Skip to main content
Log in

Role of salicylic acid in resistance to cadmium stress in plants

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

We review and introduce the importance of salicylic acid in plants under cadmium stress, and provide insights into potential regulatory mechanisms for alleviating cadmium toxicity.

Abstract

Cadmium (Cd) is a widespread and potentially toxic environmental pollutant, originating mainly from rapid industrial processes, the application of fertilizers, manures and sewage sludge, and urban activities. It is easily taken up by plants, resulting in obvious toxicity symptoms, including growth retardation, leaf chlorosis, leaf and root necrosis, altered structures and ultrastructures, inhibition of photosynthesis, and cell death. Therefore, alleviating Cd toxicity in plants is a major aim of plant research. Salicylic acid (SA) is a ubiquitous plant phenolic compound that has been used in many plant species to alleviate Cd toxicity by regulating plant growth, reducing Cd uptake and distribution in plants, protecting membrane integrity and stability, scavenging reactive oxygen species and enhancing antioxidant defense system, improving photosynthetic capacity. Furthermore, SA functions as a signaling molecule involved in the expression of several important genes. Significant amounts of research have focused on understanding SA functions and signaling in plants under Cd stress, but several questions still remain unanswered. In this article, the influence of SA on Cd-induced stress in plants and the potential regulation mechanism for alleviating Cd toxicity are reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171

    Article  CAS  PubMed  Google Scholar 

  • Agarwal S, Sairam R, Srivastava G, Meena R (2005) Changes in antioxidant enzymes activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes. Biol Plant 49:541–550

    Article  CAS  Google Scholar 

  • Agtuca B, Rieger E, Hilger K, Song L, Robert CA, Erb M, Karve A, Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in regulating leaf physiology, Leaf metabolism, and resource allocation patterns that impact root growth in Zea mays. J Plant Growth Regul 33:328–339

    Article  CAS  Google Scholar 

  • Ali E, Maodzeka A, Hussain N, Shamsi IH, Jiang L (2015) The alleviation of cadmium toxicity in oilseed rape (Brassica napus) by the application of salicylic acid. Plant Growth Regul 75:641–655

    Article  CAS  Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunityF. J Integr Plant Biol 53:412–428

    Article  CAS  PubMed  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Umar S, Iqbal M (2014) Assessment of cadmium accumulation, toxicity, and tolerance in Brassicaceae and Fabaceae plants—implications for phytoremediation. Environ Sci Pollut Res 21:10286–10293

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Asgher M, Khan MIR, Iqbal N, Masood A, Khan NA (2013) Cadmium tolerance in mustard cultivars: dependence on proline accumulation and nitrogen assimilation. J Funct Environ Bot 3:30–42

    Article  Google Scholar 

  • Asgher M, Khan MIR, Anjum NA, Khan NA (2014a) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252:399–413

    Article  PubMed  CAS  Google Scholar 

  • Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014b) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  PubMed  Google Scholar 

  • Astolfi S, Zuchi S, Passera C (2005) Effect of cadmium on H+ ATPase activity of plasma membrane vesicles isolated from roots of different S-supplied maize (Zea mays L.) plants. Plant Sci 169:361–368

    Article  CAS  Google Scholar 

  • Bai X, Dong Y, Kong J, Xu L, Liu S (2014) Effects of application of salicylic acid alleviates cadmium toxicity in perennial ryegrass. Plant Growth Regul 75:695–706

    Article  CAS  Google Scholar 

  • Bansal P, Sharma P, Goyal V (2002) Impact of lead and cadmium on enzyme of citric acid cycle in germinating pea seeds. Biol Plant 45:125–127

    Article  CAS  Google Scholar 

  • Barceló J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37

    Article  Google Scholar 

  • Belkadhi A, De Haro A, Obregon S, Chaïbi W, Djebali W (2015) Positive effects of salicylic acid pretreatment on the composition of flax plastidial membrane lipids under cadmium stress. Environ Sci Pollut Res 22:1457–1467

    Article  CAS  Google Scholar 

  • Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaïbi W, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicol Environ Saf 73:1004–1011

    Article  CAS  PubMed  Google Scholar 

  • Bertoli AC, Cannata MG, Carvalho R, Bastos ARR, Freitas MP, dos Santos Augusto A (2012) Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Ecotoxicol Environ Saf 86:176–181

    Article  CAS  Google Scholar 

  • Chao YY, Chen CY, Huang WD, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337

    Article  CAS  Google Scholar 

  • Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4:493–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho UH, Seo NH (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    Article  CAS  Google Scholar 

  • Choppala G, Saifullah Bolan N, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391

    Article  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot 63:5521–5534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Da Cunha KPV, Do Nascimento CWA (2009) Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Pollut 197:323–330

    Article  CAS  Google Scholar 

  • Davies P (2010) Plant hormones: biosynthesis, signal transduction, action!, revised 3rd edn. Springer, Dordrecht

  • Di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiologiae Plant 35:1281–1289

    Article  CAS  Google Scholar 

  • Djebali W, Hediji H, Abbes Z, Barhoumi Z, Yaakoubi H, Zoghlami LB, Chaibi W (2010) Aspects on growth and anatomy of internodes and leaves of cadmium-treated Solanum lycopersicum L. plants. J Biol Res (Thessaloniki) 13:75–84

    CAS  Google Scholar 

  • Dong J, Wu F, Zhang G (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666

    Article  CAS  PubMed  Google Scholar 

  • Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511–517

    Article  CAS  Google Scholar 

  • Dražić G, Mihailović N (2009) Salicylic acid modulates accumulation of Cd in seedlings of Cd-tolerant and Cd-susceptible soybean genotypes. Arch Biol Sci 61:431–439

    Article  Google Scholar 

  • Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 271:28492–28501

    Article  CAS  PubMed  Google Scholar 

  • Eichhorn H, Klinghammer M, Becht P, Tenhaken R (2006) Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. J Exp Bot 57:2193–2201

    Article  CAS  PubMed  Google Scholar 

  • Ernst WH, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    CAS  PubMed  Google Scholar 

  • Fang Y, Sun X, Yang W, Ma N, Xin Z, Fu J, Liu X, Liu M, Mariga AM, Zhu X (2014) Concentrations and health risks of lead, cadmium, arsenic, and mercury in rice and edible mushrooms in China. Food Chem 147:147–151

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120

    Article  CAS  PubMed  Google Scholar 

  • Gomes MP, Marques TCLLd, e Melo S, Nogueira MDOG, Castro EMD, Soares ÂM (2011) Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Scientia Agricola 68:566–573

  • Gordon L, Minibayeva F, Rakhmatullina D, Alyabyev A, Ogorodnikova T, Loseva N, Valitova Y (2004) Heat production of wheat roots induced by the disruption of proton gradient by salicylic acid. Thermochim Acta 422:101–104

    Article  CAS  Google Scholar 

  • Guan C, Ji J, Jia C, Guan W, Li X, Jin C, Wang G (2015) A GSHS-like gene from Lycium chinense maybe regulated by cadmium-induced endogenous salicylic acid and overexpression of this gene enhances tolerance to cadmium stress in Arabidopsis. Plant Cell Rep 34:871–884

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Liang Y, Zhu Y, Zhao F (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Liang Y, Zhu Y (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J Plant Physiol 166:20–31

    Article  CAS  PubMed  Google Scholar 

  • Guo Q, Meng L, Mao P-C, Jia Y-Q, Shi Y-J (2013) Role of exogenous salicylic acid in alleviating cadmium-induced toxicity in Kentucky bluegrass. Biochem Syst Ecol 50:269–276

    Article  CAS  Google Scholar 

  • Hartke S, Da Silva AA, de Moraes MG (2013) Cadmium accumulation in tomato cultivars and its effect on expression of metal transport-related genes. Bull Environ Contam Toxicol 90:227–232

    Article  CAS  PubMed  Google Scholar 

  • Hassan MJ, Shao G, Zhang G (2005) Influence of cadmium toxicity on growth and antioxidant enzyme activity in rice cultivars with different grain cadmium accumulation. J Plant Nutr 28:1259–1270

    Article  CAS  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25

    Article  CAS  Google Scholar 

  • He J, Ren Y, Pan X, Yan Y, Zhu C, Jiang D (2010) Salicylic acid alleviates the toxicity effect of cadmium on germination, seedling growth, and amylase activity of rice. J Plant Nutr Soil Sci 173:300–305

    Article  CAS  Google Scholar 

  • Hédiji H, Djebali W, Cabasson C, Maucourt M, Baldet P, Bertrand A, Zoghlami LB, Deborde C, Moing A, Brouquisse R (2010) Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicol Environ Saf 73:1965–1974

    Article  PubMed  CAS  Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300

    Article  CAS  Google Scholar 

  • Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37

    Article  CAS  Google Scholar 

  • Huang J, Zhang Y, Peng J-S, Zhong C, Yi H-Y, Ow DW, Gong J-M (2012) Fission yeast HMT1 lowers seed cadmium through phytochelatin-dependent vacuolar sequestration in Arabidopsis. Plant Physiol 158:1779–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138

    Article  CAS  PubMed  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

    Article  CAS  Google Scholar 

  • Janda T, Gondor OK, Yordanova R, Szalai G, Pál M (2014) Salicylic acid and photosynthesis: signalling and effects. Acta Physiologiae Plant 36:2537–2546

    Article  CAS  Google Scholar 

  • Janicka-Russak M, Kabała K, Burzyński M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208

    Article  PubMed  CAS  Google Scholar 

  • Kang G, Li G, Liu G, Xu W, Peng X, Wang C, Zhu Y, Guo T (2013) Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. Biol Plant 57:718–724

    Article  CAS  Google Scholar 

  • Kang G, Li G, Guo T (2014) Molecular mechanism of salicylic acid-induced abiotic stress tolerance in higher plants. Acta Physiologiae Plant 36:2287–2297

    Article  CAS  Google Scholar 

  • Kawano T, Bouteau F (2013) Crosstalk between intracellular and extracellular salicylic acid signaling events leading to long-distance spread of signals. Plant Cell Rep 32:1125–1138

    Article  CAS  PubMed  Google Scholar 

  • Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74

    Article  CAS  PubMed  Google Scholar 

  • Kosolsaksakul P, Farmer JG, Oliver IW, Graham MC (2014) Geochemical associations and availability of cadmium (Cd) in a paddy field system, northwestern Thailand. Environ Pollut 187:153–161

    Article  CAS  PubMed  Google Scholar 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931

    Article  CAS  PubMed  Google Scholar 

  • Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674

    Article  PubMed  Google Scholar 

  • Leita L, De Nobili M, Mondini C, Garcia MB (1993) Response of Leguminosae to cadmium exposure. J Plant Nutr 16:2001–2012

    Article  CAS  Google Scholar 

  • Li X, Ma L, Bu N, Li Y, Zhang L (2014) Effects of salicylic acid pre-treatment on cadmium and/or UV-B stress in soybean seedlings. Biol Plant 58:195–199

    Article  CAS  Google Scholar 

  • Liang Y, Chen Q, Liu Q, Zhang W, Ding R (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J Plant Physiol 160:1157–1164

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Qian M, Cai G, Yang J, Zhu Q (2007) Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater 143:443–447

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Guo J, Cui Y, Lü T, Zhang X, Shi G (2011) Effects of cadmium and salicylic acid on growth, spectral reflectance and photosynthesis of castor bean seedlings. Plant Soil 344:131–141

    Article  CAS  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Ueno D, Zhao F-J, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736

    Article  CAS  PubMed  Google Scholar 

  • Macek T, Macková M, Pavlíková D, Száková J, Truksa M, Cundy AS, Kotrba P, Yancey N, Scouten WH (2002) Accumulation of cadmium by transgenic tobacco. Keynote Lect 42

  • Meng H, Hua S, Shamsi IH, Jilani G, Li Y, Jiang L (2009) Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59

    Article  CAS  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz K-J (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz K-J (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    CAS  PubMed  Google Scholar 

  • Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104

    Article  CAS  PubMed  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    Article  CAS  PubMed  Google Scholar 

  • Mouron SA, Grillo CA, Dulout FN, Golijow CD (2004) A Comparative Investigation of DNA Strand Breaks, Sister Chromatid Exchanges and K-Ras Gene Mutations Induced by Cadmium Salts in Cultured Human Cells. Mutat Res 568:221–231

    Article  CAS  PubMed  Google Scholar 

  • Mutlu S, Atici Ö, Nalbantoglu B (2009) Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. Biol Plant 53:334–338

    Article  CAS  Google Scholar 

  • Myśliwa-Kurdziel B, Strzałka K (2002)  Influence of metals on the biosynthesis of photosynthetic pigments. In: Prasad MNV, Strzalka K(eds) Physiologyand biochemistry of metal toxicity andtolerance in plants. Springer, Dordrecht, pp 201–228

  • Nagajyoti P, Lee K, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  Google Scholar 

  • Nan ZR, Li JJ, Zhang JN, Cheng GD (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285:187–195

    Article  CAS  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489

    Article  CAS  Google Scholar 

  • Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora-Morphol Distrib Funct Ecol Plants 204:316–324

    Article  Google Scholar 

  • Noriega G, Caggiano E, Lecube ML, Santa Cruz D, Batlle A, Tomaro M, Balestrasse KB (2012) The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals 25:1155–1165

    Article  CAS  PubMed  Google Scholar 

  • Ouariti O, Gouia H, Ghorbal MH (1997) Responses of bean and tomato plants to cadmium: growth, mineral nutrition, and nitrate reduction. Plant Physiol Biochem 35:347–354

  • Pál M, Szalai G, Horváth E, Janda T, Páldi E (2002) Effect of salicylic acid during heavy metal stress. Acta Biologica Szegediensis 46:119–120

    Google Scholar 

  • Palmgren MG, Harper JF (1999) Pumping with plant P-type ATPases. J Exp Bot 50:883–893

    Article  CAS  Google Scholar 

  • Panda SK, Patra HK (2007) Effect of salicylic acid potentiates cadmium-induced oxidative damage in Oryza sativa L. leaves. Acta Physiologiae Plant 29:567–575

    Article  CAS  Google Scholar 

  • Parida AK, Jha B (2010) Antioxidative defense potential to salinity in the euhalophyte Salicornia brachiata. J Plant Growth Regul 29:137–148

    Article  CAS  Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45

    Article  Google Scholar 

  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231

    Article  CAS  PubMed  Google Scholar 

  • Poschenrieder C, Gunsé B, Barceló J (1989) Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad M (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Prasad MNV (2013) Heavy metal stress in plants: from biomolecules to ecosystems. Springer Science & Business Media, New York

  • Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes (salicylic acid-mediated oxidative damage requires H2O2). Plant Physiol 115:137–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raza SH, Shafiq F (2013) Exploring the role of salicylic acid to attenuate cadmium accumulation in radish (Raphanus sativus). Int J Agric Biol 15:547–552

    CAS  Google Scholar 

  • Recatalá L, Sánchez J, Arbelo C, Sacristán D (2010) Testing the validity of a Cd soil quality standard in representative Mediterranean agricultural soils under an accumulator crop. Sci Total Environ 409:9–18

    Article  PubMed  CAS  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  CAS  PubMed  Google Scholar 

  • Sandalio L, Dalurzo H, Gomez M, Romero-Puertas M, Del Rio L (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24:216–224

    Article  CAS  PubMed  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  Google Scholar 

  • Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161

    Article  CAS  Google Scholar 

  • Seo PJ, Lee A-K, Xiang F, Park C-M (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49:334–344

    Article  CAS  PubMed  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey R (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  CAS  PubMed  Google Scholar 

  • Shi G, Cai Q (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46:627–630

    Article  CAS  Google Scholar 

  • Shi Q, Zhu Z (2008) Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environ Exp Bot 63:317–326

    Article  CAS  Google Scholar 

  • Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48:127–135

    Article  CAS  Google Scholar 

  • Shi G, Cai Q, Liu Q, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiologiae Plant 31:969–977

    Article  CAS  Google Scholar 

  • Sridhar BM, Diehl S, Han F, Monts D, Su Y (2005) Anatomical changes due to uptake and accumulation of Zn and Cd in Indian mustard (Brassica juncea). Environ Exp Bot 54:131–141

    Article  CAS  Google Scholar 

  • Stroiński A, Giżewska K, Zielezińska M (2013) Abscisic acid is required in transduction of cadmium signal to potato roots. Biol Plant 57:121–127

    Article  CAS  Google Scholar 

  • Szalai G, Krantev A, Yordanova R, Popova LP, Janda T (2013) Influence of salicylic acid on phytochelatin synthesis in Zea mays during Cd stress. Turk J Botany 37:708–714

    CAS  Google Scholar 

  • Tamás L, Mistrík I, Alemayehu A, Zelinová V, Bočová B, Huttová J (2015) Salicylic acid alleviates cadmium-induced stress responses through the inhibition of Cd-induced auxin-mediated reactive oxygen species production in barley root tips. J Plant Physiol 173:1–8

    Article  CAS  Google Scholar 

  • Taşgın E, Atıcı Ö, Nalbantoğlu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  PubMed  CAS  Google Scholar 

  • Tóth T, Zsiros O, Kis M, Garab G, Kovacs L (2012) Cadmium exerts its toxic effects on photosynthesis via a cascade mechanism in the cyanobacterium, Synechocystis PCC 6803. Plant, cell & environment 35:2075–2086

    Article  CAS  Google Scholar 

  • Ünyayar S, Değer AG, Çelik A, Çekiç FÖ, Çevik S (2010) Cadmium-induced antioxidant status and sisterchromatid exchanges in Vicia faba L. Turkish Journal of Biology 34:413–422

    Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13(3):195–206

    Article  Google Scholar 

  • Vollenweider P, Cosio C, Günthardt-Goerg MS, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.): part II Microlocalization and cellular effects of cadmium. Environ Exp Bot 58:25–40

    Article  CAS  Google Scholar 

  • Waalkes M (2000) Cadmium carcinogenesis in review. J Inorg Biochem 79:241–244

    Article  CAS  PubMed  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan Z (2013a) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11–20

    Article  CAS  Google Scholar 

  • Wang Q, Liang X, Dong Y, Xu L, Zhang X, Kong J, Liu S (2013b) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. J Plant Growth Regul 32:721–731

    Article  CAS  Google Scholar 

  • Wang X, Zhang Z-W, Tu S-H, Feng W-Q, Xu F, Zhu F, Zhang D-W, Du J-B, Yuan S, Lin H-H (2013c) Comparative study of four rice cultivars with different levels of cadmium tolerance. Biologia 68:74–81

    CAS  Google Scholar 

  • White P, Brown P (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu F, Zhang G, Dominy P (2003) Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environ Exp Bot 50:67–78

    Article  CAS  Google Scholar 

  • Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Dong Y, Kong J, Liu S (2014) Effects of root and foliar applications of exogenous NO on alleviating cadmium toxicity in lettuce seedlings. Plant Growth Regul 72:39–50

    Article  CAS  Google Scholar 

  • Xu L, Fan Z, Dong Y, Kong J, Bai X (2015) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress. Biol Plant 59:171–182

    Article  CAS  Google Scholar 

  • Xue Z-C, Gao H-Y, Zhang L-T (2013) Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol Plant 57:587–590

    Article  CAS  Google Scholar 

  • Yamaguchi H, Nishizawa NK, Nakanishi H, Mori S (2002) IDI7, a new iron-regulated ABC transporter from barley roots, localizes to the tonoplast. J Exp Bot 53:727–735

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Lan C, Wang H, Zhuang P, Shu W (2006) Cadmium in soil–rice system and health risk associated with the use of untreated mining wastewater for irrigation in Lechang, China. Agric Water Manag 84:147–152

    Article  Google Scholar 

  • Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36:1–15

    Article  CAS  PubMed  Google Scholar 

  • Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197

    Article  CAS  Google Scholar 

  • Zhang F, Zhang H, Xia Y, Wang G, Xu L, Shen Z (2011) Exogenous application of salicylic acid alleviates cadmium toxicity and reduces hydrogen peroxide accumulation in root apoplasts of Phaseolus aureus and Vicia sativa. Plant Cell Rep 30:1475–1483

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater 239:302–307

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31401299, 31470368, 31401356), and Zhejiang Provincial Natural Science Foundation of China (LZ14C020001, LY13C020002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cheng Zhu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. Stewart.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Z., Ding, Y., Wang, F. et al. Role of salicylic acid in resistance to cadmium stress in plants. Plant Cell Rep 35, 719–731 (2016). https://doi.org/10.1007/s00299-015-1925-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1925-3

Keywords

Navigation