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Alleviation of selenium toxicity in Brassica juncea L.: salicylic acid-mediated modulation in toxicity indicators, stress modulators, and sulfur-related gene transcripts

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Abstract

The present work reveals the response of different doses of selenium (Se) and alleviating effect of salicylic acid (SA) on Se-stressed Brassica juncea seedlings. Selenium, a micronutrient, is essential for both humans and animals but is toxic at higher doses. Its beneficial role for the survival of plants, however, is still debatable. On the other hand, SA, a phenolic compound, is known to have specific responses under environmental stresses. Experiments were conducted using leaves of hydroponically grown seedlings of Pusa bold (PB) variety of B. juncea, treated with different concentrations of Se (50, 150, 300 μM) for 24- and 96-h exposure times. Increasing Se concentrations inhibited growth and, caused lipid peroxidation, concomitantly increased stress modulators (proline, cysteine, SOD, CAT) along with sulfur-related gene transcripts (LAST, APS, APR, GR, OASL, MT-2, PCS) in Brassica seedlings. On the basis of the above studied parameters, maximum inhibition in growth was observed at 300 μM Se after 96-h exposure time. Further, co-application of SA along with 300 μM Se helped to mitigate Se stress, as shown by improved levels of growth parameters, toxicity indicators (chlorophyll, protein, MDA), stress modulators (proline, cysteine, SOD, and CAT), and expression of sulfur-related genes as compared to Se-treated seedlings alone. Altogether, this study revealed that Se + SA combinations improved seedling morphology and were effective in alleviation of Se stress in PB variety of B. juncea.

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References

  • Aebi HE (1983) Catalase. In: Bergmeyer HIJ (ed) Methods of enzymatic analysis Vertag Chemie 273–286

  • Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H (2011) Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biol Trace Elem Res 140:354–367

    Article  CAS  PubMed  Google Scholar 

  • Ahmad MA, Gupta M (2013) Exposure of Brassica juncea (L) to arsenic species in hydroponic medium: comparative analysis in accumulation and biochemical and transcriptional alterations. Environ Sci Pollut Res 20:8141–8150

    Article  CAS  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals- concepts and applications. Chemosphere 91:869–881

    Article  CAS  PubMed  Google Scholar 

  • Ansari MKA, Ahmad A, Umar S, Ansari SH, Iqbal M, Owens G, Shao HB (2012) Screening Indian mustard genotypes for phytoremediating arsenic-contaminated soil. CLEAN 41:195–201

    Google Scholar 

  • Armas T, Pinto AP, de Varennes A, Mourato MP, Martins LL, Gonçalves MLS, Mota AM (2015) Comparison of cadmium-induced oxidative stress in Brassica juncea in soil and hydroponic cultures. Plant Soil 388:294–305

    Article  Google Scholar 

  • Arnon DE (1949) Copper enzymes in isolated chloroplast, polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajaj M, Eiche E, Neumann T, Winter J, Gallert C (2011) Hazardous concentrations of selenium in soil and groundwater in North-West India. J Hazard Mater 189(3):640–646

    Article  CAS  PubMed  Google Scholar 

  • Bañuelos G, Terry N, LeDuc DL, Pilon-Smits EAH, Mackey B (2005) Field trial of transgenic Indian mustard plants shows enhanced phytoremediation of selenium-contaminated sediment. Environ Sci Technol 39:1771–1777

    Article  PubMed  Google Scholar 

  • Bañuelos G, LeDuc DL, Pilon-Smits EAH, Terry N (2007) Transgenic Indian mustard overexpressing selenocysteine lyase or selenocysteine methyltransferase exhibit enhanced potential for selenium phytoremediation under field conditions. Environ Sci Technol 41:599–605

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Belkhadi A, Hediji H, Abbes Z, Djebali W, Chaibi W (2012) Influence of salicylic acid pre-treatment on cadmium tolerance and its relationship with non-protein thiol production in flax root. Afr J Biotechnol 11(41):9788–9796

    Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cartes P, Jara AA, Pinilla L, Rosas A, Mora ML (2010) Selenium improves the antioxidant ability against aluminium-induced oxidative stress in ryegrass roots. Ann Appl Biol 156:297–307

    Article  CAS  Google Scholar 

  • Chen J, Zhu C, Li L, Sun Z, Pan X (2007) Effects of exogenous salicylic acid on growth and H2O2-metabolizing enzymes in rice seedlings under lead stress. J Environ Sci 19:44–49

    Article  CAS  Google Scholar 

  • Chen Y, Mo H-Z, Zheng M-Y, Xian M, Qi Z-Q et al (2014a) Selenium inhibits root elongation by repressing the generation of endogenous hydrogen sulfide in Brassica rapa. PLoS ONE 9(10):e110904. doi:10.1371/journal.pone.0110904

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Mo H-Z, Hu L-B, Li Y-Q, Chen J et al (2014b) The endogenous nitric oxide mediates selenium-induced phytotoxicity by promoting ROS generation in Brassica rapa. PLoS ONE 9(10):e110901. doi:10.1371/journal.pone.0110901

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Wang R, Guo J, Wu F, Xu Y, Feng R (2015) The effect of selenium on the subcellular distribution of antimony to regulate the toxicity of antimony in paddy rice. Environ Sci Pollut Res 22:5111–5123

    Article  CAS  Google Scholar 

  • Domenech J, Mir G, Huguet G, Capdevila M, Molinas M, Atrian S (2006) Plant metallothionein domains: functional insight into physiological metal binding and protein folding. Biochimie 88:583–593

    Article  CAS  PubMed  Google Scholar 

  • Feng CX, Liu JJ, Liu S, Hu RZ, Chi GX (2009) Petrogenesis and sedimentary environment of the cherts from Yutangba, western Hubei Province: evidence from silicon, oxygen, carbon and sulfur isotopic compositions. Acta Petrol Sin 25(5):1253–1259

    CAS  Google Scholar 

  • Fordyce F, Selinus O, Alloway B, Centeno J, Finkelman R, Fuge R, Lindh U, Smedley P (2005) Selenium deficiency and toxicity in the environment. In Essentials of Medical Geology, Elsevier 373–415

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176219

    Article  Google Scholar 

  • Freeman JL, Quinn CF, Marcus MA, Fakra S, Pilon-Smits EAH (2006) Selenium-tolerant diamondback moth disarms hyperaccumulator plant defense. Curr Biol 16:2181–2192

    Article  CAS  PubMed  Google Scholar 

  • Freeman JL, Tamaoki M, Stushnoff C et al (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galeas ML, Zhang LH, Freeman JL, Wegner M, Pilon-Smits EAH (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium-hyperaccumulators and related non-accumulators. New Phytol 173:517–525

    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 

  • Guan C, Ji J, Jia C, Guan W, Li X, Jin C, Wang G (2015) A GSHS-like gene from Lycium chinense may be regulated by cadmium-induced endogenous salicylic acid and overexpression of this gene enhances tolerance to cadmium stress in Arabidopsis. Plant Cell Rep 34(5):871–84

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (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 WJ, Meetam M, Goldsbrough P (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 164(4):1697–1706

    Article  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 

  • Gupta S, Gupta M (2013) Indian mustard varieties (Brassica juncea) respond differently under selenium stress. Intern J Environ Res Develop 3:70–73

    CAS  Google Scholar 

  • Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326:1–36

    Article  CAS  PubMed  Google Scholar 

  • Hartikainen H, Xue T, Piironen V (2000) Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant Soil 225:193–200

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2011) Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol Trace Elem Res 143:1758–76

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721

    Article  CAS  PubMed  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 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hira CK, Partal K, Dhillon K (2004) Dietary selenium intake by men and women in high and low selenium areas of Punjab. Public Health Nutr 7:39–43

    Article  PubMed  Google Scholar 

  • Hong SH, Choi SA, Yoon H, Cho KS (2011) Screening of Cucumis sativus as a new arsenic-accumulating plant and its arsenic accumulation in hydroponic culture. Environ Geochem Health 33:143–149

    Article  CAS  PubMed  Google Scholar 

  • Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634

    Article  CAS  PubMed  Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP et al (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeDuc DL, AbdelSamie M, Montes-Bayon M, Wu CP, Reisinger SJ, Terry N (2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environ Pollut 144:70–76

    Article  CAS  PubMed  Google Scholar 

  • Lehotai N, Kolbert Z, Peto A et al (2012) Selenite-induced hormonal and signaling mechanisms during root growth of Arabidopsis thaliana L. J Exp Bot 63:5677–5687

    Article  CAS  PubMed  Google Scholar 

  • Lemire M, Mergler D, Huel G, Passos CJS, Fillion M, Philibert A et al (2009) Biomarkers of selenium status in the amazonian context: blood, urine and sequential hair segments. J Expo Sci Environ Epidemiol 19:213–222

    Article  CAS  PubMed  Google Scholar 

  • Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol 178:92–102

    Article  CAS  PubMed  Google Scholar 

  • Li T, Hu Y, Du X, Tang H, Shen C, Wu J (2014) Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS ONE 9(10):e109492. doi:10.1371/journal.pone.0109492

    Article  PubMed  PubMed Central  Google Scholar 

  • Longchamp M, Castrec-Rouelle M, Biron P, Bariac T (2015) Variations in the accumulation, localization and rate of metabolization of selenium in mature Zea mays plants supplied with selenite or selenate. Food Chem 182:128–135

    Article  CAS  PubMed  Google Scholar 

  • Lyubenova L, Sabodash X, Schroder P, Michalke B (2015) Selenium species in the roots and shoots of chickpea plants treated with different concentrations of sodium selenite. Environ Sci Pollut Res. doi:10.1007/s11356-015-4755-5

    Google Scholar 

  • Maughan S, Foyer CH (2006) Genetic approaches to modulating the glutathione network in plants, nutriomics and biofortification. Physiol Plant 126:382–397

    Article  CAS  Google Scholar 

  • Mei L, Daud MK, Ullah N, Ali S, Khan M, Malik Z, Zhu SJ (2015) Pretreatment with salicylic acid and ascorbic acid significantly mitigate oxidative stress induced by copper in cotton genotypes. Environ Sci Pollut 1356–015:4075–4079

    Google Scholar 

  • Mishra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189

    Article  Google Scholar 

  • Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973

    Article  CAS  PubMed  Google Scholar 

  • Mroczek-Zdyrska M, Wojcik M (2012) The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res 147:320–328

    Article  CAS  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    Article  CAS  PubMed  Google Scholar 

  • Nemeth M, Janda T, Horvath E, Paldi E, Szalai G (2002) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci 162:569–574

    Article  CAS  Google Scholar 

  • Nowak BH (2013) Comparative effects of selenite and selenate on growth and selenium accumulation in lettuce plants under hydroponic condition. Plant Growth Regul 70:149–157

    Article  Google Scholar 

  • Nowak BH, Matraszek R, Szymanska M (2010) Selenium modifies the effect of short-term chilling stress on cucumber plants. Biol Trace Elem Res 138:307–315

    Article  Google Scholar 

  • Paciolla C, De Leonardis S, Dipierro S (2011) Effects of selenite and selenate on the antioxidant systems in Senecio scandens L. Plant Biosyst 145:253–259

    Article  Google Scholar 

  • Pal M, Szalai G, Horvath E, Janda T, Paldi E (2002) Effect of salicylic acid during heavy metal stress. Acta Biol Szeged 46(3–4):119–120

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pandey C, Gupta M (2015) Selenium and auxin mitigates arsenic stress in rice (Oryza sativa L.) by combining the role of stress indicators, modulators and genotoxicity assays. J Hazard Mater 287:384–391

    Article  CAS  PubMed  Google Scholar 

  • Pandey P, Srivastava RK, Dubey RS (2013) Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology 22:656–667

    Article  CAS  PubMed  Google Scholar 

  • Parlak KU, Yilmaz DD (2012) Response of antioxidant defences to Zn stress in three duckweed species. Ecotoxicol Environ Saf 85:52–58

    Article  Google Scholar 

  • Pena LB, Azpilicueta CE, Gallego SM (2011) Sunflower cotyledons cope with copper stress by inducing catalase subunits less sensitive to oxidation. J Trace Elem Med Biol 25:125–129

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EAH, LeDuc DL (2009) Phytoremediation of selenium using transgenic plants. Curr Opin Biotechnol 20:207–212

    Article  CAS  PubMed  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 

  • Purakayastha TJ, Viswanath T, Bhadraray S, Chhonkar PK, Adhikari PP, Suribabu K (2008) Phytoextraction of zinc, copper, nickel and lead from a contaminated soil by different species of Brassica. Int J Phytoremediation 10:61–72

    Article  CAS  PubMed  Google Scholar 

  • Quinn CF, Freeman JL, Reynolds RJB, Lindblom SD, Cappa JJ, Fakra SF, Marcus MA, Pilon-Smits EAH (2010) Selenium hyperaccumulation offers protection from cell disruptor herbivores. BMC Ecol 10:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramos SJ, Rutzke MA, Hayes RJ, Faquin V, Guilherme LR, Li L (2011) Selenium accumulation in lettuce germplasm. Planta 233:649–660

    Article  CAS  PubMed  Google Scholar 

  • Reeves MA, Hoffman PR (2009) The human selenoproteome: recent insights into functions and regulation. Cell Mol Life Sci 66:2457–2478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rios JJ, Blasco B, Cervilla LM, Rubio-Wilhelmi MM, Ruiz JM, Romero L (2008) Regulation of sulphur assimilation in lettuce plants in the presence of selenium. Plant Growth Regul 56:43–51

    Article  CAS  Google Scholar 

  • Roosens NH, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222:716–729

    Article  CAS  PubMed  Google Scholar 

  • Saidi I, Chtourou Y, Djebali W (2014) Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171:85–91

    Article  CAS  PubMed  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid derived molecules in plant responses and heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Bansal A, Dhillon S, Dhillon K (2010) Comparative effects of selenate and selenite on growth and biochemical composition of rapeseed (Brassica napus L.). Plant Soil 329:339–348

    Article  CAS  Google Scholar 

  • Sharma S, Goyal R, Sadana US (2014) Selenium accumulation and antioxidant status of rice plants grown on seleniferous soil from Northwestern India. Rice Sci 21(6):327–334

    Article  Google Scholar 

  • Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, Pickering IJ, Salt DE (2005) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J 42:785–797

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Srivastava AK, Suprasanna P, D'Souza SF (2009) Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. J Exp Bot 60:3419–3431

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H (2010) Regulation of sulfate transport and assimilation in plants. In: Kwang WJ (ed) International review of cell and molecular biology. Academic Press 129–159

  • Tseng MJ, Liu CW, Yiu JC (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833

    Article  CAS  PubMed  Google Scholar 

  • Wang YS, Wang J, Yang ZM, Lu B, Wang QY, Li SQ, Lu YP, Wang SH, Sun X (2004) Salicylic acid modulates aluminum induced oxidative stress in roots of Cassia tora L. Bot Stud 46:819–828

    CAS  Google Scholar 

  • Wang H, Feng T, Peng X, Yan M, Tang X (2009) Up-regulation of chloroplastic antioxidant capacity is involved in alleviation of nickel toxicity of Zea mays L. by exogenous salicylic acid. Ecotoxicol Environ Saf 72(5):1354–1362

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Zhang S, Wang P, Hou J, Qian J, Ao Y, Lu J, Li L (2011) Salicylic acid involved in the regulation of nutrient elements uptake and oxidative stress in Vallisneria natans (Lour.) Hara under Pb stress. Chemosphere 84:136–142

    Article  CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362

    Article  CAS  PubMed  Google Scholar 

  • Yang ZM, Wang J, Wang SH, Xu LL (2003) Salicylic acid-induced aluminium tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217:168–174

    CAS  PubMed  Google Scholar 

  • Zasoski RJ, Burau RG (1977) A rapid nitric-perchloric acid digestion procedure for multi-element tissue analysis. Commun Soil Sci Plant Anal 8:425–436

    Article  CAS  Google Scholar 

  • Zengin F (2014) Exogenous treatment with salicylic acid alleviating copper toxicity in bean seedlings. PNAS 84:749–755

    CAS  Google Scholar 

  • Zhang Y, Gladyshev VN (2010) General trends in trace element utilization revealed by comparative genomic analyses of Co, Cu, Mo, Ni, and Se. J Biol Chem 285:3393–3405

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Xu S, Yang S, Chen Y (2014) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma. doi:10.1007/s00709-014-0732-y

    Google Scholar 

  • Zhou ZS, Guo K, Abdou-Elbaz A, Yang ZM (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34

    Article  CAS  Google Scholar 

  • Zhu Y-G, Pilon-Smits EAH, Zhao F-J, Williams PN, Meharg AA (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 19:436–442

    Article  Google Scholar 

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SG thanks Council of Scientific and Industrial Research (CSIR), New Delhi, India, for fellowship.

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Gupta, S., Gupta, M. Alleviation of selenium toxicity in Brassica juncea L.: salicylic acid-mediated modulation in toxicity indicators, stress modulators, and sulfur-related gene transcripts. Protoplasma 253, 1515–1528 (2016). https://doi.org/10.1007/s00709-015-0908-0

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