Silicon Supplementation Alleviates Ammonium Toxicity in Sugar Beet (Beta vulgaris L.)

  • Dilier Olivera ViciedoEmail author
  • Renato de Mello Prado
  • Rodolfo Lizcano Toledo
  • Luiz Claudio Nascimento dos Santos
  • Alexander Calero Hurtado
  • Luke Leroy Theodore Nedd
  • Leonides Castellanos Gonzalez
Research Article


The purpose of this study is to evaluate the relationship between Si and NH4+ toxicity in the context of the nutrition, physiology, and production of sugar beet grown using hydroponics. We hypothesized that NH4+ affects the physiology of the plant, accumulation of nutrients, and dry matter, with the possibility for Si to mitigate this toxicity. The experimental design used was completely randomized, in a factorial scheme of 2 × 5, corresponding with the absence and presence of Si (2 mmol L−1) and five concentrations of NH4+ with four replicates. The following series of physiological evaluations were carried out: photosynthesis, stomatal conductance, transpiration, with the use of an infrared gas analyzer (LICOR, Inc., LI-6400), the dry biomass, N and Si accumulation, and Si use efficiency in the roots. Accumulation of N and photosynthesis in the leaves was higher in the presence of Si. An increase of NH4+ increased transpiration, especially in the plants cultivated without the incorporation of Si. Stomatal conductance was lower in the presence of Si. Dry matter was reduced when plants were exposed to higher concentrations of NH4+, showing a greater reduction in the root than in the aerial part. The use of NH4+ equal to or higher than 15 mmol L−1 damaged the photosynthesis. Transpiration and stomatal conductance were less affected in the presence of Si and in the accumulation of N and Si in the roots. Dry matter was reduced when plants were exposed to higher concentrations of NH4+, and this effect was mitigated in the presence of Si.


Abiotic stress Ammoniacal nitrogen Beneficial element Vegetables 



The present work was conducted with the support from CNPq, Brazilian National Council for Scientific and Technological Development – Brazil, and TWAS, the Academy of Sciences for the Developing World.


This study was funded by CNPq, Brazilian National Council for Scientific and Technological Development – Brazil, and TWAS, the Academy of Sciences for the Developing World (Grant number, 304201/2014-6).

Compliance with Ethical Standards

Competing Interests

The authors declared that they have no competing interests.


  1. Adrees M, Ali S, Rizwan M, Rehman MZ, Ibrahim M, Abbas F, Farid M, Qayyum MK, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197CrossRefGoogle Scholar
  2. Bakhat HF, Bibi N, Zia Z, Abbas S, Hammad HM, Fahad S, Ashraf MR, Shah GM, Rabbani F, Saeed S (2018) Silicon mitigates biotic stresses in crop plants: a review. Crop Prot 104:21–34CrossRefGoogle Scholar
  3. Barbosa JC, Maldonado JRW (2014) AgroEstat - system for statistical analysis of agronomic trials - Version Faculty of Agrarian and Veterinary Sciences, Sao Paulo State University, JaboticabalGoogle Scholar
  4. Barreto RF, Júnior AS, Maggio MA, de Mello Prado R (2017) Silicon alleviates ammonium toxicity in cauliflower and in broccoli. Sci Hortic 225:743–750CrossRefGoogle Scholar
  5. Barreto RF, Prado RM, Leal AJF, Troleis MJB, Junior GS, Monteiro CC, Carvalho RF (2016) Mitigation of ammonium toxicity by silicon in tomato depends on the ammonium concentration. Acta Agric Scand Sect B Soil Plant Sci 66:483–488Google Scholar
  6. Bataglia OC, Furlani AMC, Teixeira JPF, Furlani PR, Gallo JR (1983) Métodos de análise química de plantas. Campinas, Instituto Agronômico. 48p. Boletim técnico, 78Google Scholar
  7. Campos CNS, de Mello Prado R, Caione G, de Lima Neto AJ, Mingotte FLC (2016) Silicon and excess ammonium and nitrate in cucumber plants. Afr J Agric Res 11:276–283CrossRefGoogle Scholar
  8. Cooke J, Leishman MR (2016) Consistent alleviation of abiotic stress with silicon addition: a meta-analysis. Funct Ecol 30:1340–1357CrossRefGoogle Scholar
  9. Bittsánszky A, Pilinszk K, Gyulai G, Komives T (2015) Overcoming ammonium toxicity. Plant Sci 231:184–190CrossRefGoogle Scholar
  10. Bybordi A (2010) Influence of NO3:NH4 ratios and silicon on growth, nitrate reductase activity and fatty acid composition of canola under saline conditions. Afr J Agric Res 5:1984–1992Google Scholar
  11. Campos CNS (2013) Silício e excesso de amônio e de nitrato em plantas de cana-de açúcar e de pepino. Thesis de maestrado, Universidad Estadual Paulista, UNESP, Jaboticabal, Sao Paulo, Brasil, 60 pGoogle Scholar
  12. Camargo MS, Bezerra BLK, Vitti AC, Silva MA, Oliveira AL (2017) Silicon fertilization reduces the deleterious effects of water deficit in sugarcane. J Soil Sci Plant Nutr 17:99–111Google Scholar
  13. Cruz C, Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Bio A, Martins-Loução MA, Moran JF (2011) Intra-specific variation in pea responses to ammonium nutrition leads to different degrees of tolerance. Environ Exp Bot 70:233–243CrossRefGoogle Scholar
  14. Din M, Qasim M, Alam M (2007) Effect of different levels of N, P and K on the growth and yield of cabbage. J Agric Res 45:171–176Google Scholar
  15. Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci 91:11–17CrossRefGoogle Scholar
  16. Fageria NK, Baligar VC (2005) Enhancing nitrogen use efficiency in crop plants. Adv Agron 88:97–185CrossRefGoogle Scholar
  17. Ferreira Barreto R, Rodrigues Cruz FJ, Aparecido Gaion L, de Mello Prado R, Falleiros Carvalho R (2018) Accompanying ions of ammonium sources and nitrate: ammonium ratios in tomato plants. J Plant Nutr Soil Sci 181:382–387CrossRefGoogle Scholar
  18. Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123:521–530CrossRefGoogle Scholar
  19. Filgueira FAR (2000) Novo manual de Olericultura: Agrotecnologia moderna na produção e comercialização de hortaliças. Viçosa: UFV. MG: Editora UFVGoogle Scholar
  20. Frew A, Weston LA, Reynolds OL, Gurr GM (2018) The role of silicon in plant biology: a paradigm shift in research approaches. Ann Bot 121:1265–1273CrossRefGoogle Scholar
  21. Gao Q, Wang Y, Lu X (2014) Effects of exogenous silicon on physiological characteristics of cucumber seedlings under ammonium stress. J Appl Ecol 25:1395–1400Google Scholar
  22. Guimarães MMC, Cairo PAR, Neves OSC (2014) Crescimento de Eucalyptus urophylla em meio hidropônico com diferentes proporções de nitrato e amônio. Floresta Ambient 21:52–61CrossRefGoogle Scholar
  23. Guntzer F, Keller C, Meunier JD (2012) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32:201–213CrossRefGoogle Scholar
  24. Hachiya T, Watanabe CK, Fujimoto M, Ishikawa T, Takahara K, Kawai-Yamada M, Noguchi K (2012) Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots. Plant Cell Physiol 53:577–591CrossRefGoogle Scholar
  25. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387CrossRefGoogle Scholar
  26. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. In: Circular. California Agricultural Experiment Station, Vol 347. pp. 22–32Google Scholar
  27. Horchani F, Hajri R, Aschi-Smiti S (2011) Is the sensitivity to ammonium nutrition related to nitrogen accumulation? Curr Bot 2:18–22Google Scholar
  28. Huang L, Lu Y, Gao X, Du G, Ma X, Liu M, Chen Y (2013) Ammonium-induced oxidative stress on plant growth and antioxidative response of duckweed (Lemna minor L.). Ecol Eng 58:355–362CrossRefGoogle Scholar
  29. Iqbal MA, Saleem AM (2015) Sugar beet potential to beat sugarcane as a sugar crop in Pakistan. Am Eurasian J Agric Environ Sci 15:36–44Google Scholar
  30. Ishikawa S, Ando S, Sakaigaichi T, Terajima Y, Matsuoka M (2009) Effects of high nitrogen application on the dry matter yield, nitrogen content and nitrate-N concentration of sugarcane. Soil Sci Plant Nutr 55:485–495CrossRefGoogle Scholar
  31. Kochanová Z, Jašková K, Sedláková B, Luxová M (2014) Silicon improves salinity tolerance and affects ammonia assimilation in maize roots. Biologia 69:1164–1171CrossRefGoogle Scholar
  32. Kraska JE, Breitenbeck GA (2010) Simple, robust method for quantifying silicon in plant tissue. Commun Soil Sci Plant Anal 41:2075–2085CrossRefGoogle Scholar
  33. Liang Y, Nikolic M, Bélanger R, Gong H, Song A (2015) Silicon in agriculture. Springer, DordrechtCrossRefGoogle Scholar
  34. Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428CrossRefGoogle Scholar
  35. Liu H, Wang QQ, Yu MM, Zhang YY, Wu YB, Zhang HX (2008) Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na+/H+ antiporter gene, AtNHX3, accumulates more soluble sugar but less salt in storage roots. Plant Cell Environ 31:1325–1334CrossRefGoogle Scholar
  36. Liu JJ, Lin SH, Xu PL, Wang XJ, Bai JG (2009) Effects of exogenous silicon on the activities of antioxidant enzymes and lipid peroxidation in chilling-stressed cucumber leaves. Agric Sci China 8:1075–1086CrossRefGoogle Scholar
  37. Mateos-Naranjo E, Andrades-Moreno L, Davy AJ (2013) Silicon alleviates deleterious effects of high salinity on the halophytic grass Spartina densiflora. Plant Physiol Biochem 63:115–121CrossRefGoogle Scholar
  38. Nasraoui-Hajaji A, Gouia H (2014) Photosynthesis sensitivity to NH4 +-N change with nitrogen fertilizer type. Plant Soil Environ 60:274–279CrossRefGoogle Scholar
  39. Olivera VD, de Mello Prado R, Lizcano Toledo R, Nascimento dos Santos LC, Peña Calzada K (2017) Response of radish seedlings (Raphanus sativus L.) to different concentrations of ammoniacal nitrogen in absence and presence of silicon. Agron Colomb 35:198–204CrossRefGoogle Scholar
  40. Oliveira AP, Moura MF, Nogueira DH, Chagas NG, Braz MSS, Oliveira MRT, Barbosa JA (2006) Produção de raízes de batata-doce em função do uso de doses de N aplicadas no solo e via foliar. Hortic Bras 24:279–282CrossRefGoogle Scholar
  41. Prado RM (2008) Nitrogênio. In: Nutrição de plantas. Jaboticabal: Editora UNESP, cap. 4:83–120Google Scholar
  42. Resende GM, Cordeiro GG (2007) Uso da água salina e condicionador de solo na produtividade de beterraba e cenoura no semi-árido do Submédio São Francisco. Embrapa Semiárido-Comunicado Técnico (INFOTECA-E). 4p. Comunicado Técnico 128Google Scholar
  43. Sandhya K, Prakash NB, Meunier JD (2018) Diatomaceous earth as source of silicon on the growth and yield of rice in contrasted soils of southern India. J Soil Sci Plant Nutr 18:344–360Google Scholar
  44. Sarasketa A, González-Moro MB, González-Murua C, Marino D (2014) Exploring ammonium tolerance in a large panel of Arabidopsis thaliana natural accessions. J Exp Bot 65:6023–6033CrossRefGoogle Scholar
  45. Song AL, Li P, Li ZJ, Fan FL, Liang YC (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:e113782CrossRefGoogle Scholar
  46. Souza RD, Fontanetti A, Fiorini CVA, Almeida KD (2003) Cultura da beterraba: Cultivo convencional e cultivo orgânico. UFLA, Lavras 37pGoogle Scholar
  47. Shaw B, Thomas TH, Cooke DT (2002) Responses of sugar beet (Beta vulgaris L.) to drought and nutrient deficiency stress. Plant Growth Regul 37:77–83CrossRefGoogle Scholar
  48. Vaculíková M, Vaculík M, Šimková L, Fialová I, Kochanová Z, Sedláková B, Luxová M (2014) Influence of silicon on maize roots exposed to antimony—growth and antioxidative response. Plant Physiol Biochem 83:279–284Google Scholar
  49. Zanin L, Zamboni A, Monte R, Tomasi N, Varanini Z, Cesco S, Pinton R (2015) Transcriptomic analysis highlights reciprocal interactions of urea and nitrate for nitrogen acquisition by maize roots. Plant Cell Physiol 56:532–548Google Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  • Dilier Olivera Viciedo
    • 1
    Email author
  • Renato de Mello Prado
    • 1
  • Rodolfo Lizcano Toledo
    • 2
  • Luiz Claudio Nascimento dos Santos
    • 1
  • Alexander Calero Hurtado
    • 1
  • Luke Leroy Theodore Nedd
    • 3
  • Leonides Castellanos Gonzalez
    • 4
  1. 1.School of Agricultural and Veterinarian SciencesSão Paulo State University (Unesp)JaboticabalBrazil
  2. 2.International Graduate SchoolUniversity of GranadaGranadaSpain
  3. 3.National Institute of Agricultural SciencesHavanaCuba
  4. 4.Faculty of Agricultural SciencesUniversity of PamplonaPamplonaColombia

Personalised recommendations