Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Impact of Exogenous Silicate Amendments on Nitrogen Metabolism in Wheat Seedlings Subjected to Arsenate Stress

Abstract

Purpose

We intended to investigate the response of arsenate on nitrogen metabolism in wheat seedlings and aimed to assess the efficacy of silicon amendments in modulating the metabolic disturbances caused by arsenate stress.

Methods

The nitrogen metabolism of wheat cultivated in different levels of arsenate with or without silicate in a medium supplemented with modified Hoagland’s solution for 21 days was studied. Experimental design was completely randomized with different arsenate concentrations (0, 25, 50 and 100 μM) with or without 5 mM silicate.

Results

Arsenate treatment decreased growth along with decline in nitrate (NO3) uptake and accumulation. Activities of nitrate reductase (NR), nitrite reductase (NiR), glutamine synthetase (GS) as well as glutamate synthase (GOGAT) were lowered in the test seedlings. Decline in nitrite (NO2) and amino acid contents were also evident along with an enhancement in the accumulation of toxic ammonia. Silicate supplementation under arsenate stress however, improved growth, repaired the arsenate-induced effects leading to an enhancement in nitrate (NO3) uptake and consequently improved nitrite (NO2) and amino acid contents as well. The total and soluble nitrogen contents were enhanced along with enhancements in activities of enzymes associated with nitrate metabolism while ammonia accumulation was lowered.

Conclusions

Results therefore, imply the involvement of exogenous silicon amendments in relieving the metabolic alterations in nitrogen metabolism caused by arsenate stress that enabled wheat seedlings to adapt under arsenate excess and eventually promoted plant growth.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M, Natasha (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59

  2. 2.

    Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum MF, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197

  3. 3.

    Azmat R, Khan N (2011) Nitrogen metabolism as a bioindicator of Cu stress in Vigna radiata. Pak J Bot 43:515–520

  4. 4.

    Basu A, Saha D, Saha R, Ghosh T, Saha B (2014) A review on sources, toxicity and remediation technologies for removing arsenic from drinking water. Res Chem Intermed 40(2):447–485

  5. 5.

    Canovas FM, Canton FR, Gallardo F, Garcia-Gutierrez A, De Vincente A (1991) Accumulation of glutamine synthetase during early development of maritime pine (Pinus pinaster) seedlings. Planta 185:372–378

  6. 6.

    Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80

  7. 7.

    Chaffei C, Gouia H, Ghorbel Mohamed H (2003) Nitrogen metabolism in tomato plants under cadmium stress. J Plant Nutr 26(8):1617–1634

  8. 8.

    Chen FL, Cullimore JV (1988) Two isoenzymes of NADH-dependent glutamate synthase in root nodules of Phaseolus vulgare L. purification, properties and activity changes during nodule development. Plant Physiol 88:1411–1417

  9. 9.

    Da silva AJ, Nascimento CW, Gouveia-Neto ADS, Silva Jr EA (2015) Effects of silicon on alleviating arsenic toxicity in maize plants. Rev Bras Ciênc Solo 39:289–296

  10. 10.

    Farooq MA, Islam A, Ali B, Najeeb U, Mao B, Gill RA, Yan G, Siddique KHM, Zhou W (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environ Exp Bot 132:42–52

  11. 11.

    Gangwar S, Singh VP (2011) Indole acetic acid differently changes growth and nitrogen metabolism in Pisum sativum L. seedlings under chromium (VI) phytotoxicity: implication of oxidative stress. Sci Hortic 129:321–328

  12. 12.

    Gao S, Liu KT, Chung TW, Chen T (2013) The effects of NaCl stress on Jatropha cotyledon growth and nitrogen metabolism. J Soil Sci Plant Nutr 13(1):99–113

  13. 13.

    Hageman RH, Reed AJ (1980) Nitrate reductase from higher plants. Methods Enzymol 69:270–280

  14. 14.

    Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to stress tolerance in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111

  15. 15.

    Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311

  16. 16.

    Jha AB, Dubey RS (2004) Arsenic exposure alters activity behaviour of key nitrogen assimilatory enzymes in growing rice plants. Plant Growth Regul 43:259–268

  17. 17.

    Kim YH, Khan AL, Kim DH, Lee SY, Kim KM, 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 14:1

  18. 18.

    Kusano M, Fukushima A, Redestig H, Saito K (2011) Metabolomic approaches toward understanding nitrogen metabolism in plants. J Exp Bot 62:1439–1453

  19. 19.

    Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77

  20. 20.

    Lee SK, Sohn EY, Hamayun M, Yoon JY, Lee IJ (2010) Effect of silicon on growth and salinity stress of soybean plant grown under hydroponic system. Agrofor Syst 80:333–340

  21. 21.

    Li N, Wang J, Song WY (2015) Arsenic uptake and translocation in plants. Plant Cell Physiol 0:1–10

  22. 22.

    Liang CG, Chen LP, Wang Y, Liu J, Xu GL, Li T (2011) High temperature at grain-filling stage affects nitrogen metabolism enzyme activities in grains and grain nutritional quality in rice. Rice Sci 18:210–216

  23. 23.

    Liang Y, Nikolic M, Bélanger R, Gong H, Song A (2015) Silicon in agriculture. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9978-2

  24. 24.

    Lowry OM, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

  25. 25.

    Ludewig U, Neuhäuser B, Dynowski M (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581:2301–2308

  26. 26.

    Luyckx M, Hausman JF, Lutts S, Guerriero G (2017) Silicon and plants: current knowledge and technological perspectives. Front Plant Sci 8:411

  27. 27.

    Maaroufi Dguimi H, Debouba M, Ghorbel MH, Gouia H (2009) Tissue-specific cadmium accumulation and its effects on nitrogen metabolism in tobacco (Nicotiana tabaccum, Bureley v. Fb9). C R Biol 332:58–68

  28. 28.

    Mallick S, Sinam G, Sinha S (2011) Study on arsenate tolerant and sensitive cultivars of Zea mays L. differential detoxification mechanism and effect on nutrients status. Ecotoxicol Environ Saf 74(5):1316–1324

  29. 29.

    Manivannan A, Ahn YK (2017) Silicon regulates potential genes involved in major physiological processes in plants to combat stress. Front Plant Sci 8:1346

  30. 30.

    Markovich O, Steiner E, Kouøil S, Tarkowski P, Aharoni A, Elbaum R (2017) Silicon promotes cytokinin biosynthesis and delays senescence in Arabidopsis and Sorghum. Plant Cell Environ 40:1189–1196. https://doi.org/10.1111/pce.12913

  31. 31.

    Martinez VD, Vucic EA, Becker-Santos DD, Gil L, Lam WL (2011) Arsenic exposure and the induction of human cancers. J Toxicol 2011:1–13

  32. 32.

    McCarty KM, Hanh HT, Kim KW (2011) Arsenic geochemistry and human health in South East Asia. Rev Environ Health 26(1):71–78

  33. 33.

    Mendez JM, Vega JM (1981) Purification and molecular properties of nitrite reductase from Anabaena sp. 7119. Physiol Plant 52(1):7–14. https://doi.org/10.1111/j.1399-3054.1981.tb06026.x

  34. 34.

    Nazmul Huda AKM, Haque MA, Zaman R, Swaraz AM, Kabir AH (2017) Silicon ameliorates chromium toxicity through phytochelatin-mediated vacuolar sequestration in the roots of Oryza sativa (L.). Int J Phytoremediation 19(3):246–253

  35. 35.

    Neto LB, Paiva ALS, Machado RD, Arenhart RA, Pinheiro MM (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40(10):373–386

  36. 36.

    Pontigo S, Godoy K, Jiménez H, Gutiérrez-Moraga A, Mora ML, Cartes P (2017) Silicon-mediated alleviation of aluminum toxicity by modulation of Al/Si uptake and antioxidant performance in ryegrass plants. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00642

  37. 37.

    Rastogi A, Tripathi DKT, Yadav S, Chauhan DK, Živčak M, Ghorbanpour M, El-Sheery NI, Brestic M (2019) Application of silicon nanoparticles in agriculture. Biotech 9:90

  38. 38.

    Rodrigues da Cruz FJ, Da Silva Lobato AK, Lobo da Costa RC, Dos Santos Lopes MJ, Borges Neves HK, De Oliveira Neto CF, Lima da Silva MH, Dos Santos Filho BG, De Lima Jr JA, Okumura RS (2011) Aluminum negative impact on nitrate reductase activity, nitrogen compounds and morphological parameters in sorghum plants. Aust J Crop Sci 5(6):641–645

  39. 39.

    Saha J, Majumder B, Mumtaz B, Biswas AK (2017) Arsenic induced oxidative stress and thiol metabolism in two cultivars of rice and its possible reversal by phosphate. Acta Physiol Plant 39:263

  40. 40.

    Sil P, Das P, Biswas AK (2018) Silicon induced mitigation of TCA cycle and GABA synthesis in arsenic stressed wheat (Triticum aestivum L.) seedlings. S Afr J Bot 119:340–352

  41. 41.

    Sil P, Das P, Biswas S, Mazumdar A, Biswas AK (2019) Modulation of photosynthetic parameters, sugar metabolism, polyamine and ion contents by silicon amendments in wheat (Triticum aestivum L.) seedlings exposed to arsenic. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-019-04896-7

  42. 42.

    Singh N, Ma LQ, Vu JC, Raj A (2009) Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns. Environ Pollut 157:2300–2305

  43. 43.

    Singh M, Singh VP, Dubey G, Prasad SM (2015) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicol Environ Saf 117:164–173

  44. 44.

    Singh AP, Dixit G, Kumar A, Mishra S, Singh PK, Dwivedi S, Trivedi PK, Chakrabarty D, Mallick S, Pandey V, Dhankher OP, Tripathi RD (2016) Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.). Front Plant Sci 6:1272

  45. 45.

    Skopelitis DS, Paranychianakis NV, Paschalidis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781

  46. 46.

    Snell FD, Snell CT (1949) Colorimetric methods of analysis. Van Nostrand, New York

  47. 47.

    Song A, Li P, Fan F, Li Z, Liang Y (2014) The effect of silicon on photosynthesis and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc stress. PLoS One 9:e113782

  48. 48.

    Song WY, Yang HC, Shao HB, Zheng AZ, Brestic M (2014) The alleviative effects of salicylic acid on the activities of catalase and superoxide dismutase in malting barley (Hordeum vulgare l.) seedling leaves stressed by heavy metals. Clean: Soil, Air, Water 42(1):88–97

  49. 49.

    Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2018) Phytohormone priming: regulator for heavy metal stress in plants. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9886-8

  50. 50.

    Tripathi DK, Singh VP, Prasad SM, Dubey NK, Chauhan DK, Rai AKV (2016) LIB spectroscopic and biochemical analysis to characterize lead toxicity alleviative nature of silicon in wheat (Triticum aestivum L.) seedling. J Photochem Photobiol B 154:89–98

  51. 51.

    Vogel AI (1961) Colorimetric estimation of nitrogen by Nessler’s reagent. In: a textbook of quantitative inorganic analysis. Langman and Green, India

  52. 52.

    Wang XP, Geng SJ, Ri YJ, Cao DH, Liu J, Shi DC, Yang CW (2011) Physiological responses and adaptive strategies of tomato plants to salt and alkali stresses. Sci Hortic 130:248–255

  53. 53.

    Wu X, Liu C, Qu C, Huang H, Liu X, Chen L, Su M, Hong F (2008) Influences of lead (II) chloride on the nitrogen metabolism of spinach. Biol Trace Elem Res 121:258–265

  54. 54.

    Zhang Y, Hu XH, Shi Y, Zou ZR, Yan F, Zhao YY, Zhang H, Zhao JZ (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline-alkaline stress. J Am Soc Hortic Sci 138(1):38–49

  55. 55.

    Zhang L, He X, Chen M, An R, An X, Li J (2014) Responses of nitrogen metabolism to copper stress in Luffa cylindrica roots. J Soil Sci Plant Nutr 14(3):616–624

  56. 56.

    Zhu YG, Geng CN, Tong YP, Smith SE, Smith FA (2006) Phosphate (Pi) and arsenate uptake by two wheat (Triticum aestivum) cultivars and their doubled haploid lines. Ann Bot 98(3):631–636

  57. 57.

    Zilli CG, Balestrasse KB, Yannarelli GG, Polizio AH, Santa- Cruz DM, Tomaro ML (2008) Heme oxygenase up-regulation under salt stress protects nitrogen metabolism in nodules of soybean plants. Environ Exp Bot 64:83–89

Download references

Acknowledgements

The authors are grateful to the University Grants Commission, New Delhi, India; for financial assistance and Centre of Advanced Study, Department of Botany, University of Calcutta, India for infrastructural facilities in completion of the work. The authors also acknowledge the assistance of Prof. Uttam Bandopadhyay, Department of Statistics, University of Calcutta, India for regression analysis.

Author information

Correspondence to Asok K. Biswas.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 18 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sil, P., Das, P. & Biswas, A.K. Impact of Exogenous Silicate Amendments on Nitrogen Metabolism in Wheat Seedlings Subjected to Arsenate Stress. Silicon 12, 535–545 (2020). https://doi.org/10.1007/s12633-019-00158-w

Download citation

Keywords

  • Arsenate
  • Growth
  • Nitrogen metabolism
  • Silicate
  • Wheat