Silicon enhances water stress tolerance by improving root hydraulic conductance in solanum lycopersicum L.

Frontiers in Plant Science

Volumn 7, Issue FEB2016, 2016, Pages

  Shi, Yu ^a,b   Zhang, Yi ^b   Han, Weihua ^a   Feng, Ru ^a   Hu, Yanhong ^a   Guo, Jia ^a   Gong, Haijun ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b SHANXI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Oxidative damage; Root hydraulic conductance; Silicon (Si); Tomato (Solanum lycopersicum); Water stress

Indexed keywords

EID: 84960099646     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00196     Document Type: Article

References (55)

1. Aroca, R., Amodeo, G., Fernández-Illescas, S., Herman, E. M., Chaumont, F., and Chrispeels, M. J. (2005). The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol. 137, 341-353. doi: 10.1104/pp.104.051045
2. Ashraf, M., and Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59, 206-216. doi: 10.1016/j.envexpbot.2005.12.006
3. Bailly, C., Benamar, A., Corbineau, F., and Come, D. (1996). Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol. Plant 97, 104-110. doi: 10.1111/j.1399-3054.1996.tb00485.x
4. Bates, L. S., Waldren, R. P., and Teare, I. D. (1973). Rapid determination of free proline for water stress studies. Plant Soil 39, 205-207. doi: 10.1016/j.dental.2010.07.006
5. Benabdellah, K., Ruiz-Lozano, J. M., and Aroca, R. (2009). Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol. Biol. 70, 647-661. doi: 10.1007/s11103-009-9497-7
6. Bergougnoux, V. (2014). The history of tomato: from domestication to biopharming.Biotechnol. Adv. 32, 170-189. doi: 10.1016/j.biotechadv.2013.11.003
7. Boursiac, Y., Boudet, J., Postaire, O., Luu, D. T., Tournaire-Roux, C., and Maurel, C. (2008a). Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J. 56, 207-218. doi: 10.1111/j.1365-313X.2008.03594.x
8. Boursiac, Y., Prak, S., Boudet, J., Postaire, O., Luu, D. T., Tournaire-Roux, C., et al. (2008b). The response of Arabidopsis root water transport to a challenging environment implicates reactive oxygen species- and phosphorylation-dependent internalization of aquaporins. Plant Signal. Behav. 3, 1096-1098. doi: 10.4161/psb.3.12.7002
9. Chaumont, F., and Tyerman, S. D. (2014). Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol. 164, 1600-1618. doi: 10.1104/pp.113.233791
10. Chen, W., Yao, X. Q., Cai, K. Z., 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
11. Csiszár, J., Gallé,Á, Horváth, E., Dancsó, P., Gombos, M., and Váry, Z. (2012). Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress. Plant Physiol. Biochem. 52, 119-129. doi: 10.1016/j.plaphy.2011.12.006
12. Diogo, R. V. C., and Wydra, K. (2007). Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol. Mol. Plant Pathol. 70, 120-129. doi: 10.1016/j.pmpp.2007.07.008
13. Elstner, E. F., and Heupel, A. (1976). Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal. Biochem.70, 616-620. doi: 10.1016/0003-2697(76)90488-7
14. Enstone, D. E., Peterson, C. A., and Ma, F. (2003). Root endodermis and exodermis: structure, function, and responses to the environment. J. Plant Growth Regul. 21, 335-351. doi: 10.1007/s00344-003-0002-2
15. 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
16. Gao, X., Zou, C., Wang, L., and Zhang, F. (2004). Silicon improves water use efficiency in maize plants. J. Plant Nutr. 27, 1457-1470. doi: 10.1081/PLN-200025865
17. 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
18. Gong, H. J., and Chen, K. M. (2012). The regulatory role of silicon on water relations, photosynthetic gas exchange, and carboxylation activities of wheat leaves in field drought conditions. Acta Physiol. Plant. 34, 1589-1594. doi: 10.1007/s11738-012-0954-6
19. Gong, H. J., Chen, K. M., Zhao, Z. G., Chen, G. C., and Zhou, W. J. (2008). Effects of silicon on defense of wheat against oxidative stress under drought at different developmental stages. Biol. Plant. 52, 592-596. doi: 10.1007/s10535-008-0118-0
20. 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
21. Hattori, T., Inanaga, S., Araki, H., An, P., Morita, S., Luxová, 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
22. Hattori, T., Sonobe, K., Inanaga, S., An, P., and Morita, S. (2008). Effects of silicon on photosynthesis of young cucumber seedlings under osmotic stress. J. Plant Nutr. 31, 1046-1058. doi: 10.1080/01904160801928380
23. Huang, C., He, W., Guo, J., Chang, X., Su, P., and Zhang, L. (2005). Increased sensitivity to salt stress in ascorbate deficient Arabidopsis mutant. J. Exp. Bot. 56, 3041-3049. doi: 10.1093/jxb/eri301
24. Javot, H., and Maurel, C. (2002). The role of aquaporins in root water uptake. Ann. Bot.90, 301-313. doi: 10.1093/aob/mcf199
25. 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
26. Kaya, C., Tuna, L., and Higgs, D. (2006). Effect of silicon on plant growth and mineral nutrition of maize grown under water-stress conditions. J. Plant Nutr. 29, 1469-1480. doi: 10.1080/01904160600837238
27. 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
28. 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
29. Ma, J. F., Miyake, Y., and Takahashi, E. (2001). "Silicon as a beneficial element for crop plants," in Silicon in Agriculture, eds L. Datonoff, G. Snyder, and G. Korndorfer (New York, NY: Elsevier Science Publishing), 17-39.
30. Matoh, T., Murata, S., and Takahashi, E. (1991). Effect of silicate application on photosynthesis of rice plants. Jap. J. Soil Sci. Plant Nutr. 62, 248-251.
31. 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
32. Miyamoto, N., Steudle, E., Hirasawa, T., and Lafitte, R. (2001). Hydraulic conductivity of rice roots. J. Exp. Bot. 52, 1835-1846. doi: 10.1093/jexbot/52.362.1835
33. Muneer, S., and Jeong, B. R. (2015). Proteomic analysis of salt-stress responsive proteins in roots of tomato (Lycopersicon esculentum L.) plants towards silicon efficiency. Plant Growth Regul. 77, 133-146. doi: 10.1007/s10725-015-0045-y
34. Muneer, S., Park, Y. G., Manivannan, A., Soundararajan, P., and Jeong, B. R. (2014). Physiological and proteomic analysis in chloroplasts of Solanum lycopersicum L. under silicon efficiency and salinity stress. Int. J. Mol. Sci. 15, 21803-21824. doi: 10.3390/ijms151221803
35. Nikolic, M., Nikolic, N., Liang, Y. C., Kirkby, E. A., and Römheld, V. (2007). Germanium-68 as an adequate tracer for silicon transport in plants. Characterization of silicon uptake in different crop species. Plant Physiol. 143, 495-503. doi: 10.1104/pp.106.090845
36. Paradiso, A., Berardino, R., de Pinto, M. C., Sanità di Toppi, L., Storelli, M. M., Tommasi, F., et al. (2008). Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol. 49, 362-374. doi: 10.1093/pcp/pcn013
37. 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
38. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 203-207. doi: 10.1093/nar/29.9.e45
39. Pompella, A., Maellaro, E., Casini, A. F., and Comporti, M. (1987). Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am. J. Pathol. 129, 295-301.
40. Razem, F. A., and Bernards, M. A. (2002). Hydrogen peroxide is required for poly-(phenolic) domain formation during wound-induced suberization. J. Agr. Food Chem.50, 1009-1015. doi: 10.1021/jf0110248
41. Rubio-Asensio, J. S., López-Berenguer, C., Garma, J. G., Burger, M., and Bloom, A. J. (2014). "Root strategies for nitrate assimilation," in Root Engineering: Basic and Applied Concepts, eds A. Morte and A. Varma (Heidelberg: Springer), 251-267.
42. Savant, N. K., Korndörfer, G. H., Datnoff, L. E., and Snyder, G. H. (1999). Silicon nutrition and sugarcane production: a review. J. Plant Nutr. 22, 1853-1903. doi: 10.1080/01904169909365761
43. Shi, Y., Zhang, Y., Yao, H. J., Wu, J. W., Sun, H., and Gong, H. J. (2014). Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol. Biochem. 78, 27-36. doi: 10.1016/j.plaphy.2014.02.009
44. Steudle, E., and Peterson, C. A. (1998). How does water get through roots? J. Exp. Bot.49, 775-788. doi: 10.1093/jxb/49.322.775
45. Sutka, M., Li, G., Boudet, J., Boursiac, Y., Doumas, P., and Maurel, C. (2011). Natural variation of root hydraulics in arabidopsis grown in normal and saltstressed conditions.Plant Physiol. 155, 1264-1276. doi: 10.1104/pp.110.163113
46. Van Bockhaven, J., De Vleesschauwer, D., and Höfte, 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
47. Vandeleur, R. K., Mayo, G., Shelden, M. C., Gilliham, M., Kaiser, B. N., and Tyerman, S. D. (2009). The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol. 149, 445-460. doi: 10.1104/pp.108.128645
48. Wang, K., Shao, X. F., Gong, Y. F., Zhu, Y., Wang, H. F., Zhang, X. L., et al. (2013). The metabolism of soluble carbohydrates related to chilling injury in peach fruit exposed to cold stress. Postharvest Biol. Technol. 86, 53-61. doi: 10.1016/j.postharvbio.2013.06.020
49. Wang, Y. S., and Yang, Z. M. (2005). Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol. 46, 1915-1923. doi: 10.1093/pcp/pci202
50. 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 torvumto cadmium stress.New Phytol. 196, 125-138. doi: 10.1111/j.1469-8137.2012.04236.x
51. Yang, Y., Liu, Q., Wang, G. X., Wang, X. D., and Guo, J. Y. (2010). Germination, osmotic adjustment, and antioxidant enzyme activities of gibberellin-pretreated Picea asperataseeds under water stress. New For. 39, 231-243. doi: 10.1007/s11056-009-9167-2
52. Ye, Q., and Steudle, E. (2006). Oxidative gating of water channels (aquaporins) in corn roots. Plant Cell Environ. 29, 459-470. doi: 10.1111/j.1365-3040.2005.01423.x
53. Yin, L. N., Wang, S. W., Li, J. Y., Tanaka, K., and Oka, M. (2013). Application of silicon improves salt tolerance through ameliorating osmotic and ionic stresses in the seedling of Sorghum bicolor. Acta Physiol. Plant. 35, 3099-3107. doi: 10.1007/s11738-013-1343-5
54. Zhu, Y. X., and Gong, H. J. (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
55. 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