanisms
NaserA.Anjum, potentially governing SA-induced plant abiotic stress-tolerance; and finally (d) briefly
CentreforEnvironmentalandMarine
highlightsmajoraspectssofarunexploredinthecurrentcontext.
Studies,DepartmentofChemistry,
UniversityofAveiro,3810-193
Keywords:abioticstress,crop-loss,phytohormones,salicylicacid,stresstolerancemechanisms
Aveiro,Portugal
[email protected]
Introduction
Specialtysection:
Thisarticlewassubmittedto
AbioticStresses andSalicylicAcidasaMajorStress Impact-Mitigation
PlantPhysiology,
asectionofthejournal Tool inPlants
FrontiersinPlantScience Abiotic stress has now been recognized as the biggest and potential threat for agricultural
Received:23January2015 productivity all over the world. Nevertheless, anthropogenic activities in the developmental
Accepted:11June2015 era have aggravated the degradation of agricultural system and its productivity due to major
Published:30June2015 abiotic stressessuch assuchasmetals/metalloids (hereafter termed as‘metal/s’),salinity, ozone,
Citation: UV-Bradiation,extremetemperatures,nutrient(deficiencyandexcess),anddrought(Khanand
KhanMIR,FatmaM,PerTS, Khan, 2013; Anjum et al., 2014a). In fact, the imposed abiotic stresses can potentially influence
AnjumNAandKhanNA(2015) almost all physiological, biochemical, and molecular processes in plants from the early stage of
Salicylicacid-inducedabioticstress
seed germination to maturity, and eventually cause severe losses in the economic yield of crop
toleranceandunderlyingmechanisms
plants. It has been projected that abiotic stresses may adversely affect 70% yield of staple food
inplants.
crops (Kaur et al., 2008; Mantri et al., 2012). In one of the estimates of U.S. Environmental
Front.PlantSci.6:462.
doi:10.3389/fpls.2015.00462 Action Group, the toxicity caused by varied metals has been one of the major concerns to the
FrontiersinPlantScience|www.frontiersin.org 1 June2015|Volume6|Article462
Khanetal. SAandplant-abioticstress-tolerance
agriculture system and health of more than 10 million people SA-involvement in mitogen-activated protein kinase (MAPK)
in eight countries (such as China, Dominican Republic, India, regulation,andintheexpressionandactivationofnon-expressor
Kyrgyzstan, Peru, Russia, Ukraine, and Zambia; ENS, 2006). ofpathogenesis-relatedgenes1(NPR1)hasbeenevidenced(Chai
In addition, increasing salinization of arable land is expected etal.,2014).Nevertheless,thetranscriptionalreprogramingthat
to result in 30% land-loss by the end of 2028 and 50% by occurs during the plant defense response against biotic and
mid of the 21st century (Wang et al., 2003). Notably, the rise abiotic stress was reported to be modulated by SA, where the
in CO concentration by about 500–1000 ppm by the year transcriptionofdifferentsetsofdefensegenescanbecontrolled
2
2100 has been projected to cause an increase in the mean in a spatio-temporal manner via SA-mediated mechanisms
◦
temperature by approximately 3 C(Khanetal.,2013a).Hence, (Herrera-Vásquezetal.,2015).
together with salinization of arable land, drought, nutrients- In order to develop ideotypes for sustainable agriculture as
unavailability, metal toxicity, and climate change have been wellastoimproveoverallplantperformanceintheconditionsof
expected to significantly aggravate the problem (Anjum et al., thechangingclimateandtheincreasedseverityofabioticstresses,
2014a). it would be imperative to exploit the information available on
Plantgrowthregulatorsplayimportantrolesintheregulation theinvolvementofSAinabioticstresstoleranceinplants.Inthe
of plant developmental processes and signaling networks as currenteffort,inadditiontooverviewinghistorical background
they are involved either directly or indirectly in a wide range andbiosynthesisofSAinplantsunderbothoptimalandstressful
of biotic and abiotic stress responses and tolerance in plants environments,theroleofSAinplantsexposedtomajorabiotic
(Khan et al., 2012a,b,c; Asgher et al., 2015). Salicylic acid (SA) stress conditions is critically discussed, potential mechanisms
is a phenolic compound involved in the regulation of growth controlling SA-induced plant abiotic stress-tolerance are cross-
and development of plants, and their responses to biotic and talked,andmajoraspectssofarunexploredinthecurrentcontext
abioticstressfactors(Raskin,1992;Khanetal.,2012a,b,c,2013b; arebrieflyhighlighted.
Miura and Tada, 2014). SA is involved in the regulation of
important plantphysiological processessuchasphotosynthesis,
Salicylic Acid: Historical Background and
nitrogen metabolism, proline (Pro) metabolism, production of
glycinebetaine (GB), antioxidant defense system, and plant- Biosynthesis
water relations under stress conditions and thereby provides
protection in plants against abiotic stresses (Khan et al., 2010, Centuries ago Americans, Indians, and Greeks used willow
2012a,b,c, 2013b, 2014; Nazar et al., 2011; Miura and Tada, tree bark and leaves to cure aches and fevers, but it has
2014). Apart from its involvement in the induction of defense- beendocumentedthatHippocratesprescribedthecompoundto
related genes and stress resistance in biotic stressed plants relieve pain for women during child birth and fever was later
(Kumar, 2014), SA has been shown to improve plant tolerance recognized as SA. Ancient texts also indicate that Babylonians,
to major abiotic stresses such as metal (Zhang et al., 2015), Assyrians, and Chinese (Sharp, 1915) used willow (Salix sp.)
salinity (Khan et al., 2014; Nazar et al., 2015), osmotic (Alavi bark and leaves for medicinal purposes. The importance of
et al., 2014), drought (Fayez and Bazaid, 2014), and heat stress willow (Salix sp.) bark has also been shown in 1763 when
(Khanetal.,2013b).ExogenouslysourcedSAtostressedplants, the Reverend Edward Stone informed the Royal Society that
either through seed soaking, adding to the nutrient solution, it contained substances that relieved the symptoms of “ague”
irrigating, or spraying was reported to induce major abiotic (probablymalarialfever)effectively.Until19thcenturytheactive
stress tolerance-mechanisms (Horváth et al., 2007; Khan et al., principle of willow was not known, but later on the salicylates,
2012a,b,c, 2013b, 2014; Anwar et al., 2013; Palma et al., 2013). methyl salicylate (MeSA), saligenin (alcohol of SA), and their
SA influences plant functions in a dose dependent manner, glycosideswereisolatedfromextractsofwillowandotherplants.
whereinducedorinhibitedplantfunctionscanbepossiblewith TheSAwasisolatedandpurifiedfromwillowandmeadowsweet
low and high SA concentrations, respectively. For example, in in the first half of the 19th century (Leroux, 1830) and was
Matricariachamomilla,50and250μMSAconcentrations were chemicallysynthesizedbythecarboxylationofsodiumphenoxide
reported to, respectively, promote and inhibit growth (Kovácˇik in1860(KolbeandLautemann,1860).In1928,JohannBuchner,
etal.,2009).Inanotherinstance,0.1and0.5mMSApromoted a German scientist for the first time isolated SA from willow
photosynthesis and growth of Vigna radiata but an inhibited barkunderthename“salicin” (the glucosideofsalicylalcohol),
growth was evidenced with 1.0 mM SA (Nazar et al., 2011). whichwasthemajorsalicylateinwillowbark(Weissmann,1991).
Besidesthe concentration of SA,the duration of the treatment, ThenameSA(Clelandand Ajami,1974)isoriginated from the
plant species, age, and treated plant organ can also influence LatinwordSalixandwasgiventotheactiveingredientofwillow
theSA-effectsinplants(Shietal.,2009;MiuraandTada,2014). (Salix sp.) bark by Raffaele Piria in 1838. The first commercial
Recent molecular studies have established that SA can regulate production ofsynthetic SAbeganinGermanyin1874.Aspirin,
many aspects in plants at gene level, and thereby can improve a trade name for acetylsalicylic acid, was introduced by the
plant-abiotic stresstolerance.SAwasreportedtoinduceseveral BayerCompanyin1898andrapidlybecameoneofworld’sbest-
genes responsible for encoding chaperone, heat shock proteins selling drugs and it replaced the use of SA by producing less
(HSPs),antioxidants,andsecondarymetabolites[sinapylalcohol gastrointestinal irritation yet has similar medicinal properties.
dehydrogenase(SAD),cinnamylalcoholdehydrogenase(CAD), With the further advancement in scientific research in 20th
and cytochrome P450; Jumali et al., 2011]. Additionally, century,usesofSAasatreatmentforacne,psoriasis,warts,and
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Khanetal. SAandplant-abioticstress-tolerance
calluses became common. The use of SA as a skin softener, for by cinnamic acid either via β-oxidation of fatty acids or a
removal of dead skin cells, dirt, oil and debris and cleaning of non-oxidative pathway (Verberne et al., 1999; Mustafa et al.,
poresiswidespread.Inspiteofthefactthatthemodeofmedicinal 2009). Cinnamate 4-hydroxylase (C4H) catalyzes the second
actionofsalicylatesisasubjectofcontinualdebate,theyarebeing step in the pathway during the conversion of cinnamic acid to
usedtotreathumandiseasesrangingfromthecommoncoldto coumaric acid. Cinnamic acid is produced from phenylalanine
heartattacks.AsaspirinundergoesspontaneoushydrolysistoSA, by the action of enzyme phenylalanine ammonialyase (PAL).
thetwocompoundshavesimilareffectsinplants. Cinnamicacidishydroxylatedtoformcoumaricacidfollowedby
Salicylic acid is a seven carbon (C) containing, naturally oxidation of the side chain, and further hydroxylated and form
occurring phenolic compound and endogenously synthesized SA. In the third pathway, SA biosynthesis in plants has been
signalingmoleculeinplants.Theshikimicacidpathwayandthe reportedfromshikimicacidviachorismicacidandcomaricacid
malonic acid pathway are the two main pathways known to be (Horváthetal.,2007;AnandMou,2011;Figure1).
involved in the synthesis of plant phenolics. The shikimic acid Multiple abiotic stress factors have been evidenced to
pathway takes part in the biosynthesis of most plant phenolic modulate major enzymes involved in plant-SA biosynthesis.
compounds. It simply converts simple carbohydrate precursors Overproduction of SA via enhanced activity of SA biosynthetic
derived from glycolysis and pentose phosphate pathway to the pathway enzymes(mainlyisochorismate synthase,ICS;PAL)in
aromatic amino acids including SA precursor, phenylalanine plants helps in their protection against environmental stresses.
(Herrmann and Weaver,1999). The most common pathway in TheseenzymesarekeyregulatorsofSAfunctionsandareknown
plants for SA synthesis is phenylalanine pathway; however, SA tobemodulatedbydifferentabiotic andbioticstressfactors. In
biosynthesismayalsobeaccomplishedbyisochorismatepathway Arabidopsis,ICShasbeenfoundtobeinvolvedinthebiosynthesis
(Kawano et al., 2004; Mustafa et al., 2009). SA is produced of SA during plant defense process (Wildermuth et al., 2001).
after aseriesof chemicalreactions catalyzed bymanyenzymes. SynthesisofSAfollowingexposure toozoneinArabidopsiswas
Thehydroxylation ofbenzoicacidcatalyzedbyenzymebenzoic alsosuggestedtoinvolveICS(Ogawaetal.,2005).SAapplication
acid 2-hydroxylase synthesizes SA. Benzoic acid is synthesized can positively regulate ICS1 and improve drought tolerance in
FIGURE1|Amodelofsalicylicacid(SA)biosynthesispathwaystartingfromShikmicacidandaccomplishedbythreedifferentpathways.
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Khanetal. SAandplant-abioticstress-tolerance
plants such as Arabidopsis thaliana (Hunter et al., 2013). In SA enhanced the activity of sulfur (S) assimilation pathway
addition,mutantstudyonArabidopsis(ics1andics2)confirmed enzyme (serine acetyltransferase; SAT), glutathione (GSH)
that in the absence of ICS1, ICS2 can encode a functional ICS content and eventually increased Ni-resistance. Exogenous SA
enzyme but in limited amounts (Garcion et al., 2008). Under (3.0 mM)enhanced OsWRKY45 gene expression and increased
salt stress, high expression of ICS and C4H enzymes can be endogenous content of SA. It has been shown that increased
correlatedtothelevelofappliedSAconcentration. Tothisend, endogenousSAlevelpreventedmembranedamagebylowering
with 1.0 mM SA, induction of ICS and C4H was higher than H O content in Cd-exposed O. sativa (Chao et al., 2010).
2 2
thatobservedwith0.1mMinCarthamustinctorius.Theisolated Involvement of SA (0.5 mM) in the phytochelatins (PCs)-
genesofICSandC4HinC.tinctoriuswereconsideredsignificant mediated protection of Z. mays was evidenced against Cd-
for bothsaltstresstolerance andpathogenresistance (Dehghan toxicity (Szalai et al., 2013). SA can also significantly inhibit
etal.,2014). The involvementof enhanced PAL activity inheat Fe-deficiency-causedchlorosisinplants(Kongetal.,2014).
and chilling tolerance was documented in Musa plants (Chen
et al., 2008). Both Cd and Pb were reported to induce mRNA SalinityStress
coding for PAL in Glycine max (Pawlak-Sprada et al., 2011). Ithasbeenestimatedthatabout45millionhectaresofirrigated
Isolation and profiling of PAL and CHS in salinity exposed land have been damaged by salinity stress worldwide and
C.tinctoriusplantssuggestedthatthesetwoenzymeswerehighly considerableareaoflandaffectedbysalinityisincreasingdayby
responsiveto1.0mMSA(vs.0.1mMSA;Dehghanetal.,2014). day worldwide (Pitman and Lauchli, 2002; Munns and Tester,
Recently,bothwaterdeficitandUV-Bradiationwerereportedto 2008).Infact,thelossofplantproductivityduetosalinitystress
cause SA accumulation as a result of increased activity of PAL is a consequence of imbalance in cellular ionic and osmotic
and benzoic acid hydroxylase (BA2H; Bandurska and Cieslak, balances (Khan et al., 2012b). Major adverse effects of salinity
2013). stressincludeincreasediontoxicity,osmoticstress,andnutrient-
acquisition and homeostasis/deficiency, impaired stomatal
conductance, increased cell-turgor loss, decreased reduction in
Salicylic Acid and Abiotic
leafwaterpotential,alteredphysiological/biochemical processes,
Stress-Tolerance in Plants and elevated ROS-caused oxidative stress (Munns and Tester,
2008; Nazar et al., 2011; Khan et al., 2014). The role of SA
Metals/Metalloids in strengthening salinity stress-tolerance mechanisms has
Metal/metalloid-accrued stress has become a subject of great been extensively evidenced in many crops including Vicia
concern to sustainable agriculture and environmental system. faba (Azooz, 2009), Brassica juncea (Nazar et al., 2011, 2015),
Agricultural soils can receive metal pollutants from multiple Medicagosativa(Palmaetal.,2013),andV.radiata(Khanetal.,
pathwaysincludingindustrialeffluents,burningliquidandsolid 2014).
fuel, urban run-off, sewage waste disposal, agricultural toxic Salicylic acid was reported to induce salinity tolerance
chemicals run-off, domestic garbage dump etc. Literature is and increased biomass of Torreya grandis as a result of
full on the significance of SA in the minimization of metal- enhanced chlorophyll content and the activity of antioxidant
accruedstress-impacts.ExogenouslyappliedSAwasreportedto enzymes that eventually activated the photosynthetic process
improvegrowthandphotosynthetic traitsinseveralcropplants and alleviated oxidative stress (Li et al., 2014). SA-deficiency
includinglead[Pb−(0.05,0.15,0.25mmolL−1)]exposedOryza in plants was considered as a major reason of salinity-accrued
sativa (Chen et al., 2007), Cd (10, 15, and 25 μM)-exposed increased damages and diminished activity of antioxidant
Zea mays (Krantev et al., 2008), and Cu (0.05, 0.10, 0.15, and enzymes in SA-deficient NahG transgenic of Arabidopsis lines
0.20 mM)-exposed Phaseolus vulgaris (Zengin, 2014). Applied (Cao et al., 2009). NaCl-accrued oxidative stress in Hordeum
SA was evidencedto modulate antioxidant system-components vulgare was minimized by SA (50 μM)-mediated decrease in
and significantly decrease membrane lipid peroxidation in to cellular malondialdehyde (MDA, a marker of membrane-lipid
Cu-exposedP.vulgaris(Zengin,2014)andPb-exposedO.sativa peroxidation) andROS(suchasH O ;FayezandBazaid,2014;
2 2
(Chen et al., 2007). Recent evidences also suggested that SA Khanetal.,2014).SA-primingcanbeanimportantstrategyfor
is an important regulator of photosynthesis, photosystem II enhancingmajorGSH-basedH O -metabolizingenzymesuchas
2 2
(PSII), photosynthetic pigments, and the activity of enzymes GST.Tothisend,SAmitigatedsalinitystress-injuryinSolanum
suchasRubiscoandcarbonicanhydraseundermetalstress(Al- lycopersicumbycausingcharacteristicchangesintheexpression
Whaibi et al., 2012; Noriega et al., 2012; Zhang et al., 2015). patternofGST-genefamilymemberssuchasSlGSTT2,SlGSTT3,
Recently, an increased tolerance of Linum usitatissimum to Cd SlGSTF4(Csiszáretal.,2014).ExogenouslysourcedSA(0.5mM)
was attributed to SA-mediated control of H O accumulation was reported to improve salt tolerance in Triticum aestivum
2 2
(Belkadhi et al., 2014). Ni-impact-mitigation role of SA can duetoanenhancedtranscriptlevelofantioxidantgenes;GPX1,
differ in plants exhibiting a differential Ni-accumulation. To GPX2, DHAR, GR, GST1, GST2, MDHAR, and GS, and an
thisend,SA-biosyntheticpathwaycompoundsanditsderivative increasedactivityofascorbate(AsA)-GSHpathwayenzymes(Li
metabolites (phenylalanine, cinnamic acid, salicyloyl-glucose, et al., 2013). In another instance, SA-mediated restoration of
+
and catechol) were elevated in the hyperaccumulator Thlaspi membranepotentialandpreventionofsalt-inducedK -lossviaa
goesingense compared to the non-accumulators A. thaliana and GORKchannel,andeventuallyimprovedsalinity-tolerancewere
T. arvense (Freeman et al., 2005). Further, the presence of evincedinA.thaliana(Jayakannanetal.,2013).
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Khanetal. SAandplant-abioticstress-tolerance
Ozone Stress and protect membranes and important metabolic enzymes
Ozone is among the major components of photochemical air (Mohammed and Tarpley, 2009a). SA-mediated activation of
pollution responsible for causing significant damage to both antioxidant enzymes was considered as a major factor for
cultivated plants and forest trees (Wang et al., 2007). Ozone SA-mediated regulation of UV-induced oxidative stress in
enters to mesophyll cells via stomata where it immediately Capsicum annuum leaves (Mahdavian et al., 2007). Increased
interacts with water and other cellular components to generate photosynthetic rate,pollenviability,leafphenolicconcentration
phytotoxicity mainly by elevating the generation of ROS (such and yield in UV-B stressed-O. sativa was also reported
asO·−,H O ,.OH,and1O ),andtriggeringaseriesofsignaling (MohammedandTarpley,2013).SAcandecreaseUV-Bcaused
2 2 2 2
cascades and plant defense responses (Long and Naidu, 2002; chromosome aberration level in the meristematic root tip cells
Ashmore, 2005). Extensive reports are available on the key (Ranceliene and Vyšniauskiene˙, 2012). Exogenously applied SA
regulatory roles of SA in plant-ozone stress tolerances (Yalpani was reported to significantly improve photosynthetic function
et al., 1994; Sharma et al., 1996; Yoshida et al., 2009; Khan and its related variables in UB-B exposed plants (Karioti et al.,
etal.,2012a;Páletal.,2014).SAcan workasasignalmolecule 2008;Lietal.,2014).Earlier,UV-Cradiationwasalsoreportedto
and promote molecular and physiological changes in ozone- upregulatethetranscriptionoftheSAinductiondeficient2gene
exposed plants (Tamaoki, 2008). Moreover, SA is required to codingfortheSAbiosyntheticisochorismatesynthase1enzyme
potentiate the antioxidant response, maintain cellular redox (Martinezetal.,2004).Additionally,SA-dependentpathwaywas
state,andactivateprocessesagainsthypersensitivecelldeathand reportedtocontroltheup-regulationofthepathogenesis-related
ozone-sensitivity (Rao and Davis, 1999). SA was reported to (PR)proteins(PR-1,PR-2,andPR-5)inUV-B-exposedtransgenic
maintainplantgrowth,developmentandcellularredoxsystemby NahGA.thalianaplants(Surplusetal.,1998).
activatingtheGSH-biosyntheticpathway(Yoshidaetal.,2009).
Temperature Stress
In ozone-exposed A. thaliana, SA was involved in the
accumulation of defense-related transcripts and induced Inthecurrentchangingenvironmentalscenario,bothlow(cold
resistance (Sharmaetal.,1996).SAisalsoinvolvedinsignaling andchillingstress)andhigh(heat)temperatureshavebecomea
network integrating other phytohormones such as JA and/or potentialabioticstress-threattocropplants.Temperaturestress
ethylene in ozone-exposed plants (Rao et al., 2002). Notably, affectsmanyplant-physiological andbiochemical processesand
both SA and ethylene were evidenced by these authors to act inducesmolecularmechanismsandgeneexpressiontomodulate
in concert to regulate ozone-induced cell death in A. thaliana. plants responses (Larkindale and Knight, 2002; Khan et al.,
In the same plant, ozone-mediated induced biosynthesis of JA 2013a,b; Kazemi-Shahandashti et al., 2014; Siboza et al., 2014).
or methyl jasmonate was reported to attenuate SA-dependent SA-supplementation has been reported to differentially benefit
lesion-initiationthateventuallywasconsideredasamajorfactor severalplantspeciesexposedtolow/chillingtemperatures(Janda
forthedecreasedlesionscausedbyozone(Raoetal.,2000).Ithas et al., 1999; Ding et al., 2002; Horváth et al., 2002; Kang et al.,
alsobeenevidencedthatozone-accruedSA-accumulationcanbe 2012;Kazemi-Shahandashtietal.,2014;Sibozaetal.,2014)and
promoted by ethylene-mediated regulation of the expression of high(Heetal.,2002;LarkindaleandKnight,2002;Clarkeetal.,
the PAL and chorismate mutase (CM) genes in ozone-exposed 2004;Shietal.,2006;WangandLi,2006;Wangetal.,2010;Khan
Nicotianatabacum(Ogawaetal.,2005).Inanotherstudy,ozone- et al., 2013a,b). SA (0.5 mM) modulated antioxidant enzymes
sensitivity in hybrid poplar was correlated with insensitivity to (suchasascorbateperoxidase,APX;superoxidedismutase,SOD;
both SA and jasmonic acid, where these phytohormones were guaiacolperoxidase,GPOX;GSHreductase,GR)andimproved
◦
associated with the programmed cell death in lesion formation chlorophyllfluorescenceinZ.maysunderlow(2 C)temperature
(Kochetal.,2000). stress(Jandaetal.,1999).ExogenouslySAcaninhibittheactivity
of isozymes (CAT-1 and CAT-2) of catalase (CAT) which in
UV-BRadiation turncanmediateresponsesofZ.maystolowtemperaturestress
The effects of increased UV-B radiation (280–320 nm) on (Horváthetal.,2002).
plant growth and development raised concerns on the need Salicylic acid (2.0 mM)-mediated increased synthesis of
of protection mechanisms (Caldwell et al., 2007; Gill et al., total phenolics and the activity of PAL were reported to
2015). Increased UV-B level can significantly diminish crop improve chilling tolerance in cold-stored lemon fruit (Citrus
productivity by inhibiting PSII, electron transport systems, limon; Siboza et al., 2014). Mutlu et al. (2013) reported
photosyntheticrate,photosyntheticpigments,nucleicacids,and that exogenously sourced SA results in cold tolerance by
biomassaccumulationandpartitioning(SullivanandTeramura, enhancing antioxidant enzymes, ice nucleation activity, and
1989;MohammedandTarpley,2009a,b,2011).ExposuretoUV- the patterns of apoplastic proteins in H. vulgare genotypes. In
B radiation can decrease the expression and synthesis of key another report, SA significantly protected ultra-structures in
photosyntheticproteinssuchaschlorophylla/b-bindingproteins Musa acuminata seedlings under chilling stress (Kang et al.,
(Lhcb) and the D1 polypeptide of PSII (psbA; Jordan, 1996; 2012). Leastreports are available in literature on the molecular
Jordanetal.,1998).SignificantinductioninSA-accumulationwas mechanisms underlying SA-mediatedimproved plant tolerance
evidenced in UV radiation-exposed plants (Fodor et al., 1997; to cold/chilling temperature. Increased chilling tolerance was
Horváthetal.,2002). evidenced in chilling-exposed S. lycopersicum fruit as a result
ExogenouslyappliedSAwasreportedtomodulateantioxidant of low concentrations of (0.01 mM) MeSA-mediatedinduction
levels, detoxify superoxide radicals, prevent oxidative damage, in the synthesis of some stress proteins, such as PR proteins
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Khanetal. SAandplant-abioticstress-tolerance
(Ding et al., 2002). The applied MeSA significantly increased metabolite biosynthesis, such as SAD, CAD, and Cytochrome
accumulationofPR-2bandPR-3amRNAsbutslightlyincreased P450(CYP)respondedtoSAtreatment.Theauthorscorrelated
PR-3bmRNAaccumulation(Dingetal.,2002). the gene-expression-responses to SA with signaling pathway in
Salicylic acid-mediated improved plant tolerance to heat plants under drought stress condition. SA (0.5 mM)-mediated
stress has also been reported (He et al., 2002; Larkindale et al., significantly improved growth in drought-exposed T. aestivum
2005; Wang et al., 2010; Khan et al., 2013a,b). Larkindale and seedlings was argued as a result of SA-mediated enhancements
Knight(2002)reportedthatthetransgenicArabidopsisseedlings in the transcription of GST1, GST2, GR, MDHAR genes (Kang
showing a bacterial SA-decomposing salicylate hydroxylase etal.,2013).SA-accumulatingmutants(cpr5andacd6)exhibited
were less tolerant to heat stress. SA signaling played an stomatalclosureandimproveddroughttoleranceinA.thaliana
important role in the acquisition of Ocimum basilicum to by SA-mediated induced expression of PR genes (PR1, PR2,
heat (Clarke et al., 2004). SA application increased antioxidant and PR5; Liu et al., 2013). SIZ1-mediated endogenous SA-
system in Vitis vinifera and induced activity of APX, GR, and accumulationwasreportedtoplayanimportantroleinstomatal
monodehydroascorbate(MDHA),increasedredoxratiosofAsA closureanddroughttoleranceinA.thaliana(Miuraetal.,2013).
and GSH, and maintained Ca2+-homeostasis were reported in Potential involvement of SA in the 76 identified proteins was
SA-supplementedandcold/heattreatedV.vinifera(WangandLi, reported in drought-exposed T. aestivum (Kang et al., 2012).
2006).SA(1.0 mM)decreasedelectrolyte leakageandoxidative Theses identified proteins were advocated to perform major
stress, and improved maximum yield of PSII, Fv/Fm, and the physiological functions such as photosynthesis, carbohydrate
quantum yield of the PSII electron transport in Cucumis sativa metabolism, protein metabolism, stress and defense, energy
seedlings after both heat stress and recovery (Shi et al., 2006). production, signal transduction, and toxin metabolism. Some
Recently, Khan et al. (2013b) have shown that treatment of of the recent studies have shown that SA played significant
0.5mMSAcanalleviateheatstressinT.aestivumbyincreasing role at different concentration by regulating many metabolic
Pro-production and restriction of the stress ethylene formation mechanisms(Table1).
underheatstress.Notably,thedetailsofthemechanismsofheat
stressmitigationwiththeapplicationofSAarenotavailableand
Potential Mechanisms Underlying
the area could be an open challenge at both physiological and
molecularlevels. SA-Mediated Plant Stress-Tolerance
Drought Stress In order toenlighten the potential mechanisms underlying SA-
Drought has been considered as one of the most acute abiotic mediatedimprovedabioticstresstoleranceinplants,thissection
stresses presently affecting agriculture. Drought stress can briefly appraises recent reports available on the interaction
significantly reduce photosynthesis and stomatal conductance, of SA with major osmolytes, mineral nutrients, secondary
inhibit photosynthetic pigments synthesis and ultimately lead metabolites, and other phytohormones, and SA-involvementin
to reduction in growth of plants (reviewed by Hasanuzzaman ROS-signalingandthemodulationofantioxidants.
et al., 2013). SA (500 μM)-supplementation to drought
stressed H. vulgare resulted in increased net CO assimilation InteractionofSAwithOsmolytes
2
rate due to increased stomatal conductance and eventually To counteract the adverse effects of abiotic stresses-induced
in increased plant dry mass (Habibi, 2012). Exogenously excess ROS production, plants have developed mechanisms
applied SA can modulate important enzymatic (including facilitating their adaptation to osmotic and ionic stresses.
monodehydroascorbate reductase, MDHAR; dehydroascorbate Nevertheless, to maintain osmotic balance plants have well
reductase, DHAR; GR; GSH peroxidase, GPX) and non- developed protective mechanism termed as osmoregulation
enzymatic(including GSH)components ofAsA–GSHpathway, mediatedbyosmolytessuchGB,Pro,solublesugars,aminesetc.
and also glyoxalase system (Gly I and Gly II) and decrease Thesecompoundsdonotinterferewiththeotherplantmetabolic
oxidative stress in drought-exposed plants (Alam et al., 2013). processes and contribute to the turgor-maintenance in stressed
Foliar application of SA (1.0 μM) strengthened antioxidant plants(MisraandSaxena,2009).
defense system in drought-tolerant Z. mays cultivar to a great Glycinebetaineisconsideredasaneffectivecompatiblesolute
extent(vs.drought-sensitivecultivar;Saruhanetal.,2012).Low for osmotic adjustment and protection against osmotic stress
membranelipidperoxidationbutincreasedplantheightanddry (Munns,2005),saltstress(Khanetal.,2014),andalsotostresses
mass,andlesswiltingofleaveswerereportedindrought-exposed causedbyheat(Wangetal.,2010)andmetals(Bharwanaetal.,
andSA(0.5mM)-supplementedT.aestivumKangetal.(2012). 2014). The accumulation of GB in stressed plants adjusts cell
Recently, SA-biosynthetic enzymes (such as CS and ICS) were osmotic balance, stabilizes membrane integrity, prevents the
not correlated with the SA level, but ortho-hydroxy-cinnamic dissociation of polypeptides from the PSII complex, protects
(oHCA)wascorrelatedwithSAbiosynthesis andplayedcrucial Rubisco activity, and also detoxifies toxic ions (Ashraf and
roleindroughttoleranceinO.sativa(Páletal.,2014). Foolad, 2007). Notably, SA and its analog aspirin can induce
Theapplicationof5.0μMSAinducedtheexpressionofgenes GB-accumulation in the range of 0.5–2.5 mM in plants at
inMitragynaspeciosa(Jumalietal.,2011).Amongtheanalyzed high levels of NaCl, drought, and cold stresses (Jagendorf and
292 expressed sequence tags (ESTs) randomly, the most of the Takabe, 2001). The effectiveness of both salicylate and aspirin
genesthatencodechaperone,HSPs,antioxidantsandsecondary in the induction of GB-accumulation is a part of systematic
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Khanetal. SAandplant-abioticstress-tolerance
TABLE1|Summaryofrepresentativestudiesonsalicylicacid(SA)-mediatedcontrolofmajorabioticstress-impactsinplants.
Plantname AppliedSA Parametersstudied Response Reference
concentration
Saltstress
Viginaradiata 0.5mM Glycinebetaine(GB)production,netphotosynthesis,plantdrymass + Khanetal.(2014)
Torreyagrandis 0.5mM Chlorophyllcontent,netCO2assimilationrates,prolinecontent + Lietal.(2014)
Glycinemax 0.5mM Na+/K+ratio − Ardebilietal.(2014)
G.max 0.5mM Superoxidedismutaseactivity,ascorbatecontent + Ardebilietal.(2014)
Hordeumvulgare 0.05mM MDAcontent,Na+/K+ratio − FayezandBazaid(2014)
10−4mM ContentandactivityofRubisco,Rubiscoactivase + Leeetal.(2014)
Cadmiumstress
Cucumismelo 0.1mM Photosynthetic + Zhangetal.(2015)
capacity,PSIIphotochemistryefficiency,wateruseefficiency
Brassicajuncea 1.0mM Mineralnutrientscontent + Ahmadetal.(2011)
G.max 120mM Superoxidedismutaseactivity,chlorophyll,GSHcontent, + Noriegaetal.(2012)
heme-oxygenase-1activity,relativeproteinamount
Poapratensis 0.5mM Nutrientelementscontent(K,Ca,Mg,andFe) + Guoetal.(2013)
P.pratensis 0.5mM Cduptake − Guoetal.(2013)
RicinusCommunis 0.5mM Gasexchange,chlorophyllcontent − Liuetal.(2011)
Nickelstress
Catharanthusroseus 10−5M Contentofalkaloidsvincristineandvinblastine + Idreesetal.(2013)
Chillingstress
Punicagranatum 1and2mM Totalphenolics + MirdehghanandGhotbi(2014)
Citruslimon 2mM Totalphenolics,activityofphenylalanineammonialyase(PAL) + Sibozaetal.(2014)
Musaacuminata 0.5mM Ultrastructureofchloroplastofmesophyllcells,mitochondriaof + Kangetal.(2007)
mesophyllcells
Coldstress
H.vulgare 0.1mM Apoplasticantioxidativeenzymes,icenucleationactivity,patternof + Mutluetal.(2013)
apoplasticproteins
Heatstress
Triticumaestivum 0.5mM Prolinecontent,glutamylkinaseactivity,gasexchange,water + Khanetal.(2013b)
potential
Droughtstress
Zeamays 0.001mM Leafrollingdegree,waterpotential,dryweight + Saruhanetal.(2012)
Simaroubaglauca 0.05mM Polyphenol,alkaloids,flavonoidcontent + AwateandGaikwad(2014)
UV-Bstress
G.max 0.5mM Wateruseefficiency,Fv/Fm + Lietal.(2014)
G.max 0.5mM Flavonoidcontent − Lietal.(2014)
Oryzasativa 12.9gha−1 PSIIactivity,cropgraincharacteristics,totalphenolics + MohammedandTarpley(2013)
+,−symbolsindicateincreaseordecrease,respectively.
acquiredresistanceandcouldbeanimportantpartofthereason alleviationofsalinity-induced adverseeffects onphotosynthesis
for its induction in plants under NaCl-, drought-, and cold andgrowth.
stresses-plants. The induction of GB might have other effects The accumulation of another major osmolyte Pro is one
as well, such as activation of protein kinase when aroused by of the adaptive mechanisms that plants operate for survival
hyperosmotic stress (Hoyos and Zhang, 2000). SA-mediated especiallyundersalinity/osmoticstressconditions.Prodetoxifies
increase in GB-level can improve overall plant growth (Misra excessROS,adjustscellularosmoticbalance,protects biological
and Misra, 2012). The increase in GB content led to the membranes,andstabilizesenzymes/proteins(Iqbaletal.,2014).
increase in biomass of Rauwolfia serpentina. Recently, Khan Researches have well documented that SA is involved in
et al. (2014) have shown that alleviation of salinity-inhibited increasing Pro metabolism under abiotic stresses (Misra and
photosynthesis and growth by SA involves GB in V. radiata. Saxena, 2009; Khan et al., 2013b). SA (at 0.5 mM) significantly
It was shown that SA (at 0.5 mM) induced GB-accumulation inducedactivityofProbiosynthesisenzymes(suchaspyrroline-
through increased methionine content and suppressed excess 5-carboxylate reductase and γ-glutamyl kinase) under salinity
ethylene formation under salinity stress. Similar effect was stressalongwiththeincreasedProcontent.ThisincreaseinPro
observed by these authors with the application of SA-analog, metabolism was attributed to salinity stress tolerance in Lens
2, 6, dichloro-isonicotinic acid on GB accumulation and esculenta (Misra and Saxena, 2009). Misra and Misra (2012)
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Khanetal. SAandplant-abioticstress-tolerance
haveshownthatup-regulationofProbiosynthesisenzymes(such B. juncea by upregulating the assimilation of S. Exogenously
as pyrroline-5-carboxylate reductase and γ-glutamyl kinase) sourced SA (seed-soaked or soil-incorporated) can improve
and down-regulation of Pro oxidase activity were responsible overall plant growth under B-toxicity and salinity stress by
for increased Pro level. In turn, the increased Pro level was stimulating the accumulation of mineral elements including K,
advocatedtothemaintenanceofthecellturgorinR.serpentina Mg,Mn,N,andP(Gunesetal.,2005).
under salinity stress. SA-treatment (0.5 mM) alleviated heat Calcium is one of the important nutrient elements known
stress in in T. aestivum by increasing Pro-production as for various structural roles under both optimal and stressful
a result of SA-mediated increase in γ-glutamyl kinase and conditions in plants (White and Broadley, 2003). Literature
decrease in Pro oxidase activity (Khan et al., 2013b). Increased supports a close link betweenSA and Ca (and Ca-signaling) in
Pro production was argued to improve nitrogen assimilation stressed plants (Liu and Zhu, 1997; Kawano et al., 1998; Chen
and to alleviate the heat stress-impact on photosynthesis. In et al., 2001, 2011; Yang and Poovaiah, 2002; Du et al., 2009).
contrast, exogenous Pro-application was evidenced earlier to Interaction between SA and Ca2+ signaling might be involved
induceSAproduction(mediatedbyNDR1-dependentsignaling in defense mechanisms induced by stress and maintenance
+ −
pathway) and was shown to modulate calcium (Ca)-mediated of K /Na ion selectivity (Liu and Zhu, 1997; Chen et al.,
oxidative burst defense response in plants (Chen et al., 2001). SA and Ca (alone or in combination) can markedly
2011). improvesalinitytoleranceinplantsviaincreasingProlevel(Al-
Accumulation of soluble sugars and sugar alcohol mannitol Whaibi et al., 2012). Involvement of Pro in the induction of
hasalsobeenreported tocontribute inplant stresstolerance as Ca-mediated oxidative burst and SA signaling has also been
osmoprotectants (Murakeözy et al., 2003; Cheng et al., 2009). reported (Chen et al., 2011). A range of abiotic/environmental
SA was reported to inhibit valine and sucrose uptake in a stresses (such as high temperature, UV-B stress, or salt stress)
concentration-dependent manner (10–200 μM; Bourbouloux can induce the expression of Genes encoding calmodulin-
et al., 1998). Improved plant health can also be achieved bindingprotein(Ca-containingprotein).Ontheotherhand,SA
with increased contents of polysaccharides and soluble sugars, was reported to induce calmodulin-binding proteins in abiotic
respectively,with100μmolL−1 (Yuanetal.,2014),and0.5and stressed A. thaliana (Yang and Poovaiah, 2002). Ca-dependent
1.0mMSA(Luoetal.,2014). protein kinases (CDPKs) have been shown to be involved in
abioticstressresponsesandmayalsobeinducedbySA(Chung
Interaction ofSA withMineral Nutrients etal.,2004;Leclercqetal.,2005).Kawanoetal.(1998)reported
Mineral nutrition is a basic requirement for proper growth thatSA-inducedarapid andtransient generationofsuperoxide
and development and survival under different environmental anion followed by a transient increase in cytosolic free Ca ion
stress conditions. Studies have shown that mineral nutrient concentrationinN.tabacum.Khokonetal.(2011)reportedthat
+
status in plants plays a critical role in the alleviation of abiotic SAfailedtoinduceCa-Cytoscillationsinguardcells;whereas,K
stress (Iqbal et al., 2011; Nazar et al., 2011, 2015). SA can channelactivity wassuppressed bySAand lead tothe stomatal
significantly modulatethe uptake and metabolism ofimportant closure.
mineralelementsandtherebyimprovegrowthanddevelopment
inabioticstressedplants(AlpaslanandGunes,2001;Gunesetal., Involvement ofSAinROS-Signalingandthe
2007; Chen etal.,2011; Khokon etal., 2011;Wang etal.,2011; Modulation ofAntioxidants
·−
Tufailetal.,2013;Nazaretal.,2015).Inaddition,theprotective The generation and scavenging of varied ROS such as O ,
2
•
roleofSAinmembraneintegrityandregulationofionsincluding H O ,and OHareusualinthe normalaerobicmetabolism in
2 2
nutrients uptake has also been reported (Alpaslan and Gunes, plants.Notably,importantsignaltransducingrolesandtriggering
2001;Gunesetal.,2007). and/ororchestratingplantresponsestovariedstressfactorscan
Salicylic acid can be involved in the regulation of uptake be possible with the minimal levelsof ROS. However, (abiotic)
of several plant-beneficial elements such as Mn, Ca, Cu, Fe, P, stresses cause imbalance between generation and scavenging of
and Zn and thereby minimize oxidative stress under Pb stress ROS, and eventually lead to a physiological condition known
(Wang et al., 2011). SA-mediated changes in photosynthesis as oxidative stress. Thus, a number of consequences such as
were attributed to the nutrients content of N, P, K, and Ca oxidative modification of vitalbiomolecules, celldeath,and the
in B. juncea cultivars differing in salt tolerance (Syeed et al., arrest of plant growth and development can be possible under
2011).Inparticular,0.5mMSAincreasedphotosynthesisunder uncontrolledoxidativestress(GillandTuteja,2010;Anjumetal.,
+ −
salt stress by decreasing cellular Na and Cl ions, and 2012).
increasing the content of nutrients. Earlier, strongly inhibited Apoplastic-ROS have been found as regulators of cell death
+ −
Na and Cl accumulation but stimulated N, Mg, Fe, Mn, through their interplay with several other signaling pathways
and Cu concentrations were reported in SA-supplemented and including SA-mediated signaling pathways (Overmyer et al.,
salinity stressed Z. mays (Gunes et al., 2007). In another work, 2003). Both endogenous and exogenous SA was evidenced to
+ +
SA (0.5 mM)-mediated maintenance of higher K /Na and play roles in antioxidant metabolism and have a tight control
Ca2+/Na+ ratios was considered as a major factor underlying overcellularROS(Kangetal.,2014;Khanetal.,2014).However,
SA-assisted improved growth, gas exchange, yield, and salinity the coordination of SA-dependent and independent signaling
tolerance in Z. mays (Tufail et al., 2013). Recently, Nazar et al. componentswithROS-signalingprovidedanappropriatedefense
(2015) demonstrated that SA can improve salinity tolerance in response. SA can act as a signal for the development of the
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Khanetal. SAandplant-abioticstress-tolerance
systemic acquired resistance (Shirasu et al.,1997), and can also applied SA-induced SOD activity accompanied an increase in
induce the activation of a protein kinase (Mikolajczyk et al., shootCa2+(asecondmessenger)andcausedatransientincrease
2000).SAwasevidencedasamajorsignalingmoleculerequired inH O whichinturnwasarguedtoinduceantioxidantenzymes
2 2
foragonizingozone-inducedGSH-baseddefensegeneexpression andeventuallytodecreaseincellularROS(Arfan,2009).
in A. thaliana (Rao and Davis, 1999). A. thaliana plants were
able to recognize the response of ROS–SA interaction via an InteractionofSAwithMajor Secondary
antagonistic action of SA and SA-signaling on apoplastic ROS- Metabolites
signaling(XuandBrosché,2014).SA-signalingexceptfrom the Secondarymetabolites,substancesbiosyntheticallyderivedfrom
well-documented role in the regulation of defense responses primary metabolites, produced by plants as defense chemicals
was also evidenced to be involved in the regulation of light- and are not involved in plant metabolic activity. Examples of
acclimation processes and thereby influencing photosynthetic secondary metabolites include including terpenes, phenolics,
function (Mullineaux and Karpinski, 2002; Gawron´ski et al., and compounds with N (alkaloids, cyanogenic glucosides, non-
2013). protein amino acids) and S (GSH,glucosinolates, phytoalexins,
Involvement of SA in the modulation of antioxidant thionins,defensins,andallinin;Irchhaiyaetal.,2015).Secondary
metabolism hasbeenwidelyreportedtocontrol plant-tolerance metabolites have also been established as beneficial for plants
to major abiotic stresses including ozone, UV-B, heat, metal, tolerance under biotic and abiotic stress (Ramakrishna and
and osmotic stress (Wang et al., 2010; Nazar et al., 2011; Khan Ravishankar,2011).
etal.,2012a,b,c,2013a,b,2014).SA-pretreatmentwasevidenced Extensive reports are available on the direct and indirect
toalleviatetheadverseeffectsofsalinitystressonphotosynthesis involvementofSAintheinductionofthesecondarymetabolite
and growth in V. radiata through enhancing the activities of synthesis in plants (Kiddle et al., 1994; Ali et al., 2007;
antioxidant enzymes including SOD, CAT, GPX, APX, and GR Idrees et al., 2013). SA-mediated induction of glucosinolates
(Khan et al., 2014). Activities of H2O2-metabolizing enzymes production was reported in Brassica napus (Kiddle et al.,
(such as CAT, POD, and APX) and superoxide-dismutating 1994). Exogenous application of acetyl-SA to tumor lines
enzymes(SOD)werealsomodulatedwithSAinplantsexposed of Catharanthus roseus elevated therein the production of
to drought (Saruhan et al., 2012) and cold (Mutlu et al., 2013). important secondary metabolites such as alkaloids, phenolics,
SA-application (at 0.5 mM) increased activity of enzymes of furanocoumarins, and anthocyanins (Godoy-Hernández and
AsA–GSHpathwayresuledintheincreasedtoleranceofB.juncea Loyola-Vargas, 1997). Recently, in the same plant SA-mediated
to salinity stress (Nazar et al., 2015). AsA and GSH, as redox restorationofNi-inducedinhibitionwasattributedtoSA-assisted
activecompoundshavebeenextensivelyreported tomaintaina improved the content of alkaloids such as vincristine and
homeostaticbalanceofthecellularredoxstate,andareinvolved vinblastine(Idreesetal.,2013).RoleofexogenouslyappliedSA
inprotectivemechanismsagainstbothabioticandbioticstresses wasreportedinUV-BexposedT.aestivum,whereSAincreased
(Anjumetal.,2010,2014b;Noctoretal.,2012;Khanetal.,2015a). the accumulation of anthocyanin and tocopherol, and also
InCd-exposedT.aesticumvarieties,SA-signalingwascorrelated modulatedtheexpressionofPRproteins(Horváthetal.,2007).
with GSH-relatedmechanisms(Kovácsetal.,2014).Exogenous Eliciation in the PALactivity and subsequent increased vanillin
SA (0.5 mM) significantly improved salinity (250 mM NaCl) production were reported in SA-supplemented in C. chinense
toleranceinT.aestivumbymarkedlyincreasingthepoolsofAsA (Rodas-Junco et al., 2013). Foliar application of SA at the
andGSH(Lietal.,2013). rate of 50 mg L−1 induced the level of secondary metabolites
Salicylicacid-mediateddifferentialregulationofthetranscript such coumarins, sterols, xanthoproteins, cardiac glycosides and
levels of the genes encoding AsA–GSH cycle enzymes GPX saponins, and ameliorated water stress in Simarouba glauca
(GPX1), phospholipid hydroperoxide GPX (GPX2),and DHAR (Awate and Gaikwad, 2014). Earlier, SA-mediated improved
(DHAR),GR(GR),GST(GST1andGST2),MDHAR(MDHAR), thermo-tolerance inV.viniferawasadvocatedasaresultofSA-
andGSHsynthetase(GS)wasadvocatedasamajormechanisms inducedaccumulationofPALmRNA,thesynthesisofnewPAL
underlying previous role of SA in salinity tolerance via AsA protein, and significant accumulation of phenolics (Wen et al.,
and GSH (Li et al., 2013). Recently, in S. lycopersicum, SA- 2008). A schematic presentation of SA-mediated metabolisms
priming exhibited a concentration-dependent modulation of responsibleforabioticstresstoleranceisshowninFigure2.
GST-supergene family, where SA-mitigated the salinity stress-
injuryandcausedcharacteristicchangesintheexpressionpattern InteractionofSAwithOtherHormones
ofSlGSTsonlyat10−4Mconcentration(Csiszáretal.,2014).In Manyfactorsareinvolvedinacomplexprocessofplantgrowth
particular, SlGSTF4 displayed a significant up-regulation in the and development. SA can regulate various aspects of plant
leaves,whiletheabundanceofSlGSTL3,SlGSTT2,andSlGSTZ2 responses under both stressful and optimal environments
transcriptswereenhancedintherootsofplantsprimedwithhigh through signaling cross-talks with other phytohormones
SA-concentration. SA-mediated induction in SOD and GSH- (Horváth et al., 2007; Asensi-Fabado and Munné-Bosch, 2011;
based H O −metabolizing enzymesnamelyGPXand GST was Khan et al., 2012a,b, 2013b, 2014). The interaction between SA
2 2
argued to improve in ozone tolerance in plants (Abarca et al., and other phytohormones such as auxin (Iglesias et al., 2011;
2001;Millaetal.,2003).SA(500μM)improvedCd-toleranceand Khan et al., 2012a), cytokinin (Peleg et al., 2011; Khan et al.,
photosyntheticcapacityinhemp(Cannabissativa)byenhancing 2012a), gibberellins (Alonso-Ramírez et al., 2009; Khan et al.,
both SOD and POD (Shi et al., 2009). In another instance the 2012a), abscisic acid (Szepesi et al., 2009; Khan et al., 2012a),
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Khanetal. SAandplant-abioticstress-tolerance
FIGURE2|SimplifiedschemesrepresentingpotentialmechanismsunderlyingSA-mediatedplantabioticstresstolerance.
ethylene (Khan et al., 2012a, 2013b, 2014), nitric oxide (NO; Iglesias et al. (2011). The authors showed that the expression
Khanetal.,2012a;Kongetal.,2014),andbrassinosteroids(Divi of the PR1, a SA-induced gene in tir1 afb2 (auxin perception
etal.,2010;Khanetal.,2012a)hasbeenestablishedunderboth smallfamilyofF-boxproteins)mutantplantsplaysasignificant
normalandstressedconditions. role inauxin-signaling instressedplants.Furthermore,inthese
The outcomes of the SA-interaction with other mutants, PR-1 was induced to a great extent as compared with
phytohormones can be either from synergistic or antagonistic SA-treated wild-type plants, where the negative effect of SA
relation therein under optimal and stressful conditions. SA- on auxin signaling indicates the occurrence of an antagonism
mediated repression of auxin signaling was demonstrated by betweenauxinandSA-signalingpathways(Iglesiasetal.,2011).
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