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Sulfur mediated improved thiol metabolism, antioxidant enzymes system and reduced chromium accumulation in oilseed rape (Brassica napus L.) shoots

Abstract

Chromium (Cr) pollution is at a worrying level in a region of oilseed rape production in China. Sulfur (S) is an indispensable element for plants that has been confirmed to play an important role in regulating plant response to heavy metal stress. The present study was conducted to examine the role of S in alleviating Cr toxicity in oilseed rape. Cr stress strongly induced oxidative stress and inhibited plant growth. Application of S significantly enhanced the tolerance of oilseed rape exposed to Cr stress by activating several detoxification mechanisms including the ascorbate-glutathione (AsA-GSH) enzyme defense system and GSH production. The Cr and phytochelatins (PC) contents in the root under S treatment were markedly higher than those under Cr stress. The transcript abundances of the heavy metal transporters HMA2 and HMA4 were lower under S treatment than under Cr treatment. Most Cr was restricted to roots, and the translocation factor (TF) of Cr was markedly decreased in oilseed rape. In conclusion, our study revealed that S application is advantageous to oilseed rape defense against Cr toxicity and inhibits Cr translocation from roots to shoots.

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References

  1. Adhikari S, Ghosh S, Azahar I, Adhikari A, Shaw AK, Konar S, Roy S, Hossain Z (2018) Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize. Environ Exp Bot 153:143–162. https://doi.org/10.1016/j.envexpbot.2018.05.008

  2. Ali S, Farooq MA, Hussain S, Yasmeen T, Abbasi GH, Zhang G (2013) Alleviation of chromium toxicity by hydrogen sulfide in barley. Environ Toxicol Chem 32:2234–2239

  3. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E, Ahmad I, Tuteja R, Tuteja N (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251:1265–1283. https://doi.org/10.1007/s00709-014-0636-x

  4. Bhargava P, Srivastava AK, Urmil S, Rai LC (2005) Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. J Plant Physiol 162:1220–1225

  5. Buchner P, Takahashi H, Hawkesford MJ (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773

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

  7. de Pinto MC, Tommasi F, De Gara L (2000) Enzymes of the ascorbate biosynthesis and ascorbate. Plant Physiol Biochem 38:541–550

  8. Devi SR, Prasad MNV (1998) Copper toxicity in Ceratophyllum demersum L. (Coontail), a free floating macrophyte: response of antioxidant enzymes and antioxidants. Plant Sci 138:157–165

  9. 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. https://doi.org/10.1016/j.plaphy.2015.11.005

  10. Dixit G, Singh AP, Kumar A, Singh PK, Kumar S, Dwivedi S, Trivedi PK, Pandey V, Norton GJ, Dhankher OP, Tripathi RD (2015) Sulfur mediated reduction of arsenic toxicity involves efficient thiol metabolism and the antioxidant defense system in rice. J Hazard Mater 298:241–251. https://doi.org/10.1016/j.jhazmat.2015.06.008

  11. Esaka M, Hattori T, Fujisawa K, Sakajo S, Asahi T (1990) Molecular cloning and nucleotide sequence of full-length cDNA for ascorbate oxidase from cultured pumpkin cells. Eur J Biochem 191:537–541

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

  13. Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus. L Chemosphere 120:154–164

  14. Guo WJ, Meetam M, Goldsbrough PB (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706. https://doi.org/10.1104/pp.108.115782

  15. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

  16. Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family—redundancy or specialization? [review]. Physiol Plant 117:155–163

  17. Hernandez LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Caceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911. https://doi.org/10.1093/jxb/erv063

  18. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339. https://doi.org/10.1105/tpc.020487

  19. Labrou NE, Papageorgiou AC, Pavli O, Flemetakis E (2015) Plant GSTome: structure and functional role in xenome network and plant stress response. Curr Opin Biotechnol 32:186–194

  20. Lancilli C, Giacomini B, Lucchini G, Davidian J-C, Cocucci M, Sacchi GA, Nocito FF (2014) Cadmium exposure and sulfate limitation reveal differences in the transcriptional control of three sulfate transporter (Sultr1;2) genes in Brassica juncea. BMC Plant Biol 14:132. https://doi.org/10.1186/1471-2229-14-132

  21. Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165. https://doi.org/10.1146/annurev.arplant.51.1.141

  22. Liang T, Ding H, Wang G, Kang J, Pang H, Lv J (2016) Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulfur assimilation and glutathione metabolism in Brassica chinensis. L Ecotoxicol Environ Saf 124:129–137. https://doi.org/10.1016/j.ecoenv.2015.10.011

  23. Lou L, Kang J, Pang H, Li Q, Du X, Wu W, Chen J, Lv J (2017) Sulfur protects Pakchoi (Brassica chinensis L.) seedlings against cadmium stress by regulating ascorbate-glutathione metabolism. Int J Mol Sci 18. https://doi.org/10.3390/ijms18081628

  24. Ma F, Cheng L (2003) The sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate–glutathione pathway than the shaded peel. Plant Sci 165:819–827

  25. Maruyamanakashita A, Nakamura Y, Watanabetakahashi A, Yamaya T, Takahashi H (2004) Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol 45:340–345

  26. Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791. https://doi.org/10.1016/j.febslet.2004.12.040

  27. Mills RF, Peaston KA, Runions J, Williams LE (2012) HvHMA2, a P 1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS One 7:e42640

  28. Mourato MP, Moreira IN, Leitao I, Pinto FR, Sales JR, Martins LL (2015) Effect of heavy metals in plants of the genus Brassica. Int J Mol Sci 16:17975–17998. https://doi.org/10.3390/ijms160817975

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

  30. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148. https://doi.org/10.1104/pp.105.076240

  31. 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. https://doi.org/10.1111/j.1365-3040.2011.02400.x

  32. Packer RK, Garvin JL (1998) Seasonal differences in activity of perch (Perca flavescens) gill Na + /K + ATPase. Comp Biochem Physiol B Biochem Mol Biol 120:777–783

  33. Pinto MCD, Tommasi F, Gara LD (2000) Enzymes of the ascorbate biosynthesis and ascorbate-glutathione cycle in cultured cells of tobacco Bright Yellow 2. Plant Physiol Biochem 38:541–550

  34. Satohnagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224

  35. Schiavon M, Galla G, Wirtz M, Pilon-Smits EA, Telatin V, Quaggiotti S, Hell R, Barcaccia G, Malagoli M (2012) Transcriptome profiling of genes differentially modulated by sulfur and chromium identifies potential targets for phytoremediation and reveals a complex S-Cr interplay on sulfate transport regulation in B. juncea. J Hazard Mater 239-240:192–205. https://doi.org/10.1016/j.jhazmat.2012.08.060

  36. Schiavon M, Pilon-Smits EA, Wirtz M, Hell R, Malagoli M (2008) Interactions between chromium and sulfur metabolism in Brassica juncea. J Environ Qual 37:1536–1545. https://doi.org/10.2134/jeq2007.0032

  37. Schiavon M, Wirtz M, Borsa P, Quaggiotti S, Hell R, Malagoli M (2007) Chromate differentially affects the expression of a high-affinity sulfate transporter and isoforms of components of the sulfate assimilatory pathway in Zea mays (L.). Plant Biol (Stuttg) 9:662–671. https://doi.org/10.1055/s-2007-965440

  38. Sheng H, Zeng J, Liu Y, Wang X, Wang Y, Kang H, Fan X, Sha L, Zhang H, Zhou Y (2016) Sulfur mediated alleviation of Mn toxicity in Polish wheat relates to regulating Mn allocation and improving antioxidant system. Front Plant Sci 7:1382. https://doi.org/10.3389/fpls.2016.01382

  39. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254. https://doi.org/10.1007/s10311-013-0407-5

  40. Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2015) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143

  41. Tan J, Wang J, Chai T, Zhang Y, Feng S, Li Y, Zhao H, Liu H, Chai X (2013) Functional analyses of TaHMA2, a P(1B)-type ATPase in wheat. Plant Biotechnol J 11:420–431

  42. UdDin I, Bano A, Masood S (2015) Chromium toxicity tolerance of Solanum nigrum L. and Parthenium hysterophorus L. plants with reference to ion pattern, antioxidation activity and root exudation. Ecotoxicol Environ Saf 113:271–278. https://doi.org/10.1016/j.ecoenv.2014.12.014

  43. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

  44. Williams LE, Mills RF (2005) P(1B)-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502. https://doi.org/10.1016/j.tplants.2005.08.008

  45. Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126

  46. Wong CK, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78. https://doi.org/10.1111/j.1469-8137.2008.02638.x

  47. Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Hu C (2015) Xylem transport and gene expression play decisive roles in cadmium accumulation in shoots of two oilseed rape cultivars (Brassica napus). Chemosphere 119:1217–1223. https://doi.org/10.1016/j.chemosphere.2014.09.099

  48. Xu J, Yin H, Liu X, Li X (2010) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459. https://doi.org/10.1007/s00425-009-1070-8

  49. Yamaji N, Xia J, Mitaniueno N, Yokosho K, Feng MJ (2013) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol 162:927–939

  50. Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473

  51. Zhang B, Pasini R, Dan H, Joshi N, Zhao Y, Leustek T, Zheng ZL (2014a) Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. Plant J 77:185–197

  52. Zhang XM, Zhang XY, Zhong TY, Jiang H (2014b) Spatial distribution and accumulation of heavy metal in arable land soil of China. Huan Jing Ke Xue 35:692–703

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Funding

This work was supported by Agricultural Science and Technology Innovation of Shaanxi Province Key Project (China, 2016NY-135), The Science and Technology Program of Yangling (China, 2018SF-05), and the Nation Natural Science Foundation of China (NO. 31271624).

Author information

Correspondence to Jinyin Lv.

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Responsible editor: Philippe Garrigues

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Zhang, X., Kang, J., Pang, H. et al. Sulfur mediated improved thiol metabolism, antioxidant enzymes system and reduced chromium accumulation in oilseed rape (Brassica napus L.) shoots. Environ Sci Pollut Res 25, 35492–35500 (2018). https://doi.org/10.1007/s11356-018-3517-6

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Keywords

  • Chromium
  • Sulfur
  • Oilseed rape
  • Sulfur metabolism
  • Ascorbate-glutathione cycle
  • Sulfur and chromium transporters