Foliar application of salicylic acid improves growth and yield attributes by upregulating the antioxidant defense system in Brassica campestris plants grown in lead-amended soils

Mirza Hasanuzzaman, Md. Abdul Matin, Jannatul Fardus, Md. Hasanuzzaman, Md. Shahadat Hossain, Khursheda Parvin

Abstract


Lead (Pb) toxicity causes a severe impact on plant growth and productivity. A protective role of salicylic acid (SA) is well known under different abiotic stress conditions. However, very little is known about the SA-induced Pb resistance mechanism. In this study, we investigated the effect of SA on mustard plants (Brassica campestris L.) under Pb-stress conditions. Plants were exposed to three levels of Pb amendment to the soil (0.25, 0.50, 1.00 mM), with or without SA (0.25 mM). Plant growth, yield attributes, and yield at harvest were reduced depending on the severity of the Pb stress. Exogenous application of SA improved plant growth and yield. Biochemical data revealed that Pb toxicity resulted in higher oxidative damage by reducing nonenzymatic antioxidants such as ascorbate and glutathione at the higher dose of Pb treatment. Antioxidant enzymes (ascorbate peroxidase – APX, monodehydroascorbate reductase – MDHAR, dehydroascorbate reductase – DHAR, glutathione reductase – GR, guaiacol peroxidase – POD, glutathione S-transferase – GST, and catalase – CAT) responses varied with the Pb doses. Both the nonenzymatic and enzymatic components of the antioxidant defense system were upregulated after application of SA, resulting in lower oxidative damage under Pb-stress conditions. Taken together, the results suggest that exogenous application of the SA mitigates Pb-induced oxidative damage and consequently results in better growth and yield in mustard plants.

Keywords


abiotic stress; phytohormones; reactive oxygen species; soil pollution; toxic metals

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References


Malar S, Vikram SS, Favas PJC, Perumal V. Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud. 2014;55:54. https://doi.org/10.1186/s40529-014-0054-6

Wierzbicka M, Przedpełska E, Ruzik R, Ouerdane L, Połeć-Pawlak K, Jarosz M, et al. Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma. 2007;231:99–111. https://doi.org/10.1007/s00709-006-0227-6

Sharma R, Dubey R. Lead toxicity in plants. Braz J Plant Physiol. 2005;17:35–52. https://doi.org/10.1590/S1677-04202005000100004

Lakra N, Tomar PC, Mishra SN. Growth response modulation by putrescine in Indian mustard Brassica juncea L. under multiple stress. Indian J Exp Biol. 2016;54:262–270.

Hasanuzzaman M, Fujita M. Heavy metals in the environment: current status, toxic effects on plants and possible phytoremediation. In: Anjum NA, Pereira MA, Ahmad IA, Duarte AC, Umar S, Khan NA, editors. Phytotechnologies: remediation of environmental contaminants. Boca Raton, FL, USA: CRC Press; 2012. p. 7–73. https://doi.org/10.1201/b12954-4

Nareshkumar A, Veeranagamallaiah G, Pandurangaiah M, Kiranmai K, Amaranathareddy V, Lokesh U, et al. Pb-stress induced oxidative stress caused alterations in antioxidant efficacy in two groundnut (Arachis hypogaea L.). Agricultural Sciences. 2015;6:1283–1297. https://doi.org/10.4236/as.2015.610123

Shahid M, Dumat C, Pourrut B, Abbas G, Shahid N, Pinelli E. Role of metal speciation in lead-induced oxidative stress to Vicia faba roots. Russ J Plant Physiol. 2015;62:448–454. https://doi.org/10.1134/S1021443715040159

Hasanuzzaman M, Hossain MA, Fujita M. Exogenous selenium pretreatment protects rapeseed plants from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res. 2012;149:248–261. https://doi.org/10.1007/s12011-012-9419-4

Hasanuzzaman M, Hossain MA, Jaime A, da Silva T, Fujita M. Plant responses and resistance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapaka M, editors. Crop stress and its management: perspectives and strategies. Dordrecht: Springer; 2012. p. 261–316. https://doi.org/10.1007/978-94-007-2220-0_8

Rahman A, Nahar K, Hasanuzzaman M, Fujita M. Manganese induced cadmium stress resistance in rice plants: coordinated action of antioxidant defense, glyoxalase system and nutrient homeostasis. C R Biol. 2016;339:462–474. https://doi.org/10.1016/j.crvi.2016.08.002

Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA. Salicylic acid-induced abiotic stress resistance and underlying mechanisms in plants. Front Plant Sci. 2015;6:462. https://doi.org/10.3389/fpls.2015.00462

Asgher M, Khan MIR, Anjum NA, Khan NA. Minimizing toxicity of cadmium in plants – role of plant growth regulators. Protoplasma. 2015;252:399–413. https://doi.org/10.1007/s00709-014-0710-4

Khan A, Rahman MM, Tania M, Shoshee NF, Xu AH, Chen HC. Antioxidative potential of Duranta repens (Linn.) fruits against H2O2 induced cell death in vitro. Afr J Tradit Complement Altern Med. 2013;10:436–441. https://doi.org/10.4314/ajtcam.v10i3.9

Miura K, Tada Y. Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci. 2014;5:4. https://doi.org/10.3389/fpls.2014.00004

Zhang Y, Xu S, Yang S, Chen Y. Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma. 2015;252:911–924. https://doi.org/10.1007/s00709-014-0732-y

Chai J, Liu J, Zhou J, Xing D. Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J Exp Bot. 2014;65:6513–6528. https://doi.org/10.1093/jxb/eru369

Chen J, Zhu C, Li LP, Sun ZY, Pan XB. Effects of exogenous salicylic acid on growth and H2O2-metabolizing enzymes in rice plants under lead stress. Journal of Environmental Sciences. 2007;19:44–49. https://doi.org/10.1016/S1001-0742(07)60007-2

Arshad T, Maqbool N, Javed F, Wahid A, Arshad MU. Enhancing the defensive mechanism of lead affected barley (Hordeum vulgare L.) genotypes by exogenously applied salicylic acid. J Agric Sci. 2017;9:139–146. https://doi.org/10.5539/jas.v9n2p139

Belkadhi A, de Haro A, Obregon S, Chaıbi W, Djebali W. Positive effects of salicylic acid pretreatment on the composition of flax plastidial membrane lipids under cadmium stress. Environ Sci Pollut Res Int. 2015;22:1457–1467. https://doi.org/10.1007/s11356-014-3475-6

Li X, Ma L, Bu N, Li Y, Zhang L. Effects of salicylic acid pretreatment on cadmium and/or UV-B stress in soybean plants. Biol Plant. 2014;58:195–199. https://doi.org/10.1007/s10535-013-0375-4

Agami RA, Mohamed GF. Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat plants. Ecotoxicol Environ Saf. 2013;94:164–171. https://doi.org/10.1016/j.ecoenv.2013.04.013

Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W. Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot. 2012;63:5521–5534. https://doi.org/10.1093/jxb/ers201

Janda T, Gondor OK, Yordanova R, Szalai G, Pál M. Salicylic acid and photosynthesis: signalling and effects. Acta Physiol Plant. 2014;36:2537–2546. https://doi.org/10.1007/s11738-014-1620-y

Dražić G, Mihailović N. Salicylic acid modulates accumulation of Cd in plants of Cd-tolerant and Cd-susceptible soybean genotypes. Arch Biol Sci. 2009;61:431–439. https://doi.org/10.2298/ABS0903431D

Shi G, Cai Q, Liu Q, Wu L. Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiol Plant. 2009;31:969–977. https://doi.org/10.1007/s11738-009-0312-5

Barrs HD, Weatherly PE. A re-examination of relative turgidity for estimating water deficits in leaves. Aust J Biol Sci. 1962;15:413–428. https://doi.org/10.1071/BI9620413

Heath RL, Packer L. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;25:189–198. https://doi.org/10.1016/0003-9861(68)90654-1

Yu CW, Murphy TM, Lin CH. Hydrogen peroxide-induces chilling resistance in mung beans mediated through ABA independent glutathione accumulation. Funct Plant Biol. 2003;30:955–963. https://doi.org/10.1071/FP03091

Huang C, He W, Guo J, Chang X, Su P, Zhang L. Increased sensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot. 2005;56:3041–3049. https://doi.org/10.1093/jxb/eri301

Paradiso A, Berardino R, de Pinto M, di Toppi LS, Storelli FT, de Gara L. Increase in ascorbate–glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol. 2008;49:362–374. https://doi.org/10.1093/pcp/pcn013

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Hossain MA, Nakano Y, Asada K. Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol. 1984;25:385–395. https://doi.org/10.1093/oxfordjournals.pcp.a076726

Hossain MA, Hasanuzzaman M, Fujita M. Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer resistance to cadmium stress. Physiol Mol Biol Plants. 2010;16:259–272. https://doi.org/10.1007/s12298-010-0028-4

Hossain MZ, Hossain MD, Fujita M. Induction of pumpkin glutathione S-transferases by different stresses and its possible mechanisms. Biol Plant. 2006;50:210–218. https://doi.org/10.1007/s10535-006-0009-1

Shannon LM, Kay E, Lew JY. Peroxidase isozymes from horseradish roots I. Isolation and physical properties. J Biol Chem. 1966;241:2166–2172.

Gardner FP, Pearce RB, Mitchell RL. Physiology of crop plants. Iowa State Univ. USA. Int Rice Res. Notes. 1985;27:11–2.

Addinsoft. XLSTAT v. 2017: data analysis and statistics software for Microsoft Excel [Software]. Paris: Addinsoft; 2017.

Ashraf U, Tang X. Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere. 2017;176:141–155. https://doi.org/10.1016/j.chemosphere.2017.02.103

Kumar A, Prasad MNV, Sytar O. Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere. 2012;89:1056–1065. https://doi.org/10.1016/j.chemosphere.2012.05.070

Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, et al. Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. plants. Protoplasma. 2017;255:11–24. https://doi.org/10.1007/s00709-017-1124-x

Hussain A, Abbas N, Arshad F, Akram M, Khan ZI, Ahmad K, et al. Effects of diverse doses of lead (Pb) on different growth attributes of Zea mays L. Agricultural Sciences. 2013;4:262–265. https://doi.org/10.4236/as.2013.45037

Ali B. Salicylic acid induced antioxidant system enhances the resistance to aluminium in mung bean (Vigna radiata L. Wilczek) plants. Indian J Plant Physiol. 2017;22:178–189. https://doi.org/10.1007/s40502-017-0292-1

Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M. Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf. 2016;126:245–255. https://doi.org/10.1016/j.ecoenv.2015.12.026

Fontenele NMB, Otoch MDLO, Gomes-Rochette NF, de Menezes Sobreira AC, Barreto AAGC, de Oliveira FDB, et al. Effect of lead on physiological and antioxidant responses in two Vigna unguiculata cultivars differing in Pb-accumulation. Chemosphere. 2017;176:397–404. https://doi.org/10.1016/j.chemosphere.2017.02.072

Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, et al. Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crops Prod. 2014;52:617–626. https://doi.org/10.1016/j.indcrop.2013.11.033

Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D. Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol. 2010;101:3025–3032. https://doi.org/10.1016/j.biortech.2009.12.031

Shahid M, Dumat C, Pourrut B, Silvestre J, Laplanche C, Pinelli E. Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J Soils Sediments. 2014;14:835–843. https://doi.org/10.1007/s11368-013-0724-0

López-Orenes A, Martínez-Pérez A, Calderón AA, Ferrer MA. Pb-induced responses in Zygophyllum fabago plants are organ-dependent and modulated by salicylic acid. Plant Physiol Biochem. 2014;84:57–66. https://doi.org/10.1016/j.plaphy.2014.09.003

Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F. Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and plants growth. C R Biol. 2011;334:118–126. https://doi.org/10.1016/j.crvi.2010.12.006

Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, et al. Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ Exp Bot. 2016;123:1–12. https://doi.org/10.1016/j.envexpbot.2015.10.005

Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E. Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. In: Whitacre DM, editor. Reviews of environmental contamination and toxicology. Cham: Springer; 2014. p. 1–44. (Reviews of Environmental Contamination and Toxicology; vol 232). https://doi.org/10.1007/978-3-319-06746-9_1

Mahmud JA, Hasanuzzaman M, Nahar K, Bhuyan MB, Fujita M. Insights into citric acid-induced cadmium resistance and phytoremediation in Brassica juncea L.: coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol Environ Saf. 2018;147:990–1001. https://doi.org/10.1016/j.ecoenv.2017.09.045

Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M. γ-Aminobutyric acid (GABA) confers chromium stress resistance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology. 2017;26:675–690. https://doi.org/10.1007/s10646-017-1800-9

Pandey P, Singh J, Achary V, Reddy MK. Redox homeostasis via gene families of ascorbate–glutathione pathway. Front Environ Sci. 2015;3:25. https://doi.org/10.3389/fenvs.2015.00025

Khan MIR, Asgher M, Khan NA. Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycine betaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem. 2014;80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026

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

Singh AP, Dixit G, Kumar A, Mishra S, Singh PK, Dwivedi S, et al. Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci. 2016;6:1272. https://doi.org/10.3389/fpls.2015.01272

Noriega G, Caggiano E, Lecube ML, Santa Cruz D, Batlle A, Tomaro M, et al. The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals. 2012;25:1155–1165. https://doi.org/10.1007/s10534-012-9577-z

Shakirova FM, Allagulova CR, Maslennikova DR, Klyuchnikova EO, Avalbaev AM, Bezrukova MV. Salicylic acid-induced protection against cadmium toxicity in wheat plants. Environ Exp Bot. 2016;122:19–28. https://doi.org/10.1016/j.envexpbot.2015.08.002

Zhang F, Zhang H, Xia Y, Wang G, Xu L, Shen Z. Exogenous application of salicylic acid alleviates cadmium toxicity and reduces hydrogen peroxide accumulation in root apoplasts of Phaseolus aureus and Vicia sativa. Plant Cell. 2011;30:1475–1483. https://doi.org/10.1007/s00299-011-1056-4

Nahar K, Rahman M, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, et al. Physiological and biochemical mechanisms of spermine-induced cadmium stress resistance in mung bean (Vigna radiata L.) plants. Environ Sci Pollut Res Int. 2016;23:21206–21218. https://doi.org/10.1007/s11356-016-7295-8

Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BH, Fujita M. Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci. 2017;8:115. https://doi.org/10.3389/fpls.2017.00115

Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, et al. Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress resistance in plants. Int J Mol Sci. 2017;18:200. https://doi.org/10.3390/ijms18010200

Doncheva S, Moustakas M, Ananieva K, Chavdarova M, Gesheva E, Vassilevska R, et al. Plant response to lead in the presence or absence EDTA in two sunflower genotypes (cultivated H. annuus cv. 1114 and interspecific line H. annuus × H. argophyllus). Environ Sci Pollut Res Int. 2013;20:823–833. https://doi.org/10.1007/s11356-012-1274-5

Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress resistance in crop plants. Plant Physiol Biochem. 2010;48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

Hasanuzzaman M, Fujita M. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) plants by enhancing antioxidant defense and glyoxalase system. Ecotoxicology. 2013;22:584–596. https://doi.org/10.1007/s10646-013-1050-4

Verma S, Dubey RS. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 2003;164:645–655. https://doi.org/10.1016/S0168-9452(03)00022-0

Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C. Lead induced changes in antioxidant metabolism of horsegram [Macrotyloma uniflorum (Lam.) Verdc.] and bengalgram (Cicer arietinum L.). Chemosphere. 2005;60:97–104. https://doi.org/10.1016/j.chemosphere.2004.11.092