Distinct physiological responses of tomato and cucumber plants in silicon-mediated alleviation of cadmium stress

Frontiers in Plant Science

Volumn 6, Issue June, 2015, Pages

  Wu, Jiawen ^a   Guo, Jia ^a   Hu, Yanhong ^a   Gong, Haijun ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Antioxidant defense; Cadmium; Cd transport; Cell wall polysaccharide; Organic acid; Silicon

Indexed keywords

CUCUMIS SATIVUS; LYCOPERSICON ESCULENTUM;

EID: 84935889138     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00453     Document Type: Article

References (70)

1. Aery, N. C., and Rana, D. K. (2003). Growth and cadmium uptake in barley under cadmium stress. J. Environ. Biol. 24, 117-123.
2. Ali, B., Huang, C.R., Qi, Z.Y., Ali, S., Daud ,M.K., Geng, X.X., etal. (2013). 5-Aminolevulinic acid ameliorates cadmium-inducedmorphological, biochemical, and ultra structural changes in seedlings of oilseed rape. Environ. Sci. Pollutn. Res. 20, 7256–7267. doi:10.1007/s11356-013-1735-5.
3. Ali, B., Qian, P., Jin, R., Ali, S., Khan, M., Aziz, R., et al. (2014). Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol. Plantarum 58, 131-138.
4. Alvarez-Fernandez, A., Diaz-Benito, P., Abadia, A., Lopez-Millan, A.-F., and Abadia, J. (2014). Metal species involved in long distance metal transport in plants. Front. Plant Sci. 5:105. doi: 10.3389/fpls.2014.00105.
5. Arakawa, N., Tsutsumi, K., Sanceda, N. G., Kurata, T., and Inagaki, C. (1981). A rapid and sensitive method for the determination of ascorbic acid using 4,7-diphenyl-l,10-phenanthroline. Agric. Biol. Chem. 45, 1289-1290. doi: 10.1271/bbb1961.45.1289.
6. Balakhnina, T., and Borkowska, A. (2013). Effects of silicon on plant resistance to environmental stresses: Review. Int. Agrophys. 27, 225-232. doi: 10.2478/v10247-012-0089-4.
7. Bityutskii, N., Pavlovic, J., Yakkonen, K. ,Maksimovic, V., and Nikolic, M. (2014).Contrasting effect of silicon on iron,zinc and manganese status and accumulation of metal-mobilizing compounds in micronutrient-deficient cucumber. Plant Physiol. Biochem. 74, 205–211.doi: 10.1016/j.plaphy.2013.11.015.
8. Boominathan, R., and Doran, P. M. (2003). Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J. Biotechnol. 101, 131-146. doi: 10.1016/S0168-1656(02)00320-6.
9. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72, 248-254. doi: 10.1016/0003-2697(76) 90527-3.
10. Chen, G., Liu, Y., Wang, R., Zhang, J., and Owens, G. (2013). Cadmium adsorption bywillowroot: The role ofcell walls and their subfractions. Environ. Sci. Pollut. Res. 20, 5665-5672. doi: 10.1007/s11356-013-1506-3.
11. Cooke, J., and Leishman, M. R. (2011). Is plant ecology more siliceous than we realise? Trends Plant Sci. 16, 61-68. doi: 10.1016/j.tplants.2010.10.003.
12. da Cunha, K. P. V., and do Nascimento, C. W. A. (2009). Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Poll. 197, 323-330. doi: 10.1007/s11270-008-9814-9.
13. Dai, W., Zhang, K., Duan, B., Sun, C., Zheng, K., Cai, R., et al. (2005). Rapid determination ofsilicon content in rice. Rice Sci. 12, 145-147.
14. Dhindsa, R. S., Plumb-Dhindsa, P., and Thorpe, T. A. (1981). Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels ofsuperoxide dismutase and catalase. J. Exp. Bot. 32,93-101. doi: 10.1093/jxb/32.1.93.
15. Dragisic Maksimovic, J., Mojovic, M., Maksimovic, V., Romheld, V., and Nikolic, M. (2012). Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J. Exp. Bot. 63, 2411-2420. doi: 10.1093/jxb/err359.
16. Epstein, E. (1999).Silicon.Annu. Rev. Plan.tPhysiol. PlantMol. Biol. 50, 641-664. doi: 10.1146/annurev.arplant.50.1.641.
17. Farooq, M. A., Ali, S., Hameed, A., Ishaque, W., Mahmood, K., and Iqbal, Z. (2013). Alleviationofcadmiumtoxicitybysiliconis relatedto elevatedphotosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol. Environ. Saf. 96, 242-249. doi: 10.1016/j.ecoenv.2013.07.006.
18. Feng, J., Shi, Q., Wang, X., Wei, M., Yang, F., and Xu, H. (2010). Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci. Hortic. 123, 521-530. doi: 10.1016/j.scienta.2009.10.013.
19. Fryer, M. J., Oxborough, K., Mullineaux, P. M., and Baker, N. R. (2002). Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53, 1249-1254. doi: 10.1093/jexbot/53.372.1249.
20. Gonęalves, J. F., Becker, A. G., Cargnelutti, D., Tabaldi, L. A., Pereira, L. B., Battisti, V., et al. (2007). Cadmium toxicity causes oxidative stress and induces responseoftheantioxidantsystemincucumberseedlings. Braz.J. PlantPhysiol. 19,223-232. doi: 10.1590/S1677-04202007000300006.
21. Gong, H. J., Randall, D. P., and Flowers, T. J. (2006). Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant CellEnviron. 29, 1970-1979. doi: 10.1111/j.1365-3040.2006.01572.x.
22. Guri, A. (1983). Variation in glutathione and ascorbic acid content among selected cultivarsofphaseolusvulgarispriortoandafterexposuretoozone. Can.J.Plant Sci. 63, 733-737. doi: 10.4141/cjps83-090.
23. Han, F., Shan, X., Zhang, S., Wen, B., and Owens, G. (2006). Enhanced cadmium accumulation in maize roots—the impact of organic acids. Plant Soil 289, 355-368. doi: 10.1007/s11104-006-9145-9.
24. Heath, R. L., and Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125,189-198. doi: 10.1016/0003-9861(68)90654-1.
25. Heine, G., Tikum, G., and Horst, W. J. (2005). Silicon nutrition oftomato and bitter gourd with special emphasis on silicon distribution in root fractions. J. Plant Nutr. SoilSc. 168,600-606. doi: 10.1002/jpln.200420508.
26. Katz, O. (2014). Beyond grasses: the potential benefits of studying silicon accumulation in non-grass species. Front. Plant Sci. 5:376. doi: 10.3389/fpls.2014.00376.
27. Kramer, U., Pickering, I. J., Prince, R. C., Raskin, I., and Salt, D. E. (2000). Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol. 122, 1343-1353. doi: 10.1104/pp.122.4.1343.
28. Krzeslowska, M. (2011). The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol. Plant 33, 35-51. doi: 10.1007/s11738-010-0581-z.
29. Kupper, H., Mijovilovich, A., Meyer-Klaucke, W., and Kroneck, P. M. (2004). Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by x-ray absorption spectroscopy. Plant Physiol. 134, 748-757. doi: 10.1104/pp.103.032953.
30. Liang, Y., Sun, W., Zhu, Y. G., and Christie, P. (2007). Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: A review. Environ. Pollut. 147,422-428. doi: 10.1016/j.envpol.2006.06.008.
31. Liang, Y., Wong, J. W., and Wei, L. (2005). Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58, 475-483. doi: 10.1016/j.chemosphere.2004.09.034.
32. Liu, J., Ma, J., He, C., Li, X., Zhang, W., Xu, F., et al.(2013a).Inhibitionofcadmium ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon. New Phytol. 200, 691-699. doi: 10.1111/nph.12494.
33. Liu, J., Zhang, H., Zhang, Y., and Chai, T. (2013b). Silicon attenuates cadmium toxicity in Solanum nigrum L. by reducing cadmium uptake and oxidative stress. PlantPhysiol. Biochem. 68, 1-7. doi: 10.1016/j.plaphy.2013.03.018.
34. López-Millan, A. F., Sagardoy, R., Solanas, M., Abadia, A., and Abadia, J. (2009). Cadmium toxicity in tomato (Lycopersicon esculentum L.) plantsgrowninhydroponics. Environ. Exp. Bot. 65, 376-385. doi: 10.1016/j.envexpbot.2008.11.010.
35. Lu, L. L., Tian, S. K., Yang, X. E., Peng, H. Y., and Li, T. Q. (2013). Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. J. Zhejiang Univ. Sci. B 14, 106-114. doi: 10.1631/jzus.B1200211.
36. Lukacova Kulikova, Z., and Lux, A. (2010). Silicon influence on maize, Zea mays L., hybrids exposed to cadmium treatment. Bull. Environ. Contam. Toxicol. 85, 243-250. doi: 10.1007/s00128-010-0046-5.
37. Lukacova, Z., Svubova, R., Kohanova, J., and Lux, A. (2013). Silicon mitigates the Cd toxicity in maize in relation to cadmium translocation, cell distribution, antioxidant enzymes stimulation and enhanced endodermal apoplasmic barrier development. PlantGrowth Regul. 70, 89-103. doi: 10.1007/s10725-012-9781-4.
38. Ma, J., Cai, H., He, C., Zhang, W., and Wang, L. (2015). Ahemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol. 206, 1063-1074. doi: 10.1111/nph.13276.
39. Ma, J. F., and Yamaji, N. (2008). Functions and transport of silicon in plants. Cell Mol. Life Sci. 65, 3049-3057. doi: 10.1007/s00018-008-7580-x.
40. Mitani, N., and Ma, J. F. (2005). Uptake system of silicon in different plant species. J. Exp. Bot. 56,1255-1261. doi: 10.1093/jxb/eri121.
41. Naeem, A., Saifullah, U., Ghafoor, A., and Farooq, M. (2014). Suppression of cadmium concentration in wheat grains by silicon is related to its application rate and cadmium accumulating abilities of cultivars. J. Sci. Food Agric. doi: 10.1002/jsfa.6976 [Epub ahead of print].
42. Nakano, Y., and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22, 867-880.
43. Nigam, R., Srivastava, S., Prakash, S., and Srivastava, M.M. (2000). Effect of organic acids on the availability of cadmium in wheat. Chem. Spec. Bioavailab. 12, 125-132. doi: 10.3184/095422900782775481.
44. Nwugo, C. C., and Huerta, A. J. (2008). Effects of silicon nutrition on cadmium uptake, growth and photosynthesis ofrice plants exposed to low-levelcadmium. PlantSoil 311, 73-86. doi: 10.1007/s11104-008-9659-4.
45. Nwugo, C. C., and Huerta, A. J. (2011). The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmium-stress. J. Proteome Res. 10, 518-528. doi: 10.1021/pr100716h.
46. Pavlovic, J., Samardzic, J., Maksimovic, V., Timotijevic, G., Stevic, N., Laursen, K. H., et al. (2013). Silicon alleviates iron deficiency in cucumber by promoting mobilization of iron in the root apoplast. New Phytol. 198, 1096-1107. doi: 10.1111/nph.12213.
47. Regvar, M., Eichert, D., Kaulich, B., Gianoncelli, A., Pongrac, P., and Vogel-Mikus, K. (2013). Biochemical characterization of cell types within leaves of metal-hyperaccumulating Noccaea praecox (Brassicaceae). Plant Soil 373, 157-171. doi: 10.1007/s11104-013-1768-z.
48. Rennenberg, H. (1980). Glutathione metabolism and possible biological roles in higher plants. Phytochemistry 21, 2771-2781. doi: 10.1016/0031-9422(80)85045-X.
49. Rizwan, M., Meunier, J. D., Miche, H., and Keller, C. (2012). Effect of silicon on reducing cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J. Hazard Mater. 209 210, 326-334. doi: 10.1016/j.jhazmat.2012.01.033.
50. Rodriguez-Hernandez, M. D., Moreno, D. A., Carvajal, M., and Ballesta, M. D. M. (2013). Interactive effects of boron and NaCl stress on water and nutrient transport in two broccoli cultivars. Funct. Plant Biol. 40, 739-748. doi: 10.1071/FP12314.
51. Rogalla, H., and Romheld, V. (2002). Role of leaf apoplast in silicon-mediated manganesetoleranceofCucumissativusL. Plant Cell Environ. 25,549-555. doi: 10.1046/j.1365-3040.2002.00835.x.
52. Salt, D. E., Prince, R. C., Pickering, I. J., and Raskin, I. (1995). Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 109, 1427-1433.
53. Senden, M. H. M. N., van der Meer, A. J. G. M., Verburg, T. G., and Wolterbeek, H. T. (1995). Citric acid in tomato plant roots and its effect on cadmium uptake anddistribution. PlantSoil 171, 333-339. doi: 10.1007/BF00010289.
54. Shi, G. R., Cai, Q. S., Liu, C. F., and Wu, L. (2010). Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul. 61, 45-52. doi: 10.1007/s10725-010-9447-z.
55. Shi, X. H., Zhang, C. C., Wang, H., and Zhang, F. S. (2005). Effect of Si on the distribution of Cd in rice seedlings. Plant Soil 272, 53-60. doi: 10.1007/s11104-004-3920-2.
56. Song, A., Li, Z., Zhang, J., Xue, G., Fan, F., and Liang, Y. (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. doi: 10.1016/j.jhazmat.2009.06.143.
57. Stohs, S. J., and Bagchi, D. (1995). Oxidative mechanisms in the toxicity of metal ions. Free Radical Bio. Med. 18, 321-336. doi: 10.1016/0891-5849(94) 00159-H.
58. Sun, R., Zhou, Q., and Wei, S. (2011). Cadmium accumulation in relation to organic acids and nonprotein thiols in leaves of the recently found Cd hyperaccumulator Rorippa globosa and the Cd-accumulating plant Rorippa islandica. J. Plant Growth Regul. 30, 83-91. doi: 10.1007/s00344-010-9176-6.
59. Tian, S., Lu, L., Labavitch, J., Yang, X., He, Z., Hu, H., et al. (2011). Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. PlantPhysiol. 157,1914-1925. doi: 10.1104/pp.111.183947.
60. Tiryakioglu, M., Eker, S., Ozkutlu, F., Husted, S., and Cakmak, I. (2006). Antioxidant defense system and cadmium uptake in barley genotypes differing in cadmium tolerance. J. Trace Elem. Med. Biol. 20, 181-189. doi: 10.1016/j.jtemb.2005.12.004.
61. Vaculik, M., Landberg, T., Greger, M., Luxova, M., Stolarikova, M., and Lux, A. (2012). Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Ann. Bot. 110, 433-443. doi: 10.1093/aob/mcs039.
62. Vaculik, M., Lux, A., Luxova, M., Tanimoto, E., and Lichtscheidl, I. (2009). Silicon mitigates cadmium inhibitory effects in young maize plants. Environ. Exp. Bot. 67, 52-58. doi: 10.1016/j.envexpbot.2009.06.012.
63. Vatehova, Z., Kollarova, K., Zelko, I., Richterova-Kucerova, D., Bujdoś, M., and Liskova, D. (2012). Interaction of silicon and cadmium in Brassica juncea and Brassica napus. Biologia 67, 498-504. doi: 10.2478/s11756-012-0034-9.
64. Velikova, V., Yordanov, I., and 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. doi: 10.1016/S0168-9452(99)00197-1.
65. Wu, J. W., Shi, Y., Zhu, Y. X., Wang, Y. C., and Gong, H. J. (2013). Mechanisms ofenhanced heavymetal tolerance in plants bysilicon: A review. Pedosphere 23, 815-825. doi: 10.1016/S1002-0160(13)60073-9.
66. Xu, J., Zhu, Y. Y., Ge, Q., Li, Y. L., Sun, J. H., Zhang, Y., et al. (2012). Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. New Phytol. 196, 125-138. doi: 10.1111/j.1469-8137.2012. 04236.x.
67. Yang, J. L., Zhu, X. F., Peng, Y. X., Zheng, C., Li, G. X., Liu, Y., et al. (2011). Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol. 155, 1885-1892. doi: 10.1104/pp.111.172221.
68. Zhang, H., Xia, Y., Wang, G., and Shen, Z. (2008). Excess copper induces accumulation of hydrogen peroxide and increases lipid peroxidation and total activity of copper-zinc superoxide dismutase in roots of Elsholtzia haichowensis. Planta 227, 465-475. doi: 10.1007/s00425-007-0632-x.
69. Zheng, S. J., Lin, X. Y., Yang, J. L., Liu, Q., and Tang, C. X. (2004). The kinetics of aluminum adsorption and desorption by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant Soil 261, 85-90. doi: 10.1023/B:PLSO.0000035576.71760.2b.
70. Zhong, H., and Lauchli, A. (1993). Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J. Exp. Bot. 44, 773-778. doi: 10.1093/jxb/44.4.773.