Role of silicon on plant–pathogen interactions

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Wang, Min ^a   Gao, Limin ^a   Dong, Suyue ^a   Sun, Yuming ^a   Shen, Qirong ^a   Guo, Shiwei ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Biochemical; Defense response; Molecular; Physical; Plant pathogen interactions; Silicon

Indexed keywords

EID: 85019190511     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00701     Document Type: Review

References (157)

1. Andrade, C. C. L., Resende, R. S., Rodrigues, F., Ferraz, H. G. M., Moreira, W. R., Oliveira, J. R., et al. (2013). Silicon reduces bacterial speck development on tomato leaves. Trop. Plant Pathol. 38, 436–442. doi: 10.1590/S1982-56762013005000021
2. Araujo, L., Paschoalino, R. S., and Rodrigues, F. (2015). Microscopic aspects of silicon-mediated rice resistance to leaf scald. Phytopathology 106, 132–141. doi: 10.1094/PHYTO-04-15-0109-R
3. Belanger, R. R., Benhamou, N., and Menzies, J. G. (2003). Cytological evidence of an active role of silicon in wheat resistance to powdery mildew (Blumeria graminis f. sp tritici). Phytopathology 93, 402–412. doi: 10.1094/Phyto.2003.93. 4.402
4. Bi, Y., Tian, S. P., Guo, Y. R., Ge, Y. H., and Qin, G. Z. (2006). Sodium silicate reduces postharvest decay on Hami melons: induced resistance and fungistatic effects. Plant Dis. 90, 279–283. doi: 10.1094/pd-90-0279
5. Brecht, M. O., Datnoff, L. E., Kucharek, T. A., and Nagata, R. T. (2007). The influence of silicon on the components of resistance to gray leaf spot in St. Augustinegrass. J. Plant Nutr. 30, 1005–1021. doi: 10.1080/01904160701394287
6. Brisson, L. F., Tenhaken, R., and Lamb, C. (1994). Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6, 1703–1712. doi: 10.2307/3869902
7. 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
8. Cabot, C., Gallego, B., Martos, S., Barceló, J., and Poschenrieder, C. (2013). Signal cross talk in Arabidopsis exposed to cadmium, silicon, and Botrytis cinerea. Planta 237, 337–349. doi: 10.1007/s00425-012-1779-7
9. Cai, K., Gao, D., Luo, S., Zeng, R., Yang, J., and Zhu, X. (2008). Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiol. Plant 134, 324–333. doi: 10.1111/j.1399-3054.2008. 01140.x
10. Carré-Missio, V., Rodrigues, F. A., Schurt, D. A., Resende, R. S., Souza, N. F. A., Rezende, D. C., et al. (2014). Effect of foliar-applied potassium silicate on coffee leaf infection by Hemileia vastatrix. Ann. Appl. Biol. 164, 396–403. doi: 10.1111/aab.12109
11. Chain, F., Côté-Beaulieu, C., Belzile, F., Menzies, J., and Bélanger, 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, Y., Liu, M., Wang, L., Lin, W., Fan, X., and Cai, K. (2014). Proteomic characterization of silicon-mediated resistance against Ralstonia solanacearum in tomato. Plant Soil 387, 425–440. doi: 10.1007/s11104-014-2293-4
13. Chen, Y. Y., Lin, Y. M., Chao, T. C., Wang, J. F., Liu, A. C., Ho, F. I., et al. (2009). Virus-induced gene silencing reveals the involvement of ethylene-, salicylic acid- and mitogen-activated protein kinase-related defense pathways in the resistance of tomato to bacterial wilt. Physiol. Plant. 136, 324–335. doi: 10.1111/j.1399-3054.2009.01226.x
14. Chérif, M., Asselin, A., and Bélanger, R. (1994). Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Phytopathology 84, 236–242. doi: 10.1094/Phyto-84-236
15. Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M., and Dong, X. (2000). Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12, 2175–2190. doi: 10.1105/tpc.12.11.2175
16. Conceição, C. S., Felix, K. C. S., Mariano, R. L. R., Medeiros, E. V., and Souza, E. B. (2014). Combined effect of yeast and silicon on the control of bacterial fruit blotch in melon. Sci. Hortic. 174, 164–170. doi: 10.1016/j.scienta.2014.05.027
17. Coskun, D., Britto, D. T., Huynh, W. Q., and Kronzucker, H. J. (2016). The role of silicon in higher plants under salinity and drought stress. Front. Plant Sci. 7:1072. doi: 10.3389/Fpls.2016.01072
18. Cruz, M. F. A., Rodrigues, F., Diniz, A. P. C., Alves Moreira, M., and Barros, E. G. (2014). Soybean resistance to Phakopsora pachyrhizi as affected by acibenzolar-S-methyl, jasmonic acid and silicon. J. Phytopathol. 162, 133–136. doi: 10.1111/jph.12170
19. Dallagnol, L., Rodrigues, F., Pascholati, S., Fortunato, A., and Camargo, L. (2015). Comparison of root and foliar applications of potassium silicate in potentiating post-infection defences of melon against powdery mildew. Plant Pathol. 64, 1085–1093. doi: 10.1111/ppa.12346
20. Dallagnol, L. J., Rodrigues, F. A., Damatta, F. M., Mielli, M. V., and Pereira, S. C. (2011). Deficiency in silicon uptake affects cytological, physiological, and biochemical events in the rice-Bipolaris oryzae interaction. Phytopathology 101, 92–104. doi: 10.1094/PHYTO-04-10-0105
21. Dallagnol, L. J., Rodrigues, F. A., and Mielli, M. V. (2013). Silicon improves the emergence and sanity of rice seedlings obtained from seeds infected with Bipolaris oryzae. Trop. Plant Pathol. 38, 478–484. doi: 10.1590/S1982-56762013000600003
22. Dann, E. K., and Muir, S. (2002). Peas grown in media with elevated plant-available silicon levels have higher activities of chitinase and β-1, 3-glucanase, are less susceptible to a fungal leaf spot pathogen and accumulate more foliar silicon. Australas. Plant Pathol. 31, 9–13. doi: 10.1071/AP01047
23. Datnoff, L. E., Elmer, W. H., and Huber, D. M. (2007). Mineral Nutrition and Plant Disease. St. Paul, MN: The American Phytopathological Society.
24. De Vleesschauwer, D., Djavaheri, M., Bakker, P., and Hofte, M. (2008). Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol. 148, 1996–2012. doi: 10.1104/pp.108.127878
25. Deepak, S., Manjunath, G., Manjula, S., Niranjan-Raj, S., Geetha, N., and Shetty, H. S. (2008). Involvement of silicon in pearl millet resistance to downy mildew disease and its interplay with cell wall proline/hydroxyproline-rich glycoproteins. Australas. Plant Pathol. 37, 498–504. doi: 10.1071/AP08047
26. Devadas, S. K., Enyedi, A., and Raina, R. (2002). The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J. 30, 467–480. doi: 10.1046/j.1365-313X.2002.01300.x
27. Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., Reddy, M., and Wang, L. (2002). The phenylpropanoid pathway and plant defence-a genomics perspective. Mol. Plant Pathol. 3, 371–390. doi: 10.1046/j.1364-3703.2002.00131.x
28. Domiciano, G. P., Cacique, I. S., Chagas Freitas, C., Filippi, M. C., Damatta, F. M., Do Vale, F. X., et al. (2015). Alterations in gas exchange and oxidative metabolism in rice leaves infected by Pyricularia oryzae are attenuated by silicon. Phytopathology 105, 738–747. doi: 10.1094/PHYTO-10-14-0280-R
29. Domiciano, G. P., Rodrigues, F. A., Guerra, A. M. N., and Vale, F. X. R. (2013). Infection process of Bipolaris sorokiniana on wheat leaves is affected by silicon. Trop. Plant Pathol. 38, 258–263. doi: 10.1590/S1982-567620130050 00006
30. Domiciano, G. P., Rodrigues, F. A., Vale, F. X. R., Filha, M. S. X., Moreira, W. R., Andrade, C. C. L., et al. (2010). Wheat resistance to spot blotch potentiated by silicon. J. Phytopathol. 158, 334–343. doi: 10.1111/j.1439-0434.2009.01623.x
31. Dreher, K., and Callis, J. (2007). Ubiquitin, hormones and biotic stress in plants. Ann. Bot. 99, 787–822. doi: 10.1093/aob/mcl255
32. Durrant, W. E., and Dong, X. (2004). Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209. doi: 10.1146/annurev.phyto.42.040803.140421
33. Emadian, S. F., and Newton, R. J. (1989). Growth enhancement of loblolly pine (Pinus taeda L.) seedlings by silicon. J. Plant Physiol. 134, 98–103. doi: 10.1016/S0176-1617(89)80209-3
34. 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
35. Epstein, E. (1999). Silicon. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50, 641–664. doi: 10.1146/annurev.arplant.50.1.641
36. Epstein, E. (2001). Silicon in Plants: Facts vs Concepts. Amsterdam: Elsevier Science.
37. Fauteux, F., Chain, F., Belzile, F., Menzies, J. G., and Belanger, 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
38. Fauteux, F., Remus-Borel, W., Menzies, J. G., and Belanger, R. R. (2005). Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol. Lett. 249, 1–6. doi: 10.1016/j.femsle.2005.06.034
39. Fawe, A., Abou-Zaid, M., Menzies, J., and Bélanger, R. (1998). Silicon-mediated accumulation of flavonoid phytoalexins in cucumber. Phytopathology 88, 396–401. doi: 10.1094/PHYTO.1998.88.5.396
40. Filha, M. S. X., Rodrigues, F. A., Domiciano, G. P., Oliveira, H. V., Silveira, P. R., and Moreira, W. R. (2011). Wheat resistance to leaf blast mediated by silicon. Australas. Plant Pathol. 40, 28–38. doi: 10.1007/s13313-010-0010-1
41. Fortunato, A. A., Debona, D., Bernardeli, A. M. A., and Rodrigues, F. A. (2015). Defence-related enzymes in soybean resistance to target spot. J. Phytopathol. 163, 731–742. doi: 10.1111/jph.12370
42. Fortunato, A. A., Rodrigues, F., Baroni, J. C. P., Soares, G. C. B., Rodriguez, M. A. D., and Pereira, O. L. (2012a). Silicon suppresses Fusarium wilt development in banana plants. J. Phytopathol. 160, 674–679. doi: 10.1111/jph. 12005
43. Fortunato, A. A., Rodrigues, F., and Do Nascimento, K. J. (2012b). Physiological and biochemical aspects of the resistance of banana plants to Fusarium wilt potentiated by silicon. Phytopathology 102, 957–966. doi: 10.1094/PHYTO-02-12-0037-R
44. French-Monar, R. D., Rodrigues, F. A., Korndörfer, G. H., and Datnoff, L. E. (2010). Silicon suppresses Phytophthora blight development on bell pepper. J. Phytopathol. 158, 554–560. doi: 10.1111/j.1439-0434.2009. 01665.x
45. Garibaldi, A., Gilardi, G., Cogliati, E. E., and Gullino, M. L. (2011). Silicon and increased electrical conductivity reduce downy mildew of soilless grown lettuce. Eur. J. Plant Pathol. 132, 123–132. doi: 10.1007/s10658-011-9855-6
46. Ghanmi, D., Mcnally, D. J., Benhamou, N., Menzies, J. G., and Bélanger, R. R. (2004). Powdery mildew of Arabidopsis thaliana: a pathosystem for exploring the role of silicon in plant-microbe interactions. Physiol. Mol. Plant Pathol. 64, 189–199. doi: 10.1016/j.pmpp.2004.07.005
47. Ghareeb, H., Bozsó, Z., Ott, P. G., Repenning, C., Stahl, F., and Wydra, K. (2011). Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol. Mol. Plant Pathol. 75, 83–89. doi: 10.1016/j.pmpp.2010.11.004
48. Grant, M. R., Kazan, K., and Manners, J. M. (2013). Exploiting pathogens’ tricks of the trade for engineering of plant disease resistance: challenges and opportunities. Microb. Biotechnol. 6, 212–222. doi: 10.1111/1751-7915.12017
49. Guérin, V., Lebreton, A., Cogliati, E. E., Hartley, S. E., Belzile, F., Menzies, J. G., et al. (2014). A zoospore inoculation method with Phytophthora sojae to assess the prophylactic role of silicon on soybean cultivars. Plant Dis. 98, 1632–1638. doi: 10.1094/pdis-01-14-0102-re
50. 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
51. Guével, M. H., Menzies, J. G., and Bélanger, R. R. (2007). Effect of root and foliar applications of soluble silicon on powdery mildew control and growth of wheat plants. Eur. J. Plant Pathol. 119, 429–436. doi: 10.1007/s10658-007-9181-1
52. Guo, Y., Liu, L., Zhao, J., and Bi, Y. (2007). Use of silicon oxide and sodium silicate for controlling Trichothecium roseum postharvest rot in Chinese cantaloupe (Cucumis melo L.). Int. J. Food Sci. Techol. 42, 1012–1018. doi: 10.1111/j.1365-2621.2006.01464.x
53. Hao, Z., Wang, L., He, Y., Liang, J., and Tao, R. (2011). Expression of defense genes and activities of antioxidant enzymes in rice resistance to rice stripe virus and small brown planthopper. Plant Physiol. Biochem. 49, 744–751. doi: 10.1016/j.plaphy.2011.01.014
54. Hayasaka, T., Fujii, H., and Ishiguro, K. (2008). The role of silicon in preventing appressorial penetration by the rice blast fungus. Phytopathology 98, 1038–1044. doi: 10.1094/PHYTO-98-9-1038
55. He, C. W., Ma, J., and Wang, L. J. (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
56. Heine, G., Tikum, G., and Horst, W. J. (2007). The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd. J. Exp. Bot. 58, 569–577. doi: 10.1093/jxb/erl232
57. Huang, C.-H., Roberts, P. D., and Datnoff, L. E. (2011). Silicon suppresses Fusarium crown and root rot of tomato. J. Phytopathol. 159, 546–554. doi: 10.1111/j.1439-0434.2011.01803.x
58. Hutcheson, S. W. (1998). Current concepts of active defense in plants. Annu. Rev. Phytopathol. 36, 59–90. doi: 10.1146/annurev.phyto.36.1.59
59. Inanaga, S., Okasaka, A., and Tanaka, S. (1995). Does silicon exist in association with organic compounds in rice plant? Soil Sci. Plant Nutr. 41, 111–117. doi: 10.1080/00380768.1995.10419564
60. Iwai, T., Miyasaka, A., Seo, S., and Ohashi, Y. (2006). Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants. Plant Physiol. 142, 1202. doi: 10.1104/pp.106.085258
61. Jayawardana, H. A. R. K., Weerahewa, H. L. D., and Saparamadu, M. D. J. S. (2016). The mechanisms underlying the Anthracnose disease reduction by rice hull as a silicon source in capsicum (Capsicum annuum L.) grown in simplified hydroponics. Procedia Food Sci. 6, 147–150. doi: 10.1016/j.profoo.2016.02.035
62. Kablan, L., Lagauche, A., Delvaux, B., and Legrève, A. (2012). Silicon reduces black sigatoka development in banana. Plant Dis. 96, 273–278. doi: 10.1094/pdis-04-11-0274
63. Kanto, T., Miyoshi, A., Ogawa, T., Maekawa, K., and Aino, M. (2006). Suppressive effect of liquid potassium silicate on powdery mildew of strawberry in soil. J.Gen. Plant Pathol. 72, 137–142. doi: 10.1007/s10327-005-0270-8
64. Kauss, H., Kai, S., Franke, R., Gilbert, S., Dietrich, R. A., and Kröger, N. (2003). Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. Plant J. 33, 87–95. doi: 10.1046/j.1365-313X.2003. 01606.x
65. Kim, S. G., Kim, K. W., Park, E. W., and Choi, D. (2002). Silicon-induced cell wall fortification of rice leaves: a possible cellular mechanism of enhanced host resistance to blast. Phytopathology 92, 1095–1103. doi: 10.1094/PHYTO.2002. 92.10.1095
66. Kim, Y. H., Khan, A. L., Kim, D. H., Lee, S. Y., Kim, K. M., Waqas, M., et al. (2014). Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol. 14:13. doi: 10.1186/1471-2229-14-13
67. Kurabachew, H., Stahl, F., and Wydra, K. (2013). Global gene expression of rhizobacteria-silicon mediated induced systemic resistance in tomato (Solanum lycopersicum) against Ralstonia solanacearum. Physiol. Mol. Plant Pathol. 84, 44–52. doi: 10.1016/j.pmpp.2013.06.004
68. Łaźniewska, J., Macioszek, V. K., and Kononowicz, A. K. (2012). Plant-fungus interface: the role of surface structures in plant resistance and susceptibility to pathogenic fungi. Physiol. Mol. Plant Pathol. 78, 24–30. doi: 10.1016/j.pmpp. 2012.01.004
69. Lemes, E. M., Mackowiak, C. L., Blount, A., Marois, J. J., Wright, D. L., Coelho, L., et al. (2011). Effects of silicon applications on soybean rust development under greenhouse and field conditions. Plant Dis. 95, 317–324. doi: 10.1094/pdis-07-10-0500
70. Lepolu Torlon, J., Heckman, J., Simon, J., and Wyenandt, C. (2016). Silicon soil amendments for suppressing powdery mildew on pumpkin. Sustainability 8:293. doi: 10.3390/su8040293
71. Li, J., Brader, G., and Palva, E. T. (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16, 319–331. doi: 10.1105/tpc.016980
72. Li, W., Bi, Y., Ge, Y., Li, Y., Wang, J., and Wang, Y. (2011). Effects of postharvest sodium silicate treatment on pink rot disease and oxidative stress-antioxidative system in muskmelon fruit. Eur. Food Res. Technol. 234, 137–145. doi: 10.1007/s00217-011-1611-9
73. Li, Y. C., Bi, Y., Ge, Y. H., Sun, X. J., and Wang, Y. (2009). Antifungal activity of sodium silicate on Fusarium sulphureum and its effect on dry rot of potato tubers. J. Food Sci. 74, 213–218. doi: 10.1111/j.1750-3841.2009.01154.x
74. 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
75. Liang, Y. C., Sun, W., Si, J., and Römheld, V. (2005a). Effects of foliar-and root-applied silicon on the enhancement of induced resistance to powdery mildew in Cucumis sativus. Plant Pathol. 54, 678–685. doi: 10.1111/j.1365-3059.2005. 01246.x
76. Liang, Y. C., Wong, J. W. C., and Wei, L. (2005b). 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
77. Liu, L., Guo, Y., Bi, Y., Li, M., Zhao, J., and Zhao, H. (2009). Inhabited mechanisms of silicon compounds against Fusarium rot (Fusarium spp.) of postharvest Chinese cantaloupe. J. Food Process. Preserv. 33, 187–202. doi: 10.1111/j.1745-4549.2008.00292.x
78. Liu, P., Yin, L. N., Deng, X. P., Wang, S. W., Tanaka, K., and Zhang, S. Q. (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
79. 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
80. Ma, J. F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., et al. (2006). A silicon transporter in rice. Nature 440, 688–691. doi: 10.1038/nature 04590
81. 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
82. 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
83. Ma, J. F., Yamaji, N., Mitani, N., Tamai, K., Konishi, S., Fujiwara, T., et al. (2007). An efflux transporter of silicon in rice. Nature 448, 209–212. doi: 10.1038/nature05964
84. Ma, J. F., Yamaji, N., Mitani, N., Xu, X. Y., Su, Y. H., Mcgrath, S. P., et al. (2008). Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. U.S.A. 105, 9931–9935. doi: 10.1073/pnas. 0802361105
85. Majeed Zargar, S., Nazir, M., Kumar Agrawal, G., Kim, D. W., and Rakwal, R. (2010). Silicon in plant tolerance against environmental stressors: towards crop improvement using omics approaches. Curr. Proteomics 7, 135–143. doi: 10. 2174/157016410791330507
86. Marschner, P. (2012). Marschner’s Mineral Nutrition of Higher Plants. London: Academic Press.
87. Mburu, K., Oduor, R., Mgutu, A., and Tripathi, L. (2015). Silicon application enhances resistance to xanthomonas wilt disease in banana. Plant Pathol. 65, 807–818. doi: 10.1111/ppa.12468
88. McDonagh, D., and Hunter, A. (2010). Effect of silicon application on Lolium perenne development and Fusarium control. Paper presented at the XXVIII International Horticultural Congress on Science and Horticulture for People (IHC2010), Lisbon, 195–201.
89. Menzies, J., Bowen, P., Ehret, D., and Glass, A. D. (1992). Foliar applications of potassium silicate reduce severity of powdery mildew on cucumber, muskmelon, and zucchini squash. J. Am. Soc. Hortic. Sci. 117, 902–905.
90. Menzies, J., Ehret, D., Glass, A., and Samuels, A. (1991). The influence of silicon on cytological interactions between Sphaerotheca fuliginea and Cucumis sativus. Physiol. Mol. Plant Pathol. 39, 403–414. doi: 10.1016/0885-5765(91)90007-5
91. Miyake, Y., and Takahashi, E. (1983). Effect of silicon on the growth of solution-cultured cucumber plant. Soil Sci. Plant Nutr. 29, 71–83. doi: 10.1080/00380768. 1983.10432407
92. Moldes, C. A., De Lima Filho, O. F., Merini, L. J., Tsai, S. M., and Camiña, J. M. (2016). Occurrence of powdery mildew disease in wheat fertilized with increasing silicon doses: a chemometric analysis of antioxidant response. Acta Physiol. Plant. 38, 206. doi: 10.1007/s11738-016-2217-4
93. Moyer, C., Peres, N. A., Datnoff, L. E., Simonne, E. H., and Deng, Z. (2008). Evaluation of silicon for managing powdery mildew on gerbera daisy. J. Plant Nutr. 31, 2131–2144. doi: 10.1080/01904160802459641
94. Najihah, N. I., Hanafi, M. M., Idris, A. S., and Hakim, M. A. (2015). Silicon treatment in oil palms confers resistance to basal stem rot disease caused by Ganoderma boninense. Crop Prot. 67, 151–159. doi: 10.1016/j.cropro.2014. 10.004
95. Nawrath, C. (2006). Unraveling the complex network of cuticular structure and function. Curr. Opin. Plant Biol. 9, 281–287. doi: 10.1016/j.pbi.2006.03.001
96. 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
97. Pan, S., and Ye, X. (1992). Induction of chitinases in tobacco plants systemically protected against blue mold by Peronospora tabacina or tobacco mosaic virus. Phytopathology 82, 119–123. doi: 10.1094/Phyto-82-119
98. Peters, F. R., Datnoff, L., Korndörfer, G., Seebold, K., and Rush, M. (2001). Effect of silicon and host resistance on sheath blight development in rice. Plant Dis. 85, 827–832. doi: 10.1094/PDIS.2001.85.8.827
99. Pieterse, C. M., Leon-Reyes, A., Van Der Ent, S., and Van Wees, S. C. (2009). Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308–316. doi: 10.1038/nchembio.164
100. Pieterse, C. M., Van, D. D. D., Zamioudis, C., Leonreyes, A., and Van Wees, S. C. (2012). Hormonal modulation of plant immunity. Cell Dev. Biol. 28, 489–521. doi: 10.1146/annurev-cellbio-092910-154055
101. Piperno, D. R. (ed.) (2006). “The production, deposition, and dissolution of phytoliths,” in Phytoliths: A Comprehensive Guide for Archaeologists and Paleoecologists, (Lanham, MD: AltaMira Press).
102. Pirrello, J., Prasad, B. N., Zhang, W., Chen, K., Mila, I., Zouine, M., et al. (2012). Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol. 12:190. doi: 10.1186/1471-2229-12-190
103. Polanco, L. R., Rodrigues, F. A., Nascimento, K. J., Cruz, M. F., Curvelo, C. R., Damatta, F. M., et al. (2014). Photosynthetic gas exchange and antioxidative system in common bean plants infected by Colletotrichum lindemuthianum and supplied with silicon. Trop. Plant Pathol. 39, 35–42. doi: 10.1590/S1982-56762014000100005
104. Prabhu, A. S., Barbosa Filho, M. P., Datnoff, L. E., Snyder, G. H., Berni, R. F., Rodrigues, F. A., et al. (2012). Silicon reduces brown spot severity and grain discoloration on several rice genotypes. Trop. Plant Pathol. 37, 409–414. doi: 10.1590/S1982-56762012000600005
105. Qin, G. Z., and Tian, S. P. (2005). Enhancement of biocontrol activity of Cryptococcus laurentii by silicon and the possible mechanisms involved. Phytopathology 95, 69–75. doi: 10.1094/PHYTO-95-0069
106. Quarta, A., Mita, G., Durante, M., Arlorio, M., and De, P. A. (2013). Isolation of a polyphenol oxidase (PPO) cDNA from artichoke and expression analysis in wounded artichoke heads. Plant Physiol. Biochem. 68, 52–60. doi: 10.1016/j. plaphy.2013.03.020
107. Rahman, A., Wallis, C. M., and Uddin, W. (2015). Silicon-induced systemic defense responses in perennial ryegrass against infection by Magnaporthe oryzae. Phytopathology 105, 748–757. doi: 10.1094/PHYTO-12-14-0378-R
108. Ramouthar, P. V., Caldwell, P. M., and Mcfarlane, S. A. (2015). Effect of silicon on the severity of brown rust of sugarcane in South Africa. Eur. J. Plant Pathol. 145, 53–60. doi: 10.1007/s10658-015-0812-7
109. Ratnayake, R. M. R. N. K., Daundasekera, W. A. M., Ariyarathne, H. M., and Ganehenege, M. Y. U. (2016). Some biochemical defense responses enhanced by soluble silicon in bitter gourd-powdery mildew pathosystem. Australas. Plant Pathol. 45, 425–433. doi: 10.1007/s13313-016-0429-0
110. Remus-Borel, W., Menzies, J. G., and Belanger, R. R. (2005). Silicon induces antifungal compounds in powdery mildew-infected wheat. Physiol. Mol. Plant Pathol. 66, 108–115. doi: 10.1016/j.pmpp.2005.05.006
111. Resende, R. S., Rodrigues, F., Costa, R. V., and Silva, D. D. (2013). Silicon and fungicide effects on anthracnose in moderately resistant and susceptible sorghum lines. J. Phytopathol. 161, 11–17. doi: 10.1111/jph.12020
112. Reynolds, O. L., Padula, M. P., Zeng, R. S., and Gurr, G. M. (2016). Silicon: potential to promote direct and indirect effects on plant defense against arthropod pests in agriculture. Front. Plant Sci. 7:744. doi: 10.3389/fpls.2016.00744
113. 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
114. Rodrigues, F., Benhamou, N., Datnoff, L. E., Jones, J. B., and Bélanger, R. R. (2003). Ultrastructural and cytochemical aspects of silicon-mediated rice blast resistance. Phytopathology 93, 535–546. doi: 10.1094/PHYTO.2003.93. 5.535
115. Rodrigues, F., Duarte, H. S. S., Rezende, D. C., Filho, J. A. W., Korndörfer, G. H., and Zambolim, L. (2010). Foliar spray of potassium silicate on the control of angular leaf spot on beans. J. Plant Nutr. 33, 2082–2093. doi: 10.1080/01904167. 2010.519082
116. Rodrigues, F. A., and Datnof, L. E. (2015). Silicon and Plant Diseases. Berlin: Springer. doi: 10.1007/978-3-319-22930-0
117. Rodrigues, F. A., Datnoff, L. E., Korndorfer, G. H., Seebold, K. W., and Rush, M. C. (2001). Effect of silicon and host resistance on sheath blight development in rice. Plant Dis. 85, 827–832. doi: 10.1094/PDIS.2001.85.8.827
118. Rodrigues, F. A., Jurick, W. M., Datnoff, L. E., Jones, J. B., and Rollins, J. A. (2005). Silicon influences cytological and molecular events in compatible and incompatible rice-Magnaporthe grisea interactions. Physiol. Mol. Plant Pathol. 66, 144–159. doi: 10.1016/j.pmpp.2005.06.002
119. Rodrigues, F. A., Mcnally, D. J., Datnoff, L. E., Jones, J. B., Labbé, C., Benhamou, N., et al. (2004). Silicon enhances the accumulation of diterpenoid phytoalexins in rice: a potential mechanism for blast resistance. Phytopathology 94, 177–183. doi: 10.1094/PHYTO.2004.94.2.177
120. Rodrigues, F. A., Polanco, L. R., Duarte, H. S. S., Resende, R. S., and Do Vale, F. X. R. (2015a). Photosynthetic gas exchange in common bean submitted to foliar sprays of potassium silicate, sodium molybdate and fungicide and infected with Colletotrichum lindemuthianum. J. Phytopathol. 163, 554–559. doi: 10.1111/jph.12353
121. Rodrigues, F. A., Resende, R. S., Dallagnol, L. J., and Datnoff, L. E. (2015b). Silicon Potentiates Host Defense Mechanisms against Infection by Plant Pathogens. Cham: Springer International Publishing. doi: 10.1007/978-3-319-22930-0_5
122. Sakr, N. (2016). The role of silicon (Si) in increasing plant resistance against fungal diseases. Hell. Plant Protect. J. 9, 1–15. doi: 10.1515/hppj-2016-0001
123. Samuels, A. L., Adm, G., Menzies, J. G., and Ehret, D. L. (1994). Silicon in cell walls and papillae of Cucumis sativus during infection by Sphaerotheca fuliginea. Physiol. Mol. Plant Pathol. 44, 237–242. doi: 10.1016/S0885-5765(05)80027-X
124. 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
125. Savvas, D., Giotis, D., Chatzieustratiou, E., Bakea, M., and Patakioutas, G. (2009). Silicon supply in soilless cultivations of zucchini alleviates stress induced by salinity and powdery mildew infections. Environ. Exp. Bot. 65, 11–17. doi: 10.1016/j.envexpbot.2008.07.004
126. Schmelzer, E. (2002). Cell polarization, a crucial process in fungal defence. Trends Plant Sci. 7, 411–415. doi: 10.1016/S1360-1385(02)02307-5
127. Schurt, D. A., Cruz, M. F., Nascimento, K. J., Filippi, M. C., and Rodrigues, F. A. (2014). Silicon potentiates the activities of defense enzymes in the leaf sheaths of rice plants infected by Rhizoctonia solani. Trop. Plant Pathol. 39, 457–463. doi: 10.1590/S1982-56762014000600007
128. Seebold, K. W., Datnoff, L., Correa-Victoria, F. J., Kucharek, T. A., and Snyder, G. H. (2000). Effect of silicon rate and host resistance on blast, scald, and yield of upland rice. Plant Dis. 84, 871–876. doi: 10.1094/PDIS.2000.84.8.871
129. Seebold, K. W., Datnoff, L. E., Correa-Victoria, F. J., Kucharek, T. A., and Snyder, G. H. (2004). Effects of silicon and fungicides on the control of leaf and neck blast in upland rice. Plant Dis. 88, 253–258. doi: 10.1094/Pdis.2004.88. 3.253
130. Shah, J. (2003). The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6, 365–371. doi: 10.1016/S1369-5266(03)00058-X
131. Shetty, R., Jensen, B., Shetty, N. P., Hansen, M., Hansen, C. W., Starkey, K. R., et al. (2012). Silicon induced resistance against powdery mildew of roses caused by Podosphaera pannosa. Plant Pathol. 61, 120–131. doi: 10.1111/j.1365-3059. 2011.02493.x
132. Shewry, P. R., and Lucas, J. A. (1997). Plant proteins that confer resistance to pests and pathogens. Adv. Bot. Res. 26, 135–192. doi: 10.1016/S0065-2296(08) 60120-2
133. Silva, I. T., Rodrigues, F. A., Oliveira, J. R., Pereira, S. C., Andrade, C. C. L., Silveira, P. R., et al. (2010). Wheat resistance to bacterial leaf streak mediated by silicon. J. Phytopathol. 158, 253–262. doi: 10.1111/j.1439-0434.2009. 01610.x
134. Silva, R., Oliveira, R., Nascimento, K., and Rodrigues, F. (2010). Biochemical responses of coffee resistance against Meloidogyne exigua mediated by silicon. Plant Pathol. 59, 586–593. doi: 10.1111/j.1365-3059.2009.02228.x
135. Silva, W. L. D., Cruz, M. F. A., Fortunato, A. A., and Rodrigues, F. (2015). Histochemical aspects of wheat resistance to leaf blast mediated by silicon. Sci. Agric. 72, 322–327. doi: 10.1590/0103-9016-2014-0221
136. Song, A., Xue, G., Cui, P., Fan, F., Liu, H., Chang, Y., et al. (2016). The role of silicon in enhancing resistance to bacterial blight of hydroponic- and soil-cultured rice. Sci. Rep. 6:24640. doi: 10.1038/srep24640
137. Sousa, R. S., Rodrigues, F. A., Schurt, D. A., Souza, N. F. A., and Cruz, M. F. A. (2013). Cytological aspects of the infection process of Pyricularia oryzae on leaves of wheat plants supplied with silicon. Trop. Plant Pathol. 38, 472–477. doi: 10.1590/S1982-56762013000600002
138. Sun, W., Zhang, J., Fan, Q., Xue, G., Li, Z., and Liang, Y. (2010). Silicon-enhanced resistance to rice blast is attributed to silicon-mediated defence resistance and its role as physical barrier. Eur. J. Plant Pathol. 128, 39–49. doi: 10.1007/s10658-010-9625-x
139. Takahashi, E., Ma, J. F., and Miyake, Y. (1990). The possibility of silicon as an essential element for higher plants. Comment. Agric. Food Chem. 2, 99–102. doi: 10.1016/j.bbagen.2013.11.021
140. Tatagiba, S. D., Damatta, F. M., and Rodrigues, F. A. (2016). Silicon partially preserves the photosynthetic performance of rice plants infected by Monographella albescens. Ann. Appl. Biol. 168, 111–121. doi: 10.1111/aab. 12246
141. Telles Nascimento, K. J., Debona, D., Silva, L. C., Damatta, F. M., and Rodrigues, F. (2016). Silicon-induced changes in the antioxidant system reduce soybean resistance to frogeye leaf spot. J. Phytopathol. 164, 768–778. doi: 10.1111/jph. 12497
142. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., et al. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665. doi: 10.1038/nature05960
143. Uriarte, R. F., Shew, H. D., and Bowman, D. C. (2004). Effect of soluble silica on brown patch and dollar spot of creeping bentgrass. J. Plant Nutr. 27, 325–339. doi: 10.1081/PLN-120027657
144. Van, B. 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
145. Van, B. J., Spíchal, L., Novák, O., Strnad, M., Asano, T., Kikuchi, S., et al. (2015a). Silicon induces resistance to the brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene pathway. New Phytol. 206, 761–773. doi: 10.1111/nph.13270
146. Van, B. J., Steppe, K., Bauweraerts, I., Kikuchi, S., Asano, T., and De, V. D. (2015b). Primary metabolism plays a central role in molding silicon-inducible brown spot resistance in rice. Mol. Plant Pathol. 16, 811–824. doi: 10.1111/mpp.12236
147. Vermeire, M. L., Kablan, L., Dorel, M., Delvaux, B., Risède, J. M., and Legrève, A. (2011). Protective role of silicon in the banana-Cylindrocladium spathiphylli pathosystem. Eur. J. Plant Pathol. 131, 621–630. doi: 10.1007/s10658-011-9835-x
148. Vivancos, J., Labbe, C., Menzies, J. G., and Belanger, R. R. (2015). Silicon-mediated resistance of Arabidopsis against powdery mildew involves mechanisms other than the salicylic acid (SA)-dependent defence pathway. Mol. Plant Pathol. 16, 572–582. doi: 10.1111/mpp.12213
149. Waewthongrak, W., Pisuchpen, S., and Leelasuphakul, W. (2015). Effect of Bacillus subtilis and chitosan applications on green mold (Penicillium digitatum Sacc.) decay in citrus fruit. Postharvest Biol. Technol. 99, 44–49. doi: 10.1016/j. postharvbio.2014.07.016
150. Whan, J. A., Dann, E. K., and Aitken, E. A. (2016). Effects of silicon treatment and inoculation with Fusarium oxysporum f. sp. vasinfectum on cellular defences in root tissues of two cotton cultivars. Ann. Bot. 118, 219–226. doi: 10.1093/aob/mcw095
151. Wiese, J., Wiese, H., Schwartz, J., and Schubert, S. (2005). Osmotic stress and silicon act additively in enhancing pathogen resistance in barley against barley powdery mildew. J. Plant Nutr. Soil Sci. 168, 269–274. doi: 10.1002/jpln.2004 20490
152. Ye, M., Song, Y. Y., Long, J., Wang, R. L., Baerson, S. R., Pan, Z. Q., et al. (2013). Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc. Natl. Acad. Sci. U.S.A. 110, 3631–3639. doi: 10.1073/pnas. 1305848110
153. Zellner, W., Frantz, J., and Leisner, S. (2011). Silicon delays Tobacco ringspot virus systemic symptoms in Nicotiana tabacum. J. Plant Physiol. 168, 1866–1869. doi: 10.1016/j.jplph.2011.04.002
154. Zeyen, R. J., Ahlstrand, G. G., and Carver, T. L. W. (1993). X-ray microanalysis of frozen-hydrated, freeze-dried, and critical point dried leaf specimens: determination of soluble and insoluble chemical elements of Erysiphe graminis epidermal cell papilla sites in barley isolines containing Ml-O and ml-O alleles. Can. J. Bot. 71, 284–296. doi: 10.1139/b93-029
155. Zhang, G., Cui, Y., Ding, X., and Dai, Q. (2013). Stimulation of phenolic metabolism by silicon contributes to rice resistance to sheath blight. J. Plant Nutr. Soil Sci. 176, 118–124. doi: 10.1002/jpln.201200008
156. Zhang, H., Zhang, D., Chen, J., Yang, Y., Huang, Z., Huang, D., et al. (2004). Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol. Biol. 55, 825–834. doi: 10.1007/s11103-005-2140-3
157. Zhang, Q., Fry, J., Lowe, K., and Tisserat, N. (2006). Evaluation of calcium silicate for brown patch and dollar spot suppression on turfgrasses. Crop Sci. 46, 1635–1643. doi: 10.2135/cropsci2005.04-0002