Biologia plantarum 61:741-750, 2017 | DOI: 10.1007/s10535-017-0731-x

Silicon enhances the tolerance of Poa annua to cadmium by inhibiting its absorption and oxidative stress

P. Li1,2, C. Z. Zhao1, Y. Q. Zhand1, X. M. Wang1, J. F. Wang1, F. Wang1, Y. R. Bi1,*
1 Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, P.R. China
2 State Key Laboratory of Plateau Ecology and Agriculture, Qinhai University, Xining, P.R. China

Silicon (Si) could enhance plant tolerance to heavy metals; however, the mechanism of Si-mediated alleviation of cadmium (Cd) toxicity in Poa annua was not clear. In this study, we found that 100 μM Cd significantly inhibited the growth of Poa annua seedlings. Furthermore, Cd enhanced the H2O2 and malondialdehyde content. The activities of superoxide dismutase and ascorbate peroxidase were enhanced, but the catalase and peroxidase activities were reduced by Cd treatment. Cd also altered the activity and expression of glucose-6-phosphate dehydrogenase (G6PDH) in Poa annua roots. Application of Na3PO4, an inhibitor of G6PDH, decreased the activity of G6PDH, the expression of G6PDH, and increased the Cd toxicity, suggesting that G6PDH is involved in the regulation of oxidative stress induced by Cd. Application of 1 mM Si alleviated the inhibition of Cd on the growth of Poa annua seedlings. Si application not only led to reduced oxidative injuries but also decreased the accumulation of Cd in Poa annua seedlings under Cd stress. Furthermore, Si decreased the activity of G6PDH and the expression of G6PDH under Cd stress, which demonstrated that Si attenuates the Cd toxicity in Poa annua probably through decreasing the expression of G6PDH under Cd stress. When G6PDH was inhibited, the alleviation impact of Si on Cd stress was abolished. Taken together, these results demonstrated that the Cd tolerance in Poa annua enhanced by Si is mainly due to the decrease of Cd uptake in roots and lowering the oxidative stress induced by Cd.

Keywords: ascorbate proxidase; catalase; glucose-6-phosphate dehydrogenase; malondialdehyde; Na3PO4; peroxidase; superoxide dismutase
Subjects: silicon; cadmium; ascorbate peroxidase; catalase; glucose-6-phosphate dehydrogenase; peroxidase; superoxide dismutase; malondialdehyde; chlorophyll
Species: Poa annua

Received: February 23, 2016; Revised: January 4, 2017; Accepted: January 9, 2017; Published: December 1, 2017Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Li, P., Zhao, C.Z., Zhand, Y.Q., Wang, X.M., Wang, J.F., Wang, F., & Bi, Y.R. (2017). Silicon enhances the tolerance of Poa annua to cadmium by inhibiting its absorption and oxidative stress. Biologia plantarum, 61(4), 741-750. doi: 10.1007/s10535-017-0731-x.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    References

    1. Ádám, A.L., Bestwick, C.S., Barna, B., Mansfield, J.W.: Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. - Planta 197: 240-249, 1995. Go to original source...
    2. Aebi, H.: Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
    3. Balakhnina, T.I., Matichenkov, V.V., Wlodarczyk, T., Borkowska, A., Nosalewicz, M. Fomina, I.R.: Effects of silicon on growth processes and adaptive potential of barley plants under optimal soil watering and flooding. - Plant Growth Regul. 67: 35-43, 2012. Go to original source...
    4. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    5. Dal Corso, G., Farinati, S., Furini, A.: Regulatory networks of cadmium stress in plants. - Plant Signal Behav. 5: 663-667, 2010. Go to original source...
    6. Dal Santo, S., Stampfl, H., Krasensky, J., Kempa, S., Gibon, Y., Petutschnig, E., Rozhon, W., Heuck, A., Clausen, T., Jonak, C.: Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. - Plant Cell 24: 3380-3392, 2012. Go to original source...
    7. Esposito, S., Carfagna, S., Massaro, G., Vona, V., Di, M.R.V.: Glucose-6-phosphate dehydrogenase in barley roots: kinetic properties and localization of the isoforms. - Planta 212: 627-634, 2001. Go to original source...
    8. Exley, C.: Silicon in life: a bioinorganic solution to bioorganic essentiality. - J. Inorg. Biochem. 69: 139-144, 1998. Go to original source...
    9. Feng, J.G., Shi, Q.H., Wang, X.F., Wei, M., Yang, F.J., Xu, H.N.: Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. - Sci. Hort. 123: 521-530, 2010. Go to original source...
    10. Gallego, S.M., Pena, L.B., Barcia, R.A., Azpilicueta, C.E., Iannone, M.F., Rosales, E.P., Zawoznik, M.S., Groppa, M.D., Benavides, M.P.: Unravelling cadmium toxicity and tolerance in plants: insights into regulatory mechanisms. - Environ. exp. Bot. 83: 33-46, 2012. Go to original source...
    11. Graeve, K., Von Schaewen, A., Scheibe, R.: Purification, characterization, and cDNA sequence of glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). - Plant J. 5: 353-361, 1994. Go to original source...
    12. Hodges, D.M., Delong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-711, 1999. Go to original source...
    13. Janda, T., Szalai, G., Tari, I., Páldi, E.: Hydroponic treatment with salicylic acid decreases the effects of chilling in maize (Zea mays L) plants. - Planta 208: 175-180, 1999. Go to original source...
    14. Khandekar, S., Leisner, S.: Soluble silicon modulates expression of Arabidopsis thaliana genes involved in copper stress. - J Plant Physiol. 168: 699-705, 2011. Go to original source...
    15. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. - Nature 227: 680-685, 1970. Go to original source...
    16. Li, P., Song, A., Li, Z.J., Fan, F.L., Liang, Y.C.: Silicon ameliorates manganese toxicity by regulating manganese transport and antioxidant reactions in rice (Oryza sativa L.). - Plant Soil 354: 407-419, 2012. Go to original source...
    17. Lin, Y.Z., Lin, S.Z., Guo, H., Zhang, Z.Y., Chen, X.Y.: Functional analysis of PsG6PDH, a cytosolic glucose-6-phosphate dehydrogenase from Populus suaveolens, and its contribution to cold tolerance improvement in tobacco plants. - Biotechnol. Lett. 35: 1509-1518, 2013. Go to original source...
    18. Liu, S., Yang, R., Pan, Y., Ma, M., Pan, J., Zhao, Y., Cheng, Q., Wu, M., Wang, M., Zhang, L.: Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. - Ecotoxicol. environ. Safety 119: 35-46, 2015. Go to original source...
    19. Ma, F.J., Yamaji, N.: Silicon uptake and accumulation in higher plants. - Trends Plant Sci. 11: 392-397, 2006. Go to original source...
    20. Mitani, N., Ma, J.F.: Uptake system of silicon in different plant species. - J. exp. Bot. 56: 1255-1261, 2005. Go to original source...
    21. Mittler, R., Vanderauwera, S., Gollery, M., Breusegem, F.V.: Reactive oxygen gene network of plants. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
    22. Peng, Y., Huang, B.R., Xu, L.X., Li, Z.: Heat stress effects on osmotic potential, membrane fatty acid composition and lipid peroxidation content of two Kentucky bluegrass cultivars differing in drought tolerance. - Acta horticult. sin. 40: 971-980, 2013.
    23. Porra, R.J., Thompson, W.A., Kriedman, P.A.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. - Biochim. biophys. Acta 975: 384-394, 1989. Go to original source...
    24. Prochazkova, D., Sairam, R.K., Srivastava, G.C., Singh, D.V.: Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. - Plant Sci. 161: 765-771, 2001. Go to original source...
    25. Rizwan, M., Meunier, J.D., Miche, H., Keller, C.: 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, 2011.
    26. Rodríguez-Serrano, M., Romero-Puertas, M.C., Pazmiño, D.M., Testillano, P.S., Risueño, M.C., Del Rio, L.A., Sandalio, L.M.: Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. - Plant Physiol. 150: 229-243, 2009. Go to original source...
    27. Salvemini, F., Franze, A., Iervolino, A., Filosa, S., Salzano, S., Ursini, V.: Enhanced glutathione levels and oxido resistance mediated by increased glucose-6-phosphate dehydrogenase expression. - J. biol. Chem. 274: 2750-2757, 1999. Go to original source...
    28. Scharte, J., Schön, H., Tiaden, Z., Weis, E., Von Schaewen, A.: Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. - PNAS 106: 8061-8066, 2009. Go to original source...
    29. Sharma, S.S., Dietz, K.J.: The relationship between metal toxicity and cellular redox imbalance. - Trends Plant Sci. 14: 43-50, 2009. Go to original source...
    30. Shetty, R., Jensen, B., Shetty, N.P., Hansen, M., Hansen, C.W., Starkey, K.R., Jørgensen, H.J.L.: Silicon induced resistance against powdery mildew of roses caused by Podosphaera pannosa. - Plant Pathol. 61: 120-131, 2012. Go to original source...
    31. Shi, G.R., Cai, Q.S., Liu, C.F., Wu, L.: Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. - Plant Growth Regul. 61: 45-52, 2010. Go to original source...
    32. Slaski, J.J., Zhang, G.C., Basu, U., Stephens, J.L., Taylor, G.J.: Aluminum resistance in wheat (Triticum aestivum) is associated with rapid, Al-induced changes in activities of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in root apices. - Physiol. Plant. 98: 477-484, 1996. Go to original source...
    33. Song, A., Li, P., Li, Z.J., Fan, F.L., Nikolic, M., Liang, Y.C.: The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. - Plant Soil 344: 319-333, 2011. Go to original source...
    34. Sun, Y.B., Zhou, Q.X., Wang, L., Liu, W.T.: The influence of different growth stages and dosage of EDTA on Cd uptake and accumulation in Cd hyperaccumulator (Solanum nigrum L.). - Bull. Environ. Contam. Toxicol. 82: 348-353, 2009. Go to original source...
    35. Tian, W.N., Braunstein, L.D., Pang, J., Stuhlmeier, K.M., Xi, Q.C., Tian, X., Stanton, R.C.: Importance of glucose-6-phosphate dehydrogenase activity for cell growth. - J. biol. Chem. 273: 10609-10617, 1998. Go to original source...
    36. Vaculík, M., Landberg, T., Greger, M., Luxová, M., Stoláriková, M., Lux, A.: Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. - Ann. Bot. 110: 433-443, 2012. Go to original source...
    37. Van Assche, F., Cardinaels, C., Clijsters, H.: Induction of enzyme capacity in plants as a result of heavy metal toxicity: dose-response relations in Phaseolus vulgaris L., treated with zinc and cadmium. - Environ. Pollut. 52: 103-115, 1988. Go to original source...
    38. Veljovic-Jovanovic, S.D., Noctor, G., Foyer, C.H.: Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. - Plant Physiol. Biochem. 40: 501-507, 2002. Go to original source...
    39. Wang, H.H., Yang, L.D., Li, Y., Hou, J.J., Huang, J.J., Liang, W.H.: Involvement of ABA- and H2O2-dependent cytosolic glucose-6-phosphate dehydrogenase in maintaining redox homeostasis in soybean roots under drought stress. - Plant Physiol. Biochem. 107: 126-136, 2016. Go to original source...
    40. Wang, M., Zou, J.H., Duan, X.C., Jiang, W.S., Liu, D.H.: Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). - Bioresour. Technol. 98: 82-88, 2007. Go to original source...
    41. Wang, X.M., Ma, Y.Y., Huang, C.H., Wan, Q., Li, N., Bi, Y.R.: Glucose-6-phosphate dehydrogenase plays a central role in modulating reduced glutathione levels in reed callus under salt stress. - Planta 227: 611-623, 2008a. Go to original source...
    42. Wang, Z., Zhang, Y.X., Huang, Z.B., Huang, L.: Antioxidative response of metal accumulator and non-accumulator plants under cadmium stress. - Plant Soil 310: 137-149, 2008b. Go to original source...
    43. Weber, M., Trampczynska, A., Clemens, S.: Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. - Plant Cell Environ. 29: 950-963, 2006. Go to original source...
    44. Yan, H., Filardo, F., Hu, X., Zhao, X., Fu, D.: Cadmium stress alters the redox reaction and hormone balance in oilseed rape (Brassica napus L.) leaves. - Environ. Sci. Pollut. Res. Int. 23: 3758-69, 2016. Go to original source...
    45. Yang, Y.T., Fu, Z.W., Su, Y.C., Zhang, X., Li, G.Y., Guo, J.L., Que, Y.X., Xu, L.P.: A cytosolic glucose-6-phosphate dehydrogenase gene, ScG6PDH, plays a positive role in response to various abiotic stresses in sugarcane. - Sci. Rep. 4: 7090, 2014.
    46. Zhang, C.C., Wang, L.J., Nie, Q., Zhang, W.X., Zhang, F.S.: Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). - Environ. exp. Bot. 62: 300-307, 2008. Go to original source...
    47. Zhang, F.Q., Zhang, H.X., Wang, G.P., Xu, L.L., Shen, Z.G.: Cadmium-induced accumulation of hydrogen peroxide in the leaf apoplast of Phaseolus aureus and Vicia sativa and the roles of different antioxidant enzymes. - J. Hazard Mater. 168: 76-84, 2009. Go to original source...
    48. Zhang, L., Liu, J., Wang, X.M., Bi, Y.R.: Glucose-6-phosphate dehydrogenase acts as a regulator of cell redox balance in rice suspension cells under salt stress. - Plant Growth Regul. 69: 139-148, 2013. Go to original source...
    49. Zhao, C.Z, Li, P., Wang, X.M., Li, P., Wang, X.Y., Wang, F., Wang, J.F., Chang, N., Bi Y.R.: Nitrogen deprivation induces cross-tolerance of Poa annua callus to salt stress. - Biol. Plant. 60: 543-554, 2016. Go to original source...
    50. Zhao, L.Q., Zhang, F., Guo, J.K., Yang, Y.L., Li, B.B., Zhang, L.X.: Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. - Plant Physiol. 134: 849-857, 2004. Go to original source...

    Return to the content