Skip to main content
Log in

The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The objective of this study is to elucidate the roles of silicon (Si) in enhancing tolerance to excess zinc (Zn) in two contrasting rice (Oryza sativa L.) cultivars: i.e. cv. TY-167 (Zn-resistant) and cv. FYY-326 (Zn-sensitive). Root morphology, antioxidant defense reactions and lipid peroxidation, and histochemical staining were examined in rice plants grown in the nutrient solutions with normal (0.15 μM) and high (2 mM) Zn supply, without or with 1.5 mM Si. Significant inhibitory effects of high Zn treatment on plant growth were observed. Total root length (TRL), total root surface area (TRSA) and total root tip amount (TRTA) of both cultivars were decreased significantly in plants treated with high Zn, whereas these root parameters were significantly increased when Zn-stressed plants were supplied with 1.5 mM Si. Supply of Si also significantly decreased Zn concentration in shoots of both cultivars, indicating lower root-to-shoot translocation of Zn. Moreover, superoxide dismutase (SOD), catalase (CAT), and asorbate peroxidase (APX) activities were increased, whereas malondialdehyde (MDA) and hydrogen peroxide (H2O2) concentrations were decreased in Si-supplied plants of both Zn-sensitive and Zn-resistant rice cultivars exposed to Zn stress. These alleviative effects of Si, further confirmed by the histochemical staining methods, were more prominent in the Zn-resistant cultivar than in the Zn-sensitive one. Taken together, all these results suggest that Si-mediated alleviation of Zn toxicity is mainly attributed to Si-mediated antioxidant defense capacity and membrane integrity. The possible role of Si in reduction of root-to-shoot translocation of Zn can also be considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F, Agata W, Kaufman PB (1998) Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L), monitored by electrolyte leakage. Plant Prod Sci 1:96–103

    Article  Google Scholar 

  • Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stressors. Aquatic Toxicology 78:325–331

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol 43:83–116

    Article  CAS  Google Scholar 

  • 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 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Chung MJ, Walker PA, Brown RW, Hogstrand C (2005) Zinc-mediated gene expression offers protection against H2O2-induced cytotoxicity. Toxicology Appl Pharmacol 205:225–236

    Article  CAS  Google Scholar 

  • Cocker KM, Evans DE, Hodson MJ (1998) The amelioration of aluminium toxicity by silicon in higher plants: Solution chemistry or an in planta mechanism? Physiol Plant 104:608–614

    Article  CAS  Google Scholar 

  • Cuypers A, Vangronsveld J, Clijsters H (2001) The redox status of 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 

  • Dai WM, Zhang KQ, Duan BW, Sun CX, Zheng KL, Cai Y, Zhuang JY (2005) Rapid determination of silicon content in rice (Oryza sativa). Chinese J Rice Sci 19:460–462

    CAS  Google Scholar 

  • Dragišić Maksimović J, Bogdanović J, Maksimović V, Nikolic M (2007) Silicon modulates the metabolism and utilization of phenolic compounds in cucumber (Cucumis sativus L.) grown at excess manganese. J Plant Nutr Soil Sci 170:739–744

    Article  Google Scholar 

  • Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781

    Article  CAS  Google Scholar 

  • EI-Ghamery AA, El-Kholy MA, Abou El-Yousser MA (2003) Evaluation of cytological effects of Zn2+ in relation to germination and root growth of Nigella sativa L. and Triticum aestivum L. Mutat Res 537:29–41

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fontes RLF, Cox FR (1998) Iron deficiency and zinc toxicity in soybean grown in nutrient solution with different levels of sulfur. J Plant Nutr 21:1715–1722

    Article  CAS  Google Scholar 

  • Fornazier RF, Ferreira RR (2002) Effects of Cadmium on antioxidant enzyme activities in sugar cane. Biol Plant 45:91–97

    Article  CAS  Google Scholar 

  • Foyer CH, Descourvie´res P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Fridovich I (1978) The biology of oxygen radicals. Sci 201:875–880

    Article  CAS  Google Scholar 

  • Führs H, Goötze1 S, Specht A, Erban A, Gallien S, Heintz D, Van Dorsselaer A, Kopka J, Braun H-P, Horst WJ (2009) Characterization of leaf apoplastic peroxidases and metabolites in Vigna unguiculata in response to toxic manganese supply and silicon. J Exp Bot 60:1663–1678

    Article  PubMed  Google Scholar 

  • Galvez L, Clark RB, Gourley LM, Maranville JW (1987) Silicon interaction with manganese and aluminum toxicity in Sorghum. J Plant Nutr 10:1139–1147

    Article  CAS  Google Scholar 

  • Gong HJ, Zhu XY, Chen KM, Wang SM, Zhang CL (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Bagci EG, Coban S, Pilbeam DJ (2007a) Silicon mediates changes to some physiological and enzymatic parameters symptomatic for oxidative stress in spinach (Spinacia oleracea L.) grown under B toxicity. Sci Hortic-Amsterdam 113:113–119

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Bagci EG, Coban S, Sahin O (2007b) Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. Biol Plant 51:571–574

    Article  CAS  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Li ZJ, 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  PubMed  CAS  Google Scholar 

  • Hammond KE, Evans DE, Hodson MJ (1995) Aluminium/silicon interactions in barley (Hordeum vulgare L.) seedlings. Plant Soil 173:89–95

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hodson MJ, Evans DE (1995) Aluminium silicon interactions in higher plants. J Exp Bot 46:161–171

    Article  CAS  Google Scholar 

  • Horiguchi T (1988) Mechanism of manganese toxicity and tolerance in plants. IV. Effect of silicon on alleviation of manganese toxicity of rice plants. Soil Sci Plant Nutr 34:65–73

    CAS  Google Scholar 

  • Iwasaki K, Maier P, Fecht-Christoffers M, Horst W (2002) Effects of silicon supply on apoplastic manganese concentrations in leaves and their relation to manganese tolerance in cowpea Vigna unguiculata (L.) Walp. Plant Soil 238:281–288

    Article  CAS  Google Scholar 

  • 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 

  • Kiekens L (1990) Zinc. In: Alloway BJ (ed) Heavy Metals in Soils. Blackie Academic and Professional, Glasgow, pp 284–305

    Google Scholar 

  • Langer I, Krpata D, Fitz WJ, Wenzel WW, Schweiger PF (2009) Zinc accumulation potential and toxicity threshold determined for a metal-accumulating Populus canescens clone in a dose-response study. Environ Pollut 157:2871–2877

    Article  PubMed  CAS  Google Scholar 

  • Liang YC (1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant Soil 209:217–224

    Article  CAS  Google Scholar 

  • Liang YC, Chen Q, Liu Q, Zhang WH, Ding RX (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J Plant Physiol 160:1157–1164

    Article  PubMed  CAS  Google Scholar 

  • Liang YC, Shen QR, Shen ZG (1996) Effect of silicon on salinity tolerance of two barley cultivars. J Plant Nutr 19:173–183

    Article  CAS  Google Scholar 

  • Liang YC, Sun WC, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: A review. Environ Pollut 147:422–428

    Article  PubMed  CAS  Google Scholar 

  • Liang YC, Wong JWC, Wei L (2005) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:475–483

    Article  PubMed  CAS  Google Scholar 

  • Liang YC, Zhang WH, Chen Q, Liu YL, Ding RX (2006) Effect of exogenous silicon (Si) on H+-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 57:212–219

    Article  CAS  Google Scholar 

  • Liang YC, Zhu J, Li ZJ, Chu GX, Ding YF, Zhang J, Sun WC (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ Exp Bot 64:286–294

    Article  CAS  Google Scholar 

  • Lidon FC, Henriques FS (1992) Effects of copper on the nitrate to ammonia reduction mechanism in rice plants. Photosynthetica 26:371–380

    CAS  Google Scholar 

  • Lin CW, Chang HB, Huang HJ (2005) Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots. Plant Physiol Biochem 43:963–968

    Article  PubMed  CAS  Google Scholar 

  • Ma JA (2004a) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18

    CAS  Google Scholar 

  • Ma JF, Shen R, Nagao S, Tanimoto E (2004b) Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol 45:583–589

    Article  CAS  Google Scholar 

  • Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier Science B.V, Netherlands

  • Ma JF, Tamai K, Ichii M, Wu GF (2002) A rice mutant defective in Si uptake. Plant Physiol 30:2111–2117

    Article  Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397

    Article  PubMed  CAS  Google Scholar 

  • Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd edn. Academic Press Ltd, London, San Diego

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Monni S, Uhlig C, Hansen E, Magel E (2001) Ecophysiological responses of Empetrum nigrum to heavy metal pollution. Environ Pollut 112:121–129

    Article  PubMed  CAS  Google Scholar 

  • Morina F, Jovanovic L, 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

    PubMed  CAS  Google Scholar 

  • Mortvedt JJ (2000) Bioavailability of micronutrients. In: Sumner ME (ed) Handbook of Soil Science. CRC Press, Boca Raton, pp D71–D88

    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 

  • Neumann D, Zurnieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692

    Article  PubMed  CAS  Google Scholar 

  • Neumann D, Zurnieden U, Schwieger W, Leopold I, Lichtenberger O (1997) Heavy metal tolerance of Minuartia verna. J Plant Physiol 151:101–108

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol 49:249–279

    Article  CAS  Google Scholar 

  • Pompella A, Maellaro E, Casini AF, Comporti M (1987) Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Amer J Pathol 129:295–301

    CAS  Google Scholar 

  • Powell MJ, Davies MS, Francis D (1986) The influence of zinc on the cell cycle in the root meristem of zinc tolerant and a non-tolerant cultivator of Festuca rubra L. New Phytol 102:419–428

    Article  CAS  Google Scholar 

  • Qi XT, Cui QH, Luo Y, Guo CF, Chai TY (2009) Zn stress-induced inhibition of bean PvSR2-GUS fusion gene splicing is gene-specific in transgenic tobacco. J Plant Physiol 166:1223–1227

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant Physiol 127:887–898

    Article  PubMed  Google Scholar 

  • Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35:561–565

    Article  CAS  Google Scholar 

  • Shi QH, Bao ZY, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  PubMed  CAS  Google Scholar 

  • Song AL, Li ZJ, Zhang J, Xue GF, Fan FL, Liang YC (2009) Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J Hazard Mater 172:74–83

    Article  PubMed  CAS  Google Scholar 

  • Straczek A, Sarret G, Manceau A, Hinsinger P, Geoffroy N, Jaillard B (2008) Zinc distribution and speciation in roots of various genotypes of tobacco exposed to Zn. Environ Exp Bot 63:80–90

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wallace A (1992) Participation of silicon in cation-anion balance as a possible mechanism for aluminum and iron tolerance in some Gramineae. J Plant Nutr 15:1345–1351

    Article  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  PubMed  CAS  Google Scholar 

  • Weckx JEJ, Clijsters HMM (1997) Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 35:405–410

    CAS  Google Scholar 

  • Wiese H, Nikolic M, Römhel V (2007) Silicon in plant nutrition. Effect of zinc, manganese and boron leaf concentrations and compartmentation. In: Sattelmacher B, Horst WJ (eds) The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. Springer, Dordrecht, pp 33–47

    Chapter  Google Scholar 

  • Xu WH, LI WY, He J, Singh B, Xiong Z (2009) Effects of insoluble Zn, Cd, and EDTA on the growth, activities of antioxidant enzymes and uptake of Zn and Cd in Vetiveria zizanioides. J Environ Sci 21:186–192

    Article  CAS  Google Scholar 

  • Zhu ZJ, Wei GQ, Li J, Qian QQ, Yu JQ (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This research is jointly supported by Ministry of Science and Technology (2006BAD02A15), the Distinguished Talent Program from the Chinese Academy of Agricultural Sciences granted to Y. C. Liang, and the National Natural Science Foundation of China (Approved No. 40701163). M.N. thanks the Serbian Ministry of Science and Technology (Grant No. 173028).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yongchao Liang.

Additional information

Responsible Editor: Jian Feng Ma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, A., Li, P., Li, Z. et al. The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344, 319–333 (2011). https://doi.org/10.1007/s11104-011-0749-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0749-3

Keywords

Navigation