Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage

Abstract

Silicon (Si) is as an important fertilizer element, which has been found effective in enhancing plant tolerance to variety of biotic and a-biotic stresses. This study investigates the Si potential to alleviate zinc (Zn) toxicity stress in cotton (Gossypium hirsutum L.). Cotton plants were grown in hydroponics and exposed to different Zn concentration, 0, 25, and 50 μM, alone and/or in combination with 1 mM Si. Incremental Zn concentration in growth media instigated the cellular oxidative damage that was evident from elevated levels of hydrogen peroxide (H2O2), electrolyte leakage, and malondialdehyde (MDA) and consequently inhibited cotton growth, biomass, chlorophyll pigments, and photosynthetic process. Application of Si significantly suppressed Zn accumulation in various plant parts, i.e., roots, stems, and leaves and thus promoted biomass, photosynthetic, growth parameters, and antioxidant enzymes activity of Zn-stressed as well unstressed plants. In addition, Si reduced the MDA and H2O2 production and electrolyte leakage suggesting its role in protecting cotton plants from Zn toxicity-induced oxidative damage. Thus, the study indicated that exogenous Si application could improve growth and development of cotton crop experiencing Zn toxicity stress by limiting Zn bioavailability and oxidative damage.

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References

  1. Abbas G, Khan MQ, Jamil M, Tahir M, Hussain F (2009) Nutrient uptake, growth and yield of wheat (Triticum aestivum) as affected by zinc application rates. Int J Agric Biol 11:389–396

    CAS  Google Scholar 

  2. Adriano D (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer Verlag, New York

    Google Scholar 

  3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  4. Akhtar KP, Aslam M, Haq MA, Jamil FF, Khan AI, Elahi MT (2005) Plant pathology and nematology. J Cott Sci 9:175–181

    Google Scholar 

  5. Ali S, Farooq MA, Jahangir MM, Abbas F, Bharwana SA, Zhang GP (2013a) Effect of chromium and nitrogen form on photosynthesis and anti-oxidative system in barley. Biol Plant 57:785–791

    Article  Google Scholar 

  6. Ali S, Farooq MA, Yasmeen T, Hussain S, Arif MS, Abbas F, Bharwana SA, Zhang GP (2013b) The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. Ecotoxicol Environ Saf 89:66–72

    Article  CAS  Google Scholar 

  7. Basta NT, Gradwohl R, Snethen KL, Schroder JL (2001) Chemical immobilization of lead, zinc and cadmium in smelter-contaminated soils using bio-solids and rock phosphate. J Environ Qual 30:1222–1230

    Article  CAS  Google Scholar 

  8. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287

  9. Bonnet M, Camares O, Veisseire P (2000) Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot 51:945–953

    Article  CAS  Google Scholar 

  10. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254

    Article  CAS  Google Scholar 

  11. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plant. New Phytol 173:677–702

    Article  CAS  Google Scholar 

  12. Cakmak I (2000) Tansley review no. 111. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  13. Chen HM, Zheng CR, Tu C, She ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234

    Article  CAS  Google Scholar 

  14. Cocker KM, Evans DE, Hodson MJ (1998) The amelioration of aluminum toxicity by silicon in higher plants: solution chemistry or an in planta mechanism. Physiol Planta 104:608–614

    Article  CAS  Google Scholar 

  15. Currie HA, Perry C (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 23:1–7

    Google Scholar 

  16. Cuypers A, Vangronsveld J, Clijsters H (1999) The chemical behavior of heavy metals plays a prominent role in the induction of oxidative stress. Free Radic Res 31:839–843

    Article  Google Scholar 

  17. Cuypers A, Vangronsveld J, Clijsters H (2001) The redox status of the plant cells (AsA and GSH) is sensitive to zinc imposed oxidative stress in roots and primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 39:657–664

    Article  CAS  Google Scholar 

  18. Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603

    Article  CAS  Google Scholar 

  19. Dembitsky VM, Rezanka T (2003) Natural occurrence of arseno compounds in plants, lichens, fungi, algal species, and microorganisms. Plant Sci 165:1177–1192

    Article  CAS  Google Scholar 

  20. Dhindsa RS, Dhindsa PP, Thorpe TA (1981) Leaf senescence, correlated with increased level of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  21. Dionisio-Sese ML, Tobita S, (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

  22. Drazkiewice M (1994) Chlorophyll-occurrence, function and mechanism of action. Environ Exp Bot 42:1–10

    Google Scholar 

  23. Ehsan S, Ali S, Noureen S, Farid M, Shakoor MB, Aslam A, Bharwana SA, Tauqeer HM (2013) Comparative assessment of different heavy metals in urban soil and vegetables irrigated with sewage/industrial waste water. Ecoterra 35:37–53

    Google Scholar 

  24. Ehsan S, Ali S, Noureen S, Mehmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of Cd by Brassica napus L. Ecotoxicol Environ Saf 106:164–172

    Article  CAS  Google Scholar 

  25. Epstein E (1994) The anomaly of silicon in plant biology. Proc Nat Acad Sci USA 91:11–17

    Article  CAS  Google Scholar 

  26. Epstein E (1999) Silicon. Annu Rev Plant Physiol Mol Biol 50:641–664

  27. Falkengren-Grerup U, Linnermark N, Tyler G (1987) Chemosphere 16:2239

    Article  CAS  Google Scholar 

  28. Farid M, Ali S, Shakoor MB, Bharwana SA, Rizvi H, Ehsan S, Tauqeer HM, Iftikhar U, Hannan F (2013a) EDTA assisted phytoremediation of cadmium, lead and zinc. Int J Agron Plant Prod 4(11):2833–2846

    CAS  Google Scholar 

  29. Farid M, Shakoor MB, Ehsan S, Ali S, Zubair M, Hanif MS (2013b) Morpho- logical, physiological and biochemical responses of different plant species to Cd stress. Int J Chem Biochem Sci 3:53–60

    Google Scholar 

  30. Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321

    Article  CAS  Google Scholar 

  31. Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979

    Article  CAS  Google Scholar 

  32. Gong HJ, Chen KM, Zhao ZG, Chen GC, Zhou WJ (2008) Effects of silicon on defense of wheat against oxidative stress under drought at different developmental stages. Biol Plant 52:592–596

    Article  CAS  Google Scholar 

  33. Gonzalez LF, Rojas MC, Perez FJ (1999) Diferulate and lignin formation is related to biochemical differences of wall-bound peroxidases. Phytochem 50:711–717

    Article  CAS  Google Scholar 

  34. Gurmani AR, Bano A, Najeeb U, Zhang JL, Khan SU, Flowers TJ (2013) Exogenously applied silicate and abscisic acid ameliorate the growth of salinity stressed wheat (Triticum aestivum L) seedlings through Na+ exclusion. Aus J Crop Sci 7(8):1123–1130

    Google Scholar 

  35. Han FX, Banin A, Su Y, Monts DL, Plodinec MJ, Kingery WL, Triplett GE (2002) Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften 89:497–504

    Article  CAS  Google Scholar 

  36. Hattori T, Inanaga S, Araki H, An P, Morita S, Luxov AM, Lux A (2005) Application of silicon enhanced drought tolerance in Sorghum bicolor. Physiol Plant 123:459–466

    Article  CAS  Google Scholar 

  37. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  CAS  Google Scholar 

  38. Kaya C, Tuna AL, Sonmez O, Ince F, Higgs D (2009) Mitigation effects of silicon on maize plants grown at high zinc. J Plant Nutr 32:1788–1798

    Article  CAS  Google Scholar 

  39. Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84

    Article  Google Scholar 

  40. Liang Y, Si J, R¨Omheld V (2005) Silicon uptake and transport is an active process in Cucumis sativus. New Phytol 167:797–804

    Article  CAS  Google Scholar 

  41. Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428

    Article  CAS  Google Scholar 

  42. Luo YM, Christie P, Baker AJM (2000) Soil solution Zn and pH dynamics in non- rhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cd contaminated soil. Chemosphere 41:161–164

    Article  CAS  Google Scholar 

  43. Luo ZB, He XJ, Chen L, Tang S, Chen F (2010) Effects of zinc on growth and antioxidant responses in Jatropha curcas seedlings. Int J Agric Biol 12:119–124

    CAS  Google Scholar 

  44. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, pp 411–430

    Google Scholar 

  45. Miller GW, Huang IJ, Welkie GW, Pushnik JC (1995) Function of iron in plants with special emphasis on chloroplasts and photosynthetic activity. In Iron Nutrition in Soils and Plants. Springer Netherlands, pp 19–28

  46. Ming DF, Pei ZF, Naeem MS, Gong HJ, Zhou WJ (2012) Silicon alleviates PEG-induced water-deficit stress in upland rice seedlings by enhancing osmotic adjustment. J Agron Crop Sci 198:14–26

    Article  CAS  Google Scholar 

  47. Mittler R, Vanderauwera S, Gollery M, Breusegem FB (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  Google Scholar 

  48. Morina F, Jovanovic LJ, Mojovic M, Vidovic M, Pankovic D, Veljovic-Jovanovic S (2010) Zinc-induced oxidative stress in Verbascum thapsus is caused by an accumulation of reactive oxygen species and quinhydrone in the cell wall. Physiol Plant 140:209–224

    CAS  Google Scholar 

  49. 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 

  50. Neumann D, Nieden UZ (2001) Silicon and heavy metal tolerance of higher plants. Phytochem 56:685–692

    Article  CAS  Google Scholar 

  51. Pei ZF, Ming DF, Liu D, Wan GL, Geng XX, Gong HJ, Zhou WJ (2010) Silicon improves the tolerance to water-deficit stress induced by polyethylene glycol in wheat (Triticum aestivum L.) seedlings. J Plant Growth Regul 29:106–115

    Article  CAS  Google Scholar 

  52. Putter J, Becker R (1974) Methods of enzymatic analysis. Academic Press, Chicago

  53. Rao AR, Dayananda C, Sarada R, Shamala TR, Ravishankar GA (2007) Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresour Technol 98:560–564

    Article  CAS  Google Scholar 

  54. Rogalla H, Romheld V (2002) Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumic sativus L. Plant Cell Environ 25:549–555

    Article  CAS  Google Scholar 

  55. Shi XH, Zhang CC, Wang H (2005) Effect of Si on the distribution of Cd in rice seedlings. Plant Soil 272:53–60

    Article  CAS  Google Scholar 

  56. Szlek M, Miller GW, Welkie GW (1990) Potassium effect of iron stress in tomato plants. 1. The effect on pH, Fe-reductase and chlorophyll. J Plant Nutr 13:215–219

    Article  CAS  Google Scholar 

  57. Tewari RK, Kumar P, Sharma PN (2008) Morphology and physiology of zinc-stressed mulberry plants. J Plant Nutr Soil Sci 171:286–294

    Article  CAS  Google Scholar 

  58. Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35(5):785–791

  59. Zhao FJ, Lombi E, Mcgrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank the Higher Education Commission of Pakistan for the financial support. The results presented in this paper are a part of M. Phil studies of Shad Ali Anwaar.

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Correspondence to Shafaqat Ali.

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Anwaar, S.A., Ali, S., Ali, S. et al. Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ Sci Pollut Res 22, 3441–3450 (2015). https://doi.org/10.1007/s11356-014-3938-9

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Keywords

  • Antioxidant enzymes
  • Biomass
  • Zinc
  • Silicon
  • Growth