Advertisement

Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 70–82 | Cite as

Silicon (Si) Supplementation Alleviates NaCl Toxicity in Mung Bean [Vigna radiata (L.) Wilczek] Through the Modifications of Physio-biochemical Attributes and Key Antioxidant Enzymes

  • Parvaiz AhmadEmail author
  • Mohammad Abass Ahanger
  • Pravej Alam
  • Mohammed Nasser Alyemeni
  • Leonard Wijaya
  • Sajad Ali
  • Mohammad Ashraf
Article

Abstract

Mung bean is an important pulse crop. It is highly nutritive but is vulnerable to salinity stress. Therefore, the present study was aimed to investigate the protective effect of silicon (Si) against salt stress-induced damage to mung bean plants. Mung bean plants treated with NaCl (0, 50 and 100 mM) showed considerable declines in length and dry weights of shoots and roots. Chlorophyll-a (chl-a), chl-b, total chl, carotenoids and leaf relative water content (LRWC) decreased under NaCl stress. However, supplementation with Si in the form of sodium silicate (Na2SiO3) to NaCl-stressed plants ameliorated the adverse effects of NaCl on growth, biomass, pigment synthesis and leaf relative water content (LRWC). Silicon (Si)-supplemented plants exhibited enhanced chl-fluorescence and gas exchange parameters under normal (non-stress) as well as NaCl stress conditions. Salt-induced decline in the frequency of stomata and number of leaves per plant under salt stress was significantly recovered with Si supplementation. In addition, application of Si increased the levels of proline and glycine betaine in mung bean plants. Furthermore, histochemical staining tests showed that the levels of superoxide radicals and H2O2 increased with NaCl treatments, which thereby resulted in increased lipid peroxidation (LPO) and electrolyte leakage. Contrarily, decreased levels of H2O2, lipid peroxidation (measured as MDA content), and electrolyte leakage in Si-supplemented plants under NaCl stress indicated the stress mitigating role of Si. The activities of key antioxidant enzymes (SOD, CAT, APX and GR) under NaCl stress showed an increase under the NaCl regime. However, application of Si further boosted the activities of all four antioxidant enzymes in NaCl-stressed plants. The enhanced Na+ uptake and Na+/K+ ratio in mung bean plants accompanied by decreased K+ and Ca2+ uptake under NaCl stress were reversed with Si supplementation thereby resulting in enhanced accumulation of K+ and Ca2+ and decreased Na+. In conclusion, Si supplementation mitigated the negative effects of NaCl on mung bean plants through modifications in uptake of inorganic nutrients, osmolyte production and the antioxidant defence system.

Keywords

Antioxidants Mung bean NaCl Oxidative stress Silicon Histochemical staining 

Notes

Acknowledgements

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for funding this research group No. RGP-199.

Author Contributions

PA, MAA and MNA designed the experimental work. PA and LW carried out the statistical analysis. PA, MA, MAA and SA wrote and revised the manuscript. All the authors have read the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Abbas T, Balal RM, Shahid MA, Pervez MA, Ayyub CM, Aqueel MA, Javaid MM (2015) Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and antioxidant metabolism. Acta Physiol Plant.  https://doi.org/10.1007/s11738-014-1768-5 Google Scholar
  2. Abd-Alla MH, Vuong TD, Harper JE (1998) Genotypic differences in dinitrogen fixation response to NaCl stress in intact and grafted soybean. Crop Sci 38:72.  https://doi.org/10.2135/cropsci1998.0011183x003800010013x CrossRefGoogle Scholar
  3. Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F, Agata W, Kaufman PB (1998) Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L.), monitored by electrolyte leakage. Plant Prod Sci 1:96–103.  https://doi.org/10.1626/pps.1.96 CrossRefGoogle Scholar
  4. Ahanger MA, Agarwal RM (2017) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiol Biochem 115:449–460.  https://doi.org/10.1016/j.plaphy.2017.04.017 CrossRefGoogle Scholar
  5. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175.  https://doi.org/10.3109/07388550903524243 CrossRefGoogle Scholar
  6. Ahmad P, Ozturk M, Sharma S, Gucel S (2013) Effect of sodium carbonate-induced salinity–alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J Plant Interact 9:460–467.  https://doi.org/10.1080/17429145.2013.855271 CrossRefGoogle Scholar
  7. Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense system. Front Plant Sci 6  https://doi.org/10.3389/fpls.2015.00868
  8. Ahmad P, Abdel Latef AA, Hashem A, Abd_Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7  https://doi.org/10.3389/fpls.2016.00347
  9. Al-aghabary K, Zhu Z, Shi Q (2005) 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.  https://doi.org/10.1081/pln-200034641 CrossRefGoogle Scholar
  10. Ali S, Cai S, Zeng F, Qiu B, Zhang G (2012) Effect of salinity and hexavalent chromium stresses on uptake and accumulation of mineral elements in barley genotypes differing in salt tolerance. J Plant Nutr 35:827–839CrossRefGoogle Scholar
  11. Ashraf M, McNeilly T (2004) Salinity tolerance in brassica oilseeds. Crit Rev Plant Sci 23:157–174.  https://doi.org/10.1080/07352680490433286 CrossRefGoogle Scholar
  12. Ashraf MA, Ashraf M, Ali Q (2010) Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pak J Bot 42:559–565Google Scholar
  13. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207.  https://doi.org/10.1007/bf00018060 CrossRefGoogle Scholar
  14. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434CrossRefGoogle Scholar
  15. de Sousa Paula L et al (2015) Silicon (Si) ameliorates the gas exchange and reduces negative impacts on photosynthetic pigments in maize plants under Zinc (Zn) toxicity. Aust J Crop Sci 9:901Google Scholar
  16. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9.  https://doi.org/10.1016/s0168-9452(98)00025-9 CrossRefGoogle Scholar
  17. Epstein E (1999) Silicon. Annu Rev Plant Physiol 50:641–664.  https://doi.org/10.1146/annurev.arplant.50.1.641 CrossRefGoogle Scholar
  18. Fahad S et al (2014) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404.  https://doi.org/10.1007/s10725-014-0013-y CrossRefGoogle Scholar
  19. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25.  https://doi.org/10.1007/bf00386001 CrossRefGoogle Scholar
  20. Ghassemi-Golezani K, Lotfi R (2015) The impact of salicylic acid and silicon on chlorophyll a fluorescence in mung bean under salt stress. Russ J Plant Physiol 62:611–616.  https://doi.org/10.1134/s1021443715040081 CrossRefGoogle Scholar
  21. Ghassemi-Golezani K, Lotfi R, Najafi N (2015) Some physiological responses of mungbean to salicylic acid and silicon under salt stress. Adv Biores 6(4):07–13Google Scholar
  22. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307.  https://doi.org/10.1007/bf02374789 CrossRefGoogle Scholar
  23. Guerriero G, Hausman J-F, Legay S (2016) Silicon and the plant extracellular matrix. Front Plant Sci 7:463. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4828433/
  24. Habibi G, Hajiboland R (2013) Alleviation of drought stress by silicon supplementation in pistachio (Pistacia vera L.) plants. Folia Horticulturae 25:21–29CrossRefGoogle Scholar
  25. Haghighi M, Pessarakli M (2013) Influence of silicon and nano-silicon on salinity tolerance of cherry tomatoes (Solanum lycopersicum L.) at early growth stage. Sci Hort 161:111–117.  https://doi.org/10.1016/j.scienta.2013.06.034 CrossRefGoogle Scholar
  26. Hattori T, Inanaga S, Araki H, An P, Morita S, Luxova M, Lux A (2005) Application of silicon enhanced drought tolerance in Sorghum bicolor. Physiol Plant 123:459–466.  https://doi.org/10.1111/j.1399-3054.2005.00481.x CrossRefGoogle Scholar
  27. He C et al (2013) Evidence for ‘silicon’ within the cell walls of suspension-cultured rice cells. New Phytol 200:700–709.  https://doi.org/10.1111/nph.12401 CrossRefGoogle Scholar
  28. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125:189–198.  https://doi.org/10.1016/0003-9861(68)90654-1 CrossRefGoogle Scholar
  29. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334.  https://doi.org/10.1139/b79-163 CrossRefGoogle Scholar
  30. Kao W-Y, Tsai T-T, Tsai H-C, Shih C-N (2006) Response of three glycine species to salt stress. Environ Exp Bot 56:120–125.  https://doi.org/10.1016/j.envexpbot.2005.01.009 CrossRefGoogle Scholar
  31. Kariola T, Brader G, Helenius E, Li J, Heino P, Palva ET (2006) Early responsive to dehydration 15 a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiol 142:1559–1573.  https://doi.org/10.1104/pp.106.086223 CrossRefGoogle Scholar
  32. Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218.  https://doi.org/10.1016/j.niox.2012.07.005 CrossRefGoogle Scholar
  33. Khoshgoftarmanesh AH, Khodarahmi S, Haghighi M (2013) Effect of silicon nutrition on lipid peroxidation and antioxidant response of cucumber plants exposed to salinity stress. Arch Agron Soil Sci 60:639–653.  https://doi.org/10.1080/03650340.2013.822487 CrossRefGoogle Scholar
  34. Kim E-J, Bu S-Y, Sung M-K, Kang M-H, Choi M-K (2013) Analysis of antioxidant and anti-inflammatory activity of silicon in Murine macrophages. Biol Trace Elemt Res 156:329–337CrossRefGoogle Scholar
  35. Liang Y (1998) Effect of silicon on leaf ultrastructure, chlorophyll content and photosynthetic activity of barley under salt stress. Pedosphere 8:289–296Google Scholar
  36. Liang Y, Chen Q, Liu Q, Zhang Q, Ding R (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(10):1157–1164CrossRefGoogle Scholar
  37. Liu P, Yin L, Deng X, Wang S, Tanaka K, 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.  https://doi.org/10.1093/jxb/eru220 CrossRefGoogle Scholar
  38. Luck H (1974) Catalases. In: Czok R (ed) Methods of enzymatic analysis. Academic Press, New YorkGoogle Scholar
  39. Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397.  https://doi.org/10.1016/j.tplants.2006.06.007 CrossRefGoogle Scholar
  40. Maghsoudi K, Emam Y, Ashraf M (2015) Influence of foliar application of silicon on chlorophyll fluorescence, photosynthetic pigments, and growth in water-stressed wheat cultivars differing in drought tolerance. Turk J Botany 39:625–634Google Scholar
  41. Maghsoudi K, Emam Y, Pessarakli M (2016) Effect of silicon on photosynthetic gas exchange, photosynthetic pigments, cell membrane stability and relative water content of different wheat cultivars under drought stress conditions. J Plant Nutr 39:1001–1015.  https://doi.org/10.1080/01904167.2015.1109108 CrossRefGoogle Scholar
  42. Mahmood S et al. (2016) Plant growth promoting rhizobacteria and silicon synergistically enhance salinity tolerance of mung bean. Front Plant Sci 7  https://doi.org/10.3389/fpls.2016.00876
  43. Manai J, Kalai T, Gouia H, Corpas FJ (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr.  https://doi.org/10.4067/s0718-95162014005000034 Google Scholar
  44. Matoh T, Kairusmee P, Takahashi E (1986) Salt-induced damage to rice plants and alleviation effect of silicate. Soil Sci Plant Nutr 32:295–304.  https://doi.org/10.1080/00380768.1986.10557506 CrossRefGoogle Scholar
  45. Ming DF, Pei ZF, Naeem MS, Gong HJ, Zhou WJ (2011) Silicon alleviates PEG-induced water-deficit stress in upland rice seedlings by enhancing osmotic adjustment. J Agron Crop Sci 198:14–26.  https://doi.org/10.1111/j.1439-037x.2011.00486.x CrossRefGoogle Scholar
  46. Moussa HR (2006) Influence of exogenous application of silicon on physiological response of salt-stressed maize (Zea mays L.). Int J Agric Biol 8:293–297Google Scholar
  47. Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev 82:371–406.  https://doi.org/10.1007/s12229-016-9173-y CrossRefGoogle Scholar
  48. Muneer S, Jeong BR (2015) Proteomic analysis of salt-stress responsive proteins in roots of tomato (Solanum lycopersicumL.) plants towards silicon efficiency. Plant Growth Regul 77:133–146.  https://doi.org/10.1007/s10725-015-0045-y CrossRefGoogle Scholar
  49. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043.  https://doi.org/10.1093/jxb/erj100 CrossRefGoogle Scholar
  50. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880.  https://doi.org/10.1093/oxfordjournals.pcp.a076232 Google Scholar
  51. Nasir Khan M, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2009) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132.  https://doi.org/10.1007/s11738-009-0387-z CrossRefGoogle Scholar
  52. Parveen N, Ashraf M (2010) Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays L.) cultivars grown hydroponically. Pak J Bot 42:1675–1684Google Scholar
  53. Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050.  https://doi.org/10.1007/s11738-012-1142-4 CrossRefGoogle Scholar
  54. Rios JJ, Martínez-Ballesta MC, Ruiz JM, Blasco B, Carvajal M (2017) Silicon-mediated improvement in plant salinity tolerance: the role of aquaporins. Front Plant Sci 8:948.  https://doi.org/10.3389/fpls.2017.00948 CrossRefGoogle Scholar
  55. Rosenqvist E, van Kooten O (2003) Chlorophyll fluorescence: a general description and nomenclature. In: Jennifer RD, Peter M (eds) Practical applications of chlorophyll fluorescence in plant biology, vol 2. Springer, Boston, pp 31–78CrossRefGoogle Scholar
  56. Saha SR, Hossain MM, Rahman MM, Kuo CG, Abdullah S (2010) Effect of high temperature stress on the performance of twelve sweet pepper genotypes. Bangladesh J Agric Res 35  https://doi.org/10.3329/bjar.v35i3.6459
  57. Savvas D, Papastavrou D, Ntatsi G, Ropokis A, Olympios C, Hartmann H, Schwarz D (2009) Interactive effects of grafting and manganese supply on growth, yield, and nutrient uptake by tomato. HortScience 44:1978–1982CrossRefGoogle Scholar
  58. Shi H et al (2014) The Cysteine2/Histidine2-Type transcription factor ZINC FINGER OF Arabidopsis Thaliana 6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-REPEAT-BINDING FACTOR genes in Arabidopsis. Plant Physiol 165:1367–1379.  https://doi.org/10.1104/pp.114.242404 CrossRefGoogle Scholar
  59. Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H (2016) Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front Plant Sci 7  https://doi.org/10.3389/fpls.2016.00196
  60. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260.  https://doi.org/10.1104/pp.53.2.258 CrossRefGoogle Scholar
  61. Tahir MA, Aziz T, Farooq M, Sarwar G (2012) Silicon-induced changes in growth, ionic composition, water relations, chlorophyll contents and membrane permeability in two salt-stressed wheat genotypes. Arch Agron Soil Sci 58:247–256.  https://doi.org/10.1080/03650340.2010.518959 CrossRefGoogle Scholar
  62. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194.  https://doi.org/10.1046/j.1365-313x.1997.11061187.x CrossRefGoogle Scholar
  63. Tripathi AK, Pareek A, Sopory SK, Singla-Pareek SL (2012) Narrowing down the targets for yield improvement in rice under normal and abiotic stress conditions via expression profiling of yield-related genes. Rice 5:37.  https://doi.org/10.1186/1939-8433-5-37 CrossRefGoogle Scholar
  64. Tuna AL, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B (2007) The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environ Exp Bot 59:173–178.  https://doi.org/10.1016/j.envexpbot.2005.12.007 CrossRefGoogle Scholar
  65. van Rossum MWPC., Alberda M, van der Plas LHW (1997) Role of oxidative damage in tulip bulb scale micropropagation. Plant Sci 130:207–216.  https://doi.org/10.1016/s0168-9452(97)00215-x CrossRefGoogle Scholar
  66. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66.  https://doi.org/10.1016/s0168-9452(99)00197-1 CrossRefGoogle Scholar
  67. Wang S, Liu P, Chen D, Yin L, Li H, Deng X (2015) Silicon enhanced salt tolerance by improving the root water uptake and decreasing the ion toxicity in cucumber. Front Plant Sci 6  https://doi.org/10.3389/fpls.2015.00759
  68. Wang Y, Qu T, Zhao X, Tang X, Xiao H, Tang X (2016) A comparative study of the photosynthetic capacity in two green tide macroalgae using chlorophyll fluorescence. SpringerPlus 5:775. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4912542/
  69. Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059.  https://doi.org/10.1080/00103628209367332 CrossRefGoogle Scholar
  70. Yeo A (1998) Predicting the interaction between the effects of salinity and climate change on crop plants. Sci Hort 78:159–174.  https://doi.org/10.1016/s0304-4238(98)00193-9 CrossRefGoogle Scholar
  71. Yeo A, Flowers S, Rao G, Welfare K, Senanayake N, Flowers T (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 22:559–565CrossRefGoogle Scholar
  72. Zheng F, Zhao F, Qiu B, Ouyang Y, Wu F, Zhang G (2011) Alleviation of chromium toxicity by silicon addition in rice plants. Agri Sci China 10(8):1188–1196.  https://doi.org/10.1016/S1671-2927(11)60109-0 CrossRefGoogle Scholar
  73. Zhu Y, Gong H (2013) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472.  https://doi.org/10.1007/s13593-013-0194-1 CrossRefGoogle Scholar
  74. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533.  https://doi.org/10.1016/j.plantsci.2004.04.020 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Botany and Microbiology Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  2. 2.Department of BotanyS.P. CollegeSrinagarIndia
  3. 3.Department of BotanyGovt PG College RajouriRajouriIndia
  4. 4.Biology Department, College of Science and HumanitiesPrince Sattam bin Abdulaziz University (PSAU)AlkharjKingdom of Saudi Arabia
  5. 5.National Research Centre on Plant BiotechnologyNew DelhiIndia
  6. 6.College of Agronomy, Faculty of AgricultureUniversity of SargodhaSargodhaPakistan

Personalised recommendations