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Sulphur and calcium attenuate arsenic toxicity inBrassicaby adjusting ascorbateglutathione cycle and sulphur metabolism

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Abstract

Present study was performed in order to explicate whether added sulphur (S; 60 mg S kg−1 sand) and calcium (Ca; 250 mg Ca kg−1 sand) alone and in combination could modulate arsenic-induced (As1; 15 mg As kg−1 sand and As2; 30 mg As kg−1 sand) toxicity in Brassica juncea L. seedlings. To study this, growth and growth regulating processes i.e. status of oxidative stress biomarkers (H2O2 generation and lipid peroxidation), enzymes and metabolites of AsA-GSH cycle and S-metabolism were examined. Both the doses of As significantly reduced the growth as evident from diminishing dry weight and increased lipid peroxidation as a consequence of excess H2O2 accumulation. Arsenic also altered the redox status of the cell thereby depleting the AsA and GSH pool that consequently decreased AsA/DHA, AsA/H2O2 and GSH/GSSG ratios. Neverthless, APX, DHAR and GR activities were enhanced under similar conditions. Contrary to this, additional S and/ or Ca maintained the redox status of the cell that improved AsA/DHA and GSH/GSSG ratios, and further enhanced the enzymatic activities in both root and leaves of the test seedlings. Upon As exposure, test seedlings exhibited an increase in S assimilation as a result of increased enzyme activities of ATPS, OASTL and γ-ECS, which were further enhanced upon S and/ or Ca addition to stressed seedlings. Due to increment in S assimilation, PCs synthesis was also increased that restricted As translocation from root to shoot. Collectively, our result provides an insight for protective role of S and Ca alone and more efficiently in combination (S+Ca) to As-stressed Brassica seedlings suggesting that S and Ca together could be a promising candidates in managing As toxicity in crops.

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References

  • Ahmad P, Abdel Latef AA, AbdAllah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (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 

  • Ahsan N, Lee DG, Kim KH, Alam I, Lee SH, Lee KW, Lee H, Lee BH (2010) Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78:224–231

    Article  CAS  PubMed  Google Scholar 

  • Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds) Methods in plant ecology. Blackwell, Oxford, pp 285–344

    Google Scholar 

  • Anderson JW (2014) Assimilation of inorganic sulfate into cysteine. Biochem Plants 5:203–223

    Google Scholar 

  • Brehe JE, Burch HB (1976) Enzymatic assay for glutathione. Anal Biochem 74:189–197

    Article  CAS  PubMed  Google Scholar 

  • Bundschuh J, Bhattacharya P, Sracek O, Mellano MF, Ramírez AE, Storniolo AR, Martín RA, Cortés J, Litter MI, Jean JS (2011) Arsenic removal from groundwater of the Chaco-Pampean plain (Argentina) using natural geological materials as adsorbents. J Environ Sci Health 46:1297–1310

    Article  CAS  Google Scholar 

  • Capaldi R, Gratão PL, Reis AR, Lima LW, Azevedo RA (2015) Sulfur metabolism and stress defense responses in plants. Tropical Plant Biol 8:60–73

    Article  CAS  Google Scholar 

  • De Tullio MC, Paciolla C, DallaVecchia F, Rascio N, D’Emerico S, De Gara L, Liso R, Arrigoni O (1999) Changes in onion root development induced by the inhibition of peptidyl-proyl hydroxylase and influence of the ascorbate system on cell division and elongation. Planta 209:424–434

    Article  PubMed  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    Article  CAS  PubMed  Google Scholar 

  • Dixit G, Singh AP, Kumar A, Dwivedi S, Deeba F, Kumar S, Suman S, Adhikari B, Shukla Y, Trivedi PK, Pandey V, Tripathi RD (2015) Sulfur alleviates arsenic toxicity by reducing its accumulation and modulating proteome, amino acids and thiol metabolism in rice leaves. Sci Rep 5:16205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixit G, Singh AP, Kumar A, Mishra S, Dwivedi S, Kumar S, Trivedi PK, Pandey V, Tripathi RD (2016) Reduced arsenic accumulation in rice (Oryza sativa L.) shoot involves sulfur mediated improved thiol metabolism, antioxidant system and altered arsenic transporters. Plant Physiol Biochem 99:86–96

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  • Food and Agricultural Organization [FAO] (2009) How to Feed the World in 2050. Food and Agriculture Organization, Rome

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    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 

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

    Article  CAS  Google Scholar 

  • Grant CA, Mahli SS, Karamanos RE (2012) Sulfur management for rapeseed. Field Crops Res 128:119–128

    Article  Google Scholar 

  • Gupta M, Ahmad MA (2014) Arsenate induced differential response in rice genotypes. Ecotoxicol Environ Saf 107:46–54

    Article  CAS  PubMed  Google Scholar 

  • Hartley-Whitaker J, Ainsworth G, Vooijs R, Bookum WT, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126:299–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hernandez JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–39

    Google Scholar 

  • Hossain MA, Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295

    CAS  Google Scholar 

  • Huang J, Zhang J, Yu YM, Liu JX, Li MJ, Zhu KY (2012) Effects of calcium fertilizer on the development, survival, and feeding of B-biotype Bemisia tabaci on Euphorbia pulcherrima. J Appl Ecol 23:2521–2528

    CAS  Google Scholar 

  • Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal induced oxidative stress defenses. Int J Mol Sci 13:3145–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan NA, Nazar R, Anjum NA (2009) Growth, photosynthesis and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in ATP-sulfurylase activity under salinity stress. Sci Hort 122:455–460

    Article  CAS  Google Scholar 

  • Kirkegaard JA, Hocking PJ, Angus JF, Howe GN, Gardner PA (1997) Comparison of canola, Indian mustard and Linola in two contrasting environments. II. Break-crop and nitrogen effects on subsequent wheat crops. Field Crops Res 52:179–191

    Article  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO42־ uptake in intact canola. The role of phloem translocated glutathione. Plant Physiol 111:147–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang T, Ding H, Wang G, Kang J, Pang H, Lv J (2016) Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulphur assimilation and glutathione metabolism in Brassica chinensis L. Ecotoxicol Environ Saf 124:129–137

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Li Z, Wu J, Shen Y, Li Y, Zou B, Tang Y, Zhuang P (2017) Influences of calcium silicate on chemical forms and subcellular distribution of cadmium in Amaranthus hypochondriacus L. Sci Rep 7:40583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Markovska YK, Gorinova NI, Nedkovska MP, Miteva KM (2009) Cadmium-induced oxidative damage and antioxidant responses in Brassica juncea plants. Biol Plant 53:151–154

    Article  CAS  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione-S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  CAS  PubMed  Google Scholar 

  • McCarty KM, Hanh HT, Kim KW (2011) Arsenic geochemistry and human health in South-East Asia. Rev Environ Health 26:71–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNeill A, Eriksen J, Bergström L, Smith K, Marstorp H, Kirchmann H, Nilsson I (2005) Nitrogen and sulphur management: challenges for organic sources in temperate agricultural systems. Soil Use Manag 21:82–93

    Article  Google Scholar 

  • Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitrobluetetrazolium. Anal Biochem 212:540–546

    Article  CAS  PubMed  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate–specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Newman DK, Beveridge TJ, Morel F (1997) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Appl Environ Microbiol 63:2022–2028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Phartiyal P, Kim WS, Cahoon RE, Jez JM, Krishnan HB (2006) Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch Biochem Biophys 450:20–29

    Article  CAS  PubMed  Google Scholar 

  • Rahman H, Xu YP, Zhang XR, Cai XZ (2016) Brassica napus genome possesses extraordinary high number of CAMTA genes and CAMTA3 contributes to PAMP triggered immunity and resistance to Sclerotinia sclerotiorum. Front Plant Sci 7:581

    PubMed  PubMed Central  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    Article  CAS  PubMed  Google Scholar 

  • Riemenschneider A, Riedel K, Hoefgen R, Papenbrock J, Hesse H (2005) Impact of reduced acetylserine (thiol) lyase isoform contents on potato plant metabolism. Plant Physiol 137:892–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochaix JD (2011) Assembly of the photosynthetic apparatus. Plant Physiol 155:1493–1500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruíz-Torres C, Feriche-Linares R, Rodríguez-Ruíz M, Palma JM, Corpas FJ (2017) Arsenic induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH generating systems in roots. J Plant Physiol 211:27–35

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Kurosawa M, Tatsuguchi K, Takagi Y, Murakoshi I (1994) Modulation of cysteine biosynthesis in chloroplasts of transgenic tobacco over expressing cysteine synthase [O-acetylserine (thiol)-lyase]. Plant Physiol 106:887–895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schadle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  Google Scholar 

  • Sebastian A, Prasad MNV (2014) Photosynthesis mediated decrease in cadmium translocation protect shoot growth of Oryza sativa seedlings up on ammonium phosphate-sulfur fertilization. Environ Sci Pollut Res 21:986–997

    Article  CAS  Google Scholar 

  • Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453

    Article  CAS  Google Scholar 

  • Singh M, Kushwaha BK, Singh S, Kumar V, Singh VP, Prasad SM (2017) Sulphur alters chromium (VI) toxicity in Solanum melongena seedlings: role of sulphur assimilation and sulphur containing antioxidants. Plant Physiol Biochem 112:183–192

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Parihar P, Prasad SM (2018a) Simultaneous exposure of sulphur and calcium hinder As toxicity: up-regulation of growth, mineral nutrients uptake and antioxidants system. Ecotoxicol Environ Saf 161:318–331

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Parihar P, Prasad SM (2018b) Sulfur and calcium simultaneously regulate photosynthetic performance and nitrogen metabolism status in As-challenged Brassica juncea L. seedlings. Front Plant Sci 9:772

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270

    Article  CAS  PubMed  Google Scholar 

  • Song WY, Martinoia E, Lee J, Kim D, Kim DY, Vogt E, Shim D, Choi KS, Hwang I, Lee Y (2004) A novel family of cys-rich membrane proteins mediates cadmium resistance in Arabidopsis. Plant Physiol 135:1027–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan W, Meng Q, Brestic M, Olsovska K, Yang X (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168:2063–2071

    Article  CAS  PubMed  Google Scholar 

  • Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84:63–69

    Article  CAS  PubMed  Google Scholar 

  • Tommasi F, Paciolla C, de Pinto MC, De Gara L (2001) A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. J Exp Bot 52:1647–1654

    Article  CAS  PubMed  Google Scholar 

  • Tuli R, Chakrabarty D, Trivedi PK, Tripathi RD (2010) Recent advances in arsenic accumulation and metabolism in rice. Mol Breed 26:307–323

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain treated bean plants. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Xin H, Falk CK, Yu P (2013) Studies on Brassica carinata seed. 2. Carbohydrate molecular structure in relation to carbohydrate chemical profile, energy values, and biodegradation characteristics. J Agric Food Chem 61:10127–10134

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Li X, Zhang L (2013) The effect of calcium chloride on growth, photosynthesis, and antioxidant responses of Zoysia japonica under drought conditions. PLoS ONE 8:e68214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav S (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Ye B, Gitler C, Gressel J (1997) A High-sensitivity, single-gel, polyacrylamide gel electrophoresis method for the quantitative determination of glutathione reductases. Anal Biochem 246:159–165

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Rachana Singh and Parul Parihar are very grateful to the University Grants Commission, New Delhi for providing financial support (as UGC-AU research scholar) to carry out present work. Authors are also thankful to DST-FIST programme funded by Department of Science and Technology, New Delhi, India to Department of Botany, University of Allahabad, Allahabad for providing necessary facilities.

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Singh, R., Parihar, P. & Prasad, S.M. Sulphur and calcium attenuate arsenic toxicity inBrassicaby adjusting ascorbateglutathione cycle and sulphur metabolism. Plant Growth Regul 91, 221–235 (2020). https://doi.org/10.1007/s10725-020-00601-8

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