The role of silicon in higher plants under salinity and drought stress

Frontiers in Plant Science

Volumn 7, Issue 2016JULY, 2016, Pages

  Coskun, Devrim ^a   Britto, Dev T ^a   Huynh, Wayne Q ^a   Kronzucker, Herbert J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Apoplast; Drought stress; Ion transport; Osmotic stress; Salinity stress; Silicon; Sodium toxicity; Water transport

Indexed keywords

EID: 84978757556     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01072     Document Type: Review

References (114)

1. Agarie, S. H. U., Agata, W., Kubota, F., and Kaufman, P. B. (1998). Effects of silicon on transpiration and leaf conductance in rice plants (Oryza sativa L.). Plant Prod. Sci. 1, 89–95. doi:10.1626/pps.1.89
2. Ahmad, R., Zaheer, S. H., and Ismail, S. (1992). Role of silicon in salt tolerance of wheat (Triticum aestivum L.). Plant Sci. 85, 43–50. doi:10.1016/0168-9452(92)90092-Z
3. Ahmed, M., Fayyaz Ul, H., Qadeer, U., and Aslam, M. A. (2011). Silicon application and drought tolerance mechanism of sorghum. Afr. J. Agr. Res. 6, 594–607.
4. Ahmed, M., Qadeer, U., Ahmed, Z. I., and Fayyaz-Ul, H. (2016). Improvement of wheat (Triticum aestivum) drought tolerance by seed priming with silicon. Arch. Acker Pflanzenbau Bodenkd. 62, 299–315.
5. Al-Aghabary, K., Zhu, Z., and Shi, Q. H. (2004). Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J. Plant Nutr. 27, 2101–2115. doi:10.1081/PLN-200034641
6. Alcazar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., et al. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237–1249. doi:10.1007/s00425-010-1130-0
7. Arnon, D. I., and Stout, P. R. (1939). The essentiality of certain elements in minute quantity for plants, with special reference to copper. Plant Physiol. 14, 371–375. doi:10.1104/pp.14.2.371
8. Azeem, M., Iqbal, N., Kausar, S., Javed, M. T., Akram, M. S., and Sajid, M. A. (2015). Effcacy of silicon priming and fertigation to modulate seedling’s vigor and ion homeostasis in wheat (Triticum aestivum L.) under saline environment. Environ. Sci. Pollut. Res. Int. 22, 14367–14371. doi:10.1007/s11356-015-4983-8
9. Boyer, J. S. (1982). Plant productivity and environment. Science 218, 443–448. doi:10.1126/science.218.4571.443
10. Brunings, A. M., Datnoff, L. E., Ma, J. F., Mitani, N., Nagamura, Y., Rathinasabapathi, B., et al. (2009). Differential gene expression of rice in response to silicon and rice blast fungus Magnaporthe oryzae. Ann. Appl. Biol. 155, 161–170. doi:10.1111/j.1744-7348.2009.00347.x
11. Chain, F., Côté-Beaulieu, C., Belzile, F., Menzies, J. G., and Bélanger, R. R. (2009). A comprehensive transcriptomic analysis of the effect of silicon on wheat plants under control and pathogen stress conditions. Mol. Plant Microbe Interact. 22, 1323–1330. doi:10.1094/MPMI-22-11-1323
12. Chen, W., Yao, X., Cai, K., and Chen, J. (2011). Silicon alleviates drought stress of rice plants by improving plant water status, photosynthesis and mineral nutrient absorption. Biol. Trace Elem. Res. 142, 67–76. doi:10.1007/s12011-010-8742-x
13. Conrath, U. (2011). Molecular aspects of defence priming. Trends Plant Sci. 16, 524–531. doi:10.1016/j.tplants.2011.06.004
14. 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
15. Coskun, D., Britto, D. T., Hamam, A. M., and Kronzucker, H. J. (2014). Measuring fluxes of mineral nutrients and toxicants in plants with radioactive tracers. J. Vis. Exp. 90:e51877. doi:10.3791/51877
16. Coskun, D., Britto, D. T., Jean, Y.-K., Kabir, I., Tolay, I., Torun, A. A., et al. (2013a). KC effux and retention in response to NaCl stress do not predict salt tolerance in contrasting genotypes of rice (Oryza sativa L.). PLoS ONE 8:e57767. doi:10.1371/journal.pone.0057767
17. Coskun, D., Britto, D. T., Jean, Y. K., Schulze, L. M., Becker, A., and Kronzucker, H. J. (2012). Silver ions disrupt KC homeostasis and cellular integrity in intact barley (Hordeum vulgare L.) roots. J. Exp. Bot. 63, 151–162. doi:10.1093/jxb/err267
18. Coskun, D., Britto, D. T., Li, M., Oh, S., and Kronzucker, H. J. (2013b). Capacity and plasticity of potassium channels and high-affnity transporters in roots of barley and Arabidopsis. Plant Physiol. 162, 496–511. doi:10.1104/pp.113.215913
19. Detmann, K., Araújo, W., Martins, S., Fernie, A. R., and DaMatta, F. (2013). Metabolic alterations triggered by silicon nutrition: is there a signaling role for silicon? Plant Signal. Behav. 8:e22523. doi:10.4161/psb.22523
20. Detmann, K. C., Araújo, W. L., Martins, S. C., Sanglard, L. M., Reis, J. V., Detmann, E., et al. (2012). Silicon nutrition increases grain yield, which, in turn, exerts a feed-forward stimulation of photosynthetic rates via enhanced mesophyll conductance and alters primary metabolism in rice. New Phytol. 196, 752–762. doi:10.1111/j.1469-8137.2012.04299.x
21. Dolan, L., and Davies, J. (2004). Cell expansion in roots. Curr. Opin. Plant Biol. 7, 33–39. doi:10.1016/j.pbi.2003.11.006
22. Eneji, A. E., Inanaga, S., Muranaka, S., Li, J., Hattori, T., An, P., et al. (2008). Growth and nutrient use in four grasses under drought stress as mediated by silicon fertilizers. J. Plant Nutr. 31, 355–365. doi:10.1080/01904160801894913
23. Epstein, E. (1994). The anomaly of silicon in plant biology. Proc. Natl. Acad. Sci. U.S.A. 91, 11–17. doi:10.1073/pnas.91.1.11
24. Epstein, E. (1999). Silicon. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50, 641–664. doi:10.1146/annurev.arplant.50.1.641
25. Epstein, E. (2009). Silicon: its manifold roles in plants. Ann. Appl. Biol. 155, 155–160. doi:10.1111/j.1744-7348.2009.00343.x
26. Epstein, E., and Bloom, A. J. (2005). Mineral Nutrition of Plants: Principles and Perspectives, 2nd Edn. Sunderland: Sinauer Associates Inc.
27. Exley, C. (2015). A possible mechanism of biological silicification in plants. Front. Plant Sci. 6:853. doi:10.3389/fpls.2015.00853
28. Fadzilla, N. M., Finch, R. P., and Burdon, R. H. (1997). Salinity, oxidative stress and antioxidant responses in shoot cultures of rice. J. Exp. Bot. 48, 325–331. doi:10.1093/jxb/48.2.325
29. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., and Basra, S. M. A. (2009). Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185–212. doi:10.1051/agro:2008021
30. Fauteux, F., Chain, F., Belzile, F., Menzies, J. G., and Bélanger, R. R. (2006). The protective role of silicon in the Arabidopsis-powdery mildew pathosystem. Proc. Natl. Acad. Sci. U.S.A. 103, 17554–17559. doi:10.1073/pnas.0606330103
31. Fauteux, F., Rémus-Borel, W., Menzies, J. G., and Bélanger, R. R. (2005). Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol. Letts. 249, 1–6. doi:10.1016/j.femsle.2005.06.034
32. Fleck, A. T., Nye, T., Repenning, C., Stahl, F., Zahn, M., and Schenk, M. K. (2011). Silicon enhances suberization and lignification in roots of rice (Oryza sativa). J. Exp. Bot. 62, 2001–2011. doi:10.1093/jxb/erq392
33. Fleck, A. T., Schulze, S., Hinrichs, M., Specht, A., Wassmann, F., Schreiber, L., et al. (2015). Silicon promotes exodermal Casparian band formation in Si-accumulating and Si-excluding species by forming phenol complexes. PLoS ONE 10:e0138555. doi:10.1371/journal.pone.0138555
34. Flowers, T. J. (2004). Improving crop salt tolerance. J. Exp. Bot. 55, 307–319. doi:10.1093/jxb/erh003
35. Flowers, T. J., Hajibagheri, M. A., and Yeo, A. R. (1991). Ion accumulation in the cell walls of rice plants growing under saline conditions – Evidence for the Oertli hypothesis. Plant Cell Environ. 14, 319–325. doi:10.1111/j.1365-3040.1991.tb01507.x
36. Gao, X., Zou, C., Wang, L., and Zhang, F. (2006). Silicon decreases transpiration rate and conductance from stomata of maize plants. J. Plant Nutr. 29, 1637–1647. doi:10.1080/01904160600851494
37. Gao, X. P., Zou, C. Q., Wang, L. J., and Zhang, F. S. (2004). Silicon emproves water use effciency in maize plants. J. Plant Nutr. 27, 1457–1470. doi:10.1081/PLN-200025865
38. Gattullo, C. E., Allegretta, I., Medici, L., Fijan, R., Pii, Y., Cesco, S., et al. (2016). Silicon dynamics in the rhizosphere: connections with iron mobilization. J. Plant Nutr. Soil Sci. 179, 409–417. doi:10.1002/jpln.201500535
39. Gill, S. S., and Tuteja, N. (2010a). Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 5, 26–33. doi:10.4161/psb.5.1.10291
40. Gill, S. S., and Tuteja, N. (2010b). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. doi:10.1016/j.plaphy.2010.08.016
41. 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 Cell Environ. 29, 1970–1979. doi:10.1111/j.1365-3040.2006.01572.x
42. Gong, H. J., Zhu, X. Y., Chen, K. M., Wang, S. M., and Zhang, C. L. (2005). Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci. 169, 313–321. doi:10.1016/j.plantsci.2005.02.023
43. Guerriero, G., Hausman, J.-F., and Legay, S. (2016). Silicon and the plant extracellular matrix. Front. Plant Sci. 7:463. doi:10.3389/fpls.2016.00463
44. Guntzer, F., Keller, C., and Meunier, J.-D. (2012). Benefits of plant silicon for crops: a review. Agron. Sustain. Dev. 32, 201–213. doi:10.1007/s13593-011-0039-8
45. Hamam, A. M., Britto, D. T., Flam-Shepherd, R., and Kronzucker, H. J. (2016). Measurement of differential NaC effux from apical and bulk root zones of intact barley and Arabidopsis plants. Front. Plant Sci. 7:272. doi:10.3389/fpls.2016.00272
46. Hameed, A., Sheikh, M. A., Jamil, A., and Basra, S. M. A. (2013). Seed priming with sodium silicate enhances seed germination and seedling growth in wheat (Triticum aestivum L.) under water deficit stress induced by polyethylene glycol. Pak. J. Life Soc. Sci. 11, 19–24.
47. Hattori, T., Inanaga, S., Araki, H., An, P., Morita, S., Luxova, M., et al. (2005). Application of silicon enhanced drought tolerance in Sorghum bicolor. Physiol. Plant. 123, 459–466. doi:10.1111/j.1399-3054.2005.00481.x
48. Hattori, T., Sonobe, K., Araki, H., Inanaga, S., An, P., and Morita, S. (2008). Silicon application by sorghum through the alleviation of stress-induced increase in hydraulic resistance. J. Plant Nutr. 31, 1482–1495. doi:10.1080/01904160802208477
49. Haynes, R. J. (2014). A contemporary overview of silicon availability in agricultural soils. J. Plant Nutr. Soil Sci. 177, 831–844. doi:10.1002/jpln.201400202
50. He, C., Ma, J., and Wang, L. (2015). A hemicellulose-bound form of silicon with potential to improve the mechanical properties and regeneration of the cell wall of rice. New Phytol. 206, 1051–1062. doi:10.1111/nph.13282
51. He, C., Wang, L., Liu, J., Liu, X., Li, X., Ma, J., et al. (2013). Evidence for ’silicon’ within the cell walls of suspension-cultured rice cells. New Phytol. 200, 700–709. doi:10.1111/nph.12401
52. Hernandez, J. A., Corpas, F. J., Gomez, M., Delrio, L. A., and Sevilla, F. (1993). Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol. Plant. 89, 103–110. doi:10.1111/j.1399-3054.1993.tb01792.x
53. Hossain, K. A., Horiuchi, T., and Miyagawa, S. (2001). Effects of silicate materials on growth and grain yield of rice plants grown in clay loam and sandy loam soils. J. Plant Nutr. 24, 1–13. doi:10.1081/PLN-100000308
54. Khoshgoftarmanesh, A. H., Khodarahmi, S., and Haghighi, M. (2014). Effect of silicon nutrition on lipid peroxidation and antioxidant response of cucumber plants exposed to salinity stress. Arch. Agron. Soil Sci. 60, 639–653. doi:10.1080/03650340.2013.822487
55. Krishnamurthy, P., Ranathunge, K., Nayak, S., Schreiber, L., and Mathew, M. K. (2011). Root apoplastic barriers block NaC transport to shoots in rice (Oryza sativa L.). J. Exp. Bot. 62, 4215–4228. doi:10.1093/jxb/err135
56. Kronzucker, H. J., and Britto, D. T. (2011). Sodium transport in plants: a critical review. New Phytol. 189, 54–81. doi:10.1111/j.1469-8137.2010.03540.x
57. Kronzucker, H. J., Coskun, D., Schulze, L. M., Wong, J. R., and Britto, D. T. (2013). Sodium as nutrient and toxicant. Plant Soil 369, 1–23. doi:10.1007/s11104-013-1801-2
58. Kusano, T., Berberich, T., Tateda, C., and Takahashi, Y. (2008). Polyamines: essential factors for growth and survival. Planta 228, 367–381. doi:10.1007/s00425-008-0772-7
59. Latef, A. A. A., and Tran, L.-S. P. (2016). Impacts of priming with silicon on the growth and tolerance of maize plants to alkaline stress. Front. Plant Sci. 7:243. doi:10.3389/fpls.2016.00243
60. Liang, Y., Nikolic, M., Bélanger, R., Gong, H., and Song, A. (2015). Silicon in Agriculture. Dordrecht: Springer.
61. 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
62. Liang, Y., Zhang, W., Chen, Q., Liu, Y., and Ding, R. (2006). Effect of exogenous silicon (Si) on HC-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ. Exp. Bot. 57, 212–219. doi:10.1016/j.envexpbot.2005.05.012
63. Liang, Y. C. (1999). Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant Soil 209, 217–224. doi:10.1023/A:1004526604913
64. Liang, Y. C., Chen, Q., Liu, Q., Zhang, W. H., and Ding, R. X. (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. doi:10.1078/0176-1617-01065
65. Liang, Y. C., Zhang, W. H., Chen, Q., and Ding, R. X. (2005). Effects of silicon on HC-ATPase and HC-PPase activity, fatty acid composition and fluidity of tonoplast vesicles from roots of salt-stressed barley (Hordeum vulgare L.). Environ. Exp. Bot. 53, 29–37. doi:10.1016/j.envexpbot.2004.02.010
66. Liu, P., Yin, L., Deng, X., Wang, S., Tanaka, K., and Zhang, S. (2014). Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J. Exp. Bot. 65, 4747–4756. doi:10.1093/jxb/eru220
67. Liu, P., Yin, L., Wang, S., Zhang, M., Deng, X., Zhang, S., et al. (2015). Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress in Sorghum bicolor L. Environ. Exp. Bot. 111, 42–51. doi:10.1093/jxb/eru220
68. Lux, A., Luxova, M., Abe, J., Tanimoto, E., Hattori, T., and Inanaga, S. (2003). The dynamics of silicon deposition in the sorghum root endodermis. New Phytol. 158, 437–441. doi:10.1046/j.1469-8137.2003.00764.x
69. Ma, J., Cai, H., He, C., Zhang, W., and Wang, L. (2015). A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol. 206, 1063–1074. doi:10.1111/nph.13276
70. Ma, J. F. (2004). Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci. Plant Nutr. 50, 11–18. doi:10.1080/00380768.2004.10408447
71. Ma, J. F., and Takahashi, E. (1993). Interaction between calcium and silicon in water-cultured rice plants. Plant Soil 148, 107–113. doi:10.1007/BF02185390
72. Ma, J. F., and Yamaji, N. (2006). Silicon uptake and accumulation in higher plants. Trends Plant Sci. 11, 392–397. doi:10.1016/j.tplants.2006.06.007
73. Ma, J. F., and Yamaji, N. (2015). A cooperative system of silicon transport in plants. Trends Plant Sci. 20, 435–442. doi:10.1016/j.tplants.2015.04.007
74. Malagoli, P., Britto, D. T., Schulze, L. M., and Kronzucker, H. J. (2008). Futile NaC cyling at the root plasma membrane in rice (Oryza sativa L.) – kinetics, energetics, and relation to salinity tolerance. J. Exp. Bot. 59, 4109–4117. doi:10.1093/jxb/ern249
75. Ming, D. F., Pei, Z. F., Naeem, M. S., Gong, H. J., and Zhou, W. J. (2012). Silicon alleviates PEG-induced water-deficit stress in upland rice seedlings by enhancing osmotic adjustment. J. Agron. Crop Sci. 198, 14–26. doi:10.1111/j.1439-037X.2011.00486.x
76. Moussa, H. R. (2006). Influence of exogenous application of silicon on physiological response of salt-stressed maize (Zea mays L.). Int. J. Agric. Biol. 8, 293–297.
77. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239–250. doi:10.1046/j.0016-8025.2001.00808.x
78. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681. doi:10.1146/annurev.arplant.59.032607.092911
79. 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. Prot. Res. 10, 518–528. doi:10.1021/pr100716h
80. Oertli, J. J. (1968). Extracellular salt accumulation a possible mechanism of salt injury in plants. Agrochimica 12, 461–469.
81. Pei, Z. F., Ming, D. F., Liu, D., Wan, G. L., Geng, X. X., Gong, H. J., et al. (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. doi:10.1007/s00344-009-9120-9
82. Pii, Y., Cesco, S., and Mimmo, T. (2015). Shoot ionome to predict the synergism and antagonism between nutrients as affected by substrate and physiological status. Plant Physiol. Biochem. 94, 48–56. doi:10.1016/j.plaphy.2015.05.002
83. Rengasamy, P. (2010). Soil processes affecting crop production in salt-affected soils. Funct. Plant Biol. 37, 613–620. doi:10.1071/FP09249
84. Richmond, K. E., and Sussman, M. (2003). Got silicon? The non-essential beneficial plant nutrient. Curr. Opin. Plant Biol. 6, 268–272. doi:10.1016/S1369-5266(03)00041-4
85. Rizwan, M., Ali, S., Ibrahim, M., Farid, M., Adrees, M., Bharwana, S. A., et al. (2015). Mechanisms of silicon-mediated alleviation of drought and salt stress in plants: a review. Environ. Sci. Pollut. Res. 22, 15416–15431. doi:10.1007/s11356-015-5305-x
86. Rogalla, H., and Römheld, V. (2002). Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L. Plant Cell Environ. 25, 549–555. doi:10.1046/j.1365-3040.2002.00835.x
87. Sachs, J. V. (1860). Vegetationsversuche mit ausschluss des bodens über die nährstoffe und sonstigen ernährungsbedingungen von mais, bohnen, und anderen pflanzen. Landw. Versuchsst. 2, 219–268.
88. Saqib, M., Zoerb, C., and Schubert, S. (2008). Silicon-mediated improvement in the salt resistance of wheat (Triticum aestivum) results from increased sodium exclusion and resistance to oxidative stress. Funct. Plant Biol. 35, 633–639. doi:10.1071/FP08100
89. Savant, N. K., Snyder, G. H., and Datnoff, L. E. (1997). Silicon management and sustainable rice production. Adv. Agron. 58, 151–199. doi:10.1016/S0065-2113(08)60255-2
90. Schmidhuber, J., and Tubiello, F. N. (2007). Global food security under climate change. Proc. Natl. Acad. Sci. U.S.A. 104, 19703–19708. doi:10.1073/pnas.0701976104
91. Senadheera, P., Singh, R. K., and Maathuis, F. J. M. (2009). Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. J. Exp. Bot. 60, 2553–2563. doi:10.1093/jxb/erp099
92. Shazad, M., Zörb, C., Geilfus, C. M., and Mühling, K. H. (2013). Apoplastic NaC in Vicia faba leaves rises after short-term salt stress and is remedied by silicon. J. Agron. Crop Sci. 199, 161–170. doi:10.1111/jac.12003
93. Shi, Y., Wang, Y., Flowers, T. J., and Gong, H. (2013). Silicon decreases chloride transport in rice (Oryza sativa L.) in saline conditions. J. Plant Physiol. 170, 847–853. doi:10.1016/j.jplph.2013.01.018
94. Shi, Y., Zhang, Y., Han, W., Feng, R., Hu, Y., Guo, J., et al. (2016). Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front. Plant Sci. 7:196. doi:10.3389/fpls.2016.00196
95. Sonobe, K., Hattori, T., An, P., Tsuji, W., Eneji, A. E., Kobayashi, S., et al. (2010). Effect of silicon application on sorghum root responses to water stress. J. Plant Nutr. 34, 71–82. doi:10.1080/01904167.2011.531360
96. Soylemezoglu, G., Demir, K., Inal, A., and Gunes, A. (2009). Effect of silicon on antioxidant and stomatal response of two grapevine (Vitis vinifera L.) rootstocks grown in boron toxic, saline and boron toxic-saline soil. Sci. Hortic. 123, 240–246. doi:10.1016/j.scienta.2009.09.005
97. Speer, M., and Kaiser, W. M. (1991). Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol. 97, 990–997. doi:10.1104/pp.97.3.990
98. Struyf, E., Smis, A., Van Damme, S., Garnier, J., Govers, G., Van Wesemael, B., et al. (2010). Historical land use change has lowered terrestrial silica mobilization. Nat. Commun. 1, 129. doi:10.1038/ncomms1128
99. Suzuki, S., Ma, J. F., Yamamoto, N., Hattori, T., Sakamoto, M., and Umezawa, T. (2012). Silicon deficiency promotes lignin accumulation in rice. Plant Biotechnol. 29, 391–394. doi:10.5511/plantbiotechnology.12.0416a
100. Tamai, K., and Ma, J. F. (2008). Reexamination of silicon effects on rice growth and production under field conditions using a low silicon mutant. Plant Soil 307, 21–27. doi:10.1007/s11104-008-9571-y
101. Van Bockhaven, J., De Vleesschauwer, D., and Hofte, M. (2013). Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J. Exp. Bot. 64, 1281–1293. doi:10.1093/jxb/ers329
102. van Hulten, M., Pelser, M., Van Loon, L. C., Pieterse, C. M. J., and Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 5602–5607. doi:10.1073/pnas.0510213103
103. Vandevenne, F. I., Barao, L., Ronchi, B., Govers, G., Meire, P., Kelly, E. F., et al. (2015). Silicon pools in human impacted soils of temperate zones. Glob. Biogeochem. Cycles 29, 1439–1450. doi:10.1002/2014GB005049
104. Wang, S., Liu, P., Chen, D., Yin, L., Li, H., and Deng, X. (2015). Silicon enhanced salt tolerance by improving the root water uptake and decreasing the ion toxicity in cucumber. Front. Plant Sci. 6:759. doi:10.3389/fpls.2015.00759
105. Wang, Y. X., Stass, A., and Horst, W. J. (2004). Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol. 136, 3762–3770. doi:10.1104/pp.104.045005
106. Watanabe, S., Shimoi, E., Ohkama, N., Hayashi, H., Yoneyama, T., Yazaki, J., et al. (2004). Identification of several rice genes regulated by Si nutrition. Soil Sci. Plant Nutr. 50, 1273–1276. doi:10.1080/00380768.2004.10408603
107. Yeo, A. (1999). Predicting the interaction between the effects of salinity and climate change on crop plants. Sci. Hortic. 78, 159–174. doi:10.1016/S0304-4238(98)00193-9
108. Yeo, A. R., Flowers, S. A., Rao, G., Welfare, K., Senanayake, N., and Flowers, T. J. (1999). Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ. 22, 559–565. doi:10.1046/j.1365-3040.1999.00418.x
109. Yin, L., Wang, S., Tanaka, K., Fujihara, S., Itai, A., Den, X., et al. (2016). Silicon-mediated changes in polyamines participate in silicon-induced salt tolerance in Sorghum bicolor L. Plant Cell Environ. 39, 245–258. doi:10.1111/pce.12521
110. Zhao, F., Song, C.-P., He, J., and Zhu, H. (2007). Polyamines improve KC/NaC homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol. 145, 1061–1072. doi:10.1104/pp.107.105882
111. Zhu, J. K. (2001). Plant salt tolerance. Trends Plant Sci. 6, 66–71. doi:10.1016/S1360-1385(00)01838-0
112. Zhu, Y., and Gong, H. (2014). Beneficial effects of silicon on salt and drought tolerance in plants. Agron. Sustain. Dev. 34, 455–472. doi:10.1007/s13593-013-0194-1
113. Zhu, Y.-X., Xu, X.-B., Hu, Y.-H., Han, W.-H., Yin, J.-L., Li, H.-L., et al. (2015). Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus L. Plant Cell Rep. 34, 1629–1646. doi:10.1007/s00299-015-1814-9
114. Zhu, Z. J., Wei, G. Q., Li, J., Qian, Q. Q., and Yu, J. Q. (2004). Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci. 167, 527–533. doi:10.1016/j.plantsci.2004.04.020