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Supplementation of Salicylic Acid and Citric Acid for Alleviation of Cadmium Toxicity to Brassica juncea

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Abstract

The reported study investigated the interaction between salicylic acid (SA) and citric acid (CA) in cadmium (Cd)-stressed Brassica juncea plants. Seedling received Cd (0.6 mM) stress through soil at 5-day stage of growth. SA (0.01 mM) and CA (0.6 mM) treatments were applied at 25 days after sowing. Growth, photosynthesis, oxidative burst, and antioxidant systems were examined at 30-day stage of growth. Growth and photosynthetic parameters reduced significantly in the presence of Cd, and elevated levels of H2O2 were indicative of oxidative burst which resulted in decline of cell viability. Foliar spray of SA and CA alone or in combination mitigated the toxic effects generated by Cd and enhanced plant growth parameters. The inhibitory effects of Cd toxicity on width of stomatal pore resulted in reduced internal CO2 concentration and carbonic anhydrase activity which consequently limited the photosynthetic rate. SA and CA alleviated the inhibitory effect of Cd on photosynthesis by stimulating the stomatal activity and pore size. The Cd-generated oxidative burst was reduced via enhanced antioxidant activity (catalase, peroxidase, and superoxide dismutase) upon follow-up treatment with SA and CA alone or in combination. A combined dose of SA and CA countered Cd-induced damage by reducing levels of reactive oxygen species and strengthening plant antioxidant defense systems, which resulted in membrane stabilization and recovery from stress. Combined dose of SA and CA proved more effective than their individual application towards Cd stress which suggests an effective synergism between the two acids.

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References

  • Afshan S, Ali S, Bharwana SA et al (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut Res 22:11679–11689. https://doi.org/10.1007/s11356-015-4396-8

    Article  CAS  Google Scholar 

  • Ahmad P, Jaleel CA, Salem MA (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30(3):161–175

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77(1):36–44

    Article  CAS  Google Scholar 

  • Ahmad P, Sarwat M, Bhat NA et al (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS ONE 10:1–17. https://doi.org/10.1371/journal.pone.0114571

    Article  CAS  Google Scholar 

  • Ahmad P, Abdel Latef AA, Abd_Allah EF et al (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513

    PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Alyemeni MN, Ahanger MA et al (2018) Salicylic acid (SA) induced alterations in growth, biochemical attributes and antioxidant enzyme activity in faba bean (Vicia faba L.) seedlings under NaCl toxicity. Russ J Plant Physiol 65(1):104–114

    Article  CAS  Google Scholar 

  • Al Mahmud J, Hasanuzzaman M et al (2017) Relative tolerance of different species of Brassica to cadmium toxicity: Coordinated role of antioxidant defense and glyoxalase systems. Plant Omics 10:107–117. https://doi.org/10.21475/poj.10.02.17.pne409

    Article  CAS  Google Scholar 

  • Alyemeni MN, Ahanger MA, Wijaya L (2018) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255(2):459–469

    Article  CAS  PubMed  Google Scholar 

  • Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Rodrigo MA, Adam V, Fujita M, Kizek R, Duarte AC (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192

    PubMed  PubMed Central  Google Scholar 

  • Anuradha S, Rao SSR (2009) Effect of 24-epibrassinolide on the photosynthetic activity of radish plants under cadmium stress. Photosynthetica 47:317–320

    Article  CAS  Google Scholar 

  • Balakhnina TI, Kosobryukhov AA, Ivanov AA, Kreslavskii VD (2005) The effect of cadmium on CO2 exchange, variable fluorescence of chlorophyll, and the level of antioxidant enzymes in pea leaves. Russ J Plant Physiol 52(1):15–20

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Behera RK, Mishra PC, Choudhury NK (2002) High irradiance and water stress induce alterations in pigment composition and chloroplast activities of primary wheat leaves. J Plant Physiol 159:967–973. https://doi.org/10.1078/0176-1617-00823

    Article  CAS  Google Scholar 

  • Belkadhi A, De Haro A, Soengas P et al (2014) Salicylic acid increases tolerance to oxidative stress induced by hydrogen peroxide accumulation in leaves of cadmium-exposed flax (Linum usitatissimum L.). J Plant Interact 9:647–654. https://doi.org/10.1080/17429145.2014.890751

    Article  CAS  Google Scholar 

  • Belkhadi A, Hediji H, Abbes Z et al (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 

  • Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17(1):21–34

    Article  CAS  Google Scholar 

  • Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA 102:3459–3464. https://doi.org/10.1073/pnas.0407960102

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99

    Article  CAS  PubMed  Google Scholar 

  • Dalio RJD, Pinheiro HP, Sodek L, Haddad CRB (2011) The effect of 24-epibrassinolide and clotrimazole on the adaptation of Cajanus cajan (L.) Millsp. to salinity. Acta Physiol Plant 33(5):1887–1896

    Article  CAS  Google Scholar 

  • De Miranda JR, Thomas MA, Thurman DA, Tomsett AB (1990) Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Lett 260(2):277–280

    Article  PubMed  Google Scholar 

  • Delavari PM, Baghizadeh A, Enteshari SH, Kalantari KM, Yazdanpanah A, Mousavi EA (2010) The effects of salicylic acid on some of biochemical and morphological characteristic of Ocimum basilicucm under salinity stress. Aust J Basic Appl Sci 4(10):4832–4845

    CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evaluation of a rapid test for the hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • Ehsan S, Ali S, Noureen S et al (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol Environ Saf 106:164–172. https://doi.org/10.1016/j.ecoenv.2014.03.007

    Article  CAS  PubMed  Google Scholar 

  • Erdal S, Turk H (2016) Cysteine-induced upregulation of nitrogen metabolism-related genes and enzyme activities enhance tolerance of maize seedlings to cadmium stress. Environ Exp Bot 132:92–99. https://doi.org/10.1016/j.envexpbot.2016.08.014

    Article  CAS  Google Scholar 

  • Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica 41(2):281–284

    Article  CAS  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA et al (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46. https://doi.org/10.1016/j.envexpbot.2012.04.006

    Article  CAS  Google Scholar 

  • Gao Y, Miao C, Mao L et al (2010) Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazard Mater 181:771–777. https://doi.org/10.1016/j.jhazmat.2010.05.080

    Article  CAS  PubMed  Google Scholar 

  • Ghazijahani N, Hadavi E, Jeong BR (2014) Foliar sprays of citric acid and salicylic acid alter the pattern of root acquisition of some minerals in sweet basil (Ocimum basilicum L.). Front Plant Sci 5:1–7. https://doi.org/10.3389/fpls.2014.00573

    Article  Google Scholar 

  • Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants. Plant Signal Behav 6:215–222. https://doi.org/10.4161/psb.6.2.14880

    Article  CAS  PubMed  Google Scholar 

  • Gondor OK, Pál M, Darkó É et al (2016) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS ONE 11:e0160157. https://doi.org/10.1371/journal.pone.0160157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gossett DR, Millhollon EP, Lucas M (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34(3):706–714

    Article  CAS  Google Scholar 

  • Guo B, Liang Y, Li Z, Guo W (2007) Role of salicylic acid in alleviating cadmium toxicity in rice roots. J Plant Nutr 30:427–439. https://doi.org/10.1080/01904160601171835

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateswarlu B, Shanker A, Shanker C, Maheswari M (eds) Crop stress and its management: perspectives and strategies. Springer, Dordrecht, pp 261–315

    Chapter  Google Scholar 

  • Hassan MS, Dagari MS, Babayo AU (2016) Effect of citric acid on cadmium ion uptake and stress response of hydroponically grown jute mallow (Corchorus olitorius). J Environ Anal Toxicol 6:375

    Google Scholar 

  • Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41. https://doi.org/10.1016/j.envexpbot.2006.06.002

    Article  CAS  Google Scholar 

  • Hayat S, Masood A, Yusuf M, Fariduddin Q, Ahmad A (2009) Growth of Indian mustard (Brassica juncea L.) in response to salicylic acid under high-temperature stress. Braz J Plant Physiol 21(3):187–195

    Article  Google Scholar 

  • Hayat S, Maheshwari P, Wani AS, Irfan M, Alyemeni MN, Ahmad A (2012) Comparative effect of 28 homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol Biochem 53:61–68

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Zhang Z, Xiang Z, Yang Z (2016) Exogenous application of citric acid ameliorates the adverse effect of heat stress in tall fescue (Lolium arundinaceum). Front Plant Sci 7:1–11. https://doi.org/10.3389/fpls.2016.00179

    Article  CAS  Google Scholar 

  • Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125–131

    Article  CAS  PubMed  Google Scholar 

  • Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43:1274–1279

    Article  CAS  PubMed  Google Scholar 

  • Kang GZ, Li GZ et al (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. https://doi.org/10.1007/s10535-013-0335-z

    Article  CAS  Google Scholar 

  • Kaur R, Yadav P, Sharma A et al (2017) Castasterone and citric acid treatment restores photosynthetic attributes in Brassica juncea L. under Cd (II) toxicity. Ecotoxicol Environ Saf 145:466–475

    Article  CAS  PubMed  Google Scholar 

  • Kaur R, Yadav P, Sharma A et al (2018) Castasterone and citric acid supplementation alleviates cadmium toxicity by modifying antioxidants and organic acids in Brassica juncea. J Plant Growth Regul 37(1):286–299

    Article  CAS  Google Scholar 

  • Kaur P, Bali S, Sharma A et al (2019) Cd induced generation of free radical species in Brassica juncea is regulated by supplementation of earthworms in the drilosphere. Sci Total Environ 655:663–675

    Article  CAS  PubMed  Google Scholar 

  • Kaya C, Okant M, Ugurlar F (2019) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere 225:627–638

    Article  CAS  PubMed  Google Scholar 

  • Khan NA, Singh S et al (2008) Cadmium effects on carbonic anhydrase, photosynthesis, dry mass and antioxidative enzymes in wheat (Triticum aestivum) under low and sufficient zinc. J Plant Interact 3:31–37. https://doi.org/10.1080/17429140701724958

    Article  CAS  Google Scholar 

  • Khan TA, Fariduddin Q, Yusuf M (2015) Lycopersicon esculentum under low temperature stress: an approach toward enhanced antioxidants and yield. Environ Sci Pollut Res 22:14178–14188

    Article  CAS  Google Scholar 

  • Khanna K, Jamwal VL, Kohli SK (2019) Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression. Chemosphere 217:463–474

    Article  CAS  PubMed  Google Scholar 

  • Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439–1458. https://doi.org/10.1007/BF00016484

    Article  CAS  PubMed  Google Scholar 

  • Kneer R, Zenk MH (1992) Phytochelatins protect plant enzymes from heavy metal poisoning. Phytochemistry 31(8):2663–2667

    Article  CAS  Google Scholar 

  • Kohli SK, Handa N, Sharma A et al (2018a) Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma 255(1):11–24

    Article  CAS  PubMed  Google Scholar 

  • Kohli SK, Handa N, Sharma A et al (2018b) Interaction of 24-epibrassinolide and salicylic acid regulates pigment contents, antioxidative defense responses, and gene expression in Brassica juncea L. seedlings under Pb stress. Environ Sci Pollut Res 25(15):15159–15173

    Article  CAS  Google Scholar 

  • Kohli SK, Bali S, Tejpal R et al (2019) In-situ localization and biochemical analysis of bio-molecules reveals Pb-stress amelioration in Brassica juncea L. by co-application of 24-epibrassinolide and salicylic acid. Sci Rep 9(1):3524

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu L, Sun H, Chen J et al (2014) Effects of cadmium (Cd) on seedling growth traits and photosynthesis parameters in cotton. Plant Omics 7:284–290

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Loeffler S, Hochberger A, Grill E, Winnacker EL, Zenk MH (1989) Termination of the phytochelatin synthase reaction through sequestration of heavy metals by the reaction product. FEBS Lett 258(1):42–46

    Article  CAS  Google Scholar 

  • Lu L, Tian S, Yang X et al (2013) Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. J Zhejiang Univ Sci B 14:106–114. https://doi.org/10.1631/jzus.B1200211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Q, Zhang T, Zhang W et al (2018) Alleviation of cadmium toxicity in Lemna minor by exogenous salicylic acid. Ecotoxicol Environ Saf 147:500–508. https://doi.org/10.1016/j.ecoenv.2017.09.015

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97:46–51. https://doi.org/10.1016/S0162-0134(03)00245-9

    Article  CAS  PubMed  Google Scholar 

  • Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration, and free amino acid composition of a chlorophyll mutant of barley. Can J Bot 41:1053–1062

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Manara A (2012) Plant responses to heavy metal toxicity. In: Furini A (ed) Plants and heavy metals. Springer, Dordrecht, pp 27–53

    Chapter  Google Scholar 

  • Meneguzzo S, Navam-Izzo F, Izzo R (1999) Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol 155(2):274–280

    Article  CAS  Google Scholar 

  • Meng H, Hua S, Shamsi IH et al (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. https://doi.org/10.1007/s10725-008-9351-y

    Article  CAS  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M et al (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132(1):272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Murtaza G, Javed W, Hussain A et al (2015) Metal uptake via phosphate fertilizer and city sewage in cereal and legume crops in Pakistan. Environ Sci Pollut Res 22:9136–9147. https://doi.org/10.1007/s11356-015-4073-y

    Article  CAS  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8

    Article  CAS  Google Scholar 

  • Najeeb U, Jilani G, Ali S et al (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574. https://doi.org/10.1016/j.jhazmat.2010.11.037

    Article  CAS  PubMed  Google Scholar 

  • Noriega G, Caggiano E, Lecube ML et al (2012) The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals 25:1155–1165. https://doi.org/10.1007/s10534-012-9577-z

    Article  CAS  PubMed  Google Scholar 

  • Parashar A, Yusuf M, Fariduddin Q, Ahmad A (2014) Salicylic acid enhances antioxidant system in Brassica juncea grown under different levels of manganese. Int J Biol Macromol 70:551–558

    Article  CAS  PubMed  Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54(1):45. https://doi.org/10.1186/1999-3110-54-45

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira de Araújo R, Furtado de Almeida AA, Silva Pereira L et al (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotoxicol Environ Saf 144:148–157. https://doi.org/10.1016/j.ecoenv.2017.06.006

    Article  CAS  PubMed  Google Scholar 

  • Rauser WE, Curvetto NR (1980) Metallothionein occurs in roots of Agrostis tolerant to excess copper. Nature 287(5782):563

    Article  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):2115–2126

    Article  CAS  PubMed  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365

    CAS  PubMed  Google Scholar 

  • Semida WM, Rady MM, Abd El-Mageed TA et al (2015) Alleviation of cadmium toxicity in common bean (Phaseolus vulgaris L.) plants by the exogenous application of salicylic acid. J Hortic Sci Biotechnol 90:83–91. https://doi.org/10.1080/14620316.2015.11513157

    Article  CAS  Google Scholar 

  • Shlizerman L, Marsh K, Blumwald E, Sadka A (2007) Iron-shortage-induced increase in citric acid content and reduction of cytosolic aconitase activity in citrus fruit vesicles and calli. Physiol Plant 131:72–79. https://doi.org/10.1111/j.1399-3054.2007.00935.x

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui H, Ahmed KB, Hayat S (2018) Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the performance of different components influencing the photosynthetic machinery in Brassica juncea L. Plant Physiol Biochem 129:198–212

    Article  CAS  PubMed  Google Scholar 

  • Silveira FS, Azzolini M, Divan AM (2015) Scanning cadmium photosynthetic responses of Elephantopus mollis for potential phytoremediation practices. Water Air Soil Pollut 226(11):359

    Article  CAS  Google Scholar 

  • Smith S, Stewart GR (1990) Effect of potassium levels on the stomatal behavior of the hemi-parasite Striga hermonthica. Plant Physiol 94(3):1472–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava HS (1980) Regulation of nitrate reductase activity in higher plants. Phytochemistry 19(5):725–733

    Article  CAS  Google Scholar 

  • Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa—an angiospermic parasite. J Plant Physiol 161:665–674. https://doi.org/10.1078/0176-1617-01274

    Article  CAS  PubMed  Google Scholar 

  • Sun YL, Hong SK (2011) Effects of citric acid as an important component of the responses to saline and alkaline stress in the halophyte Leymus chinensis (Trin.). Plant Growth Regul 64:129–139. https://doi.org/10.1007/s10725-010-9547-9

    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 Bot 37(4):708–714

    CAS  Google Scholar 

  • Vagner E, Williams C, Souza A, Bruno F (2013) Citric acid-assisted phytoextraction of lead: a field experiment. Chemosphere 92:213–217. https://doi.org/10.1016/j.chemosphere.2013.01.103

    Article  CAS  Google Scholar 

  • Vallee BL, Ulmer DD (1972) Biochemical effects of mercury, cadmium, and lead. Annu Rev Biochem 41(1):91–128

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163(7):723–730

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Ghani A, Ali I, Ashraf MY (2007) Effects of cadmium on carbon and nitrogen assimilation in shoots of mungbean [Vigna radiata (L.) Wilczek] seedlings. J Agron Crop Sci 193(5):357–365

    Article  CAS  Google Scholar 

  • Wang Y, Fang J, Leonard SS, Rao KMK (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443

    Article  CAS  PubMed  Google Scholar 

  • Wani AB, Chadar H, Wani AH et al (2017) Salicylic acid to decrease plant stress. Environ Chem Lett 15:101–123. https://doi.org/10.1007/s10311-016-0584-0

    Article  CAS  Google Scholar 

  • Yeh TY, Lin CF, Chuang CC, Pan CT (2012) The effect of varying soil organic levels on phytoextraction of Cu and Zn uptake, enhanced by chelator EDTA, DTPA, EDDS and Citric Acid, in Sunflower (Helianthus annuus), Chinese Cabbage (Brassica campestris), Cattail (Typha latifolia), and Reed (Phragmites communis). Environ Anal Toxicol 2(5):2. https://doi.org/10.4172/2161-0525.1000142

    Article  Google Scholar 

  • Ying RR, Qiu RL, Tang YT et al (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Physiol 167:81–87. https://doi.org/10.1016/j.jplph.2009.07.005

    Article  CAS  PubMed  Google Scholar 

  • Yusuf M, Hasan SA, Ali B, Hayat S, Fariduddin Q, Ahmad A (2008) Effect of salicylic acid on salinity-induced changes in Brassica juncea. J Integr Plant Biol 50(9):1096–1102

    Article  CAS  PubMed  Google Scholar 

  • Yusuf M, Fariduddin Q, Varshney P, Ahmad A (2012) Salicylic acid minimizes nickel and/or salinity-induced toxicity in Indian mustard (Brassica juncea) through an improved antioxidant system. Environ Sci Pollut Res 19(1):8–18

    Article  CAS  Google Scholar 

  • Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracoviensia Ser Bot 47:157–164

    Google Scholar 

  • Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179(1):21–30

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Zhang H, Xia Y et al (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. https://doi.org/10.1007/s00299-011-1056-4

    Article  CAS  PubMed  Google Scholar 

  • Zong H, Liu S, Xing R et al (2017) Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicol Environ Saf 138:271–278. https://doi.org/10.1016/j.ecoenv.2017.01.009

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Department of Botany and Aligarh Muslim University for providing the platform to perform this experiment. We thank the authors for their contribution to this experiment. Thanks to Dr. John Pichtel, Ball State University, USA, for assistance with editing the manuscript.

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Correspondence to Shamsul Hayat.

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Faraz, A., Faizan, M., Sami, F. et al. Supplementation of Salicylic Acid and Citric Acid for Alleviation of Cadmium Toxicity to Brassica juncea. J Plant Growth Regul 39, 641–655 (2020). https://doi.org/10.1007/s00344-019-10007-0

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  • DOI: https://doi.org/10.1007/s00344-019-10007-0

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