Skip to main content
Springer Nature Link
Log in

The importance of utilizing nitrate (NO3−) over ammonium (NH4+) as nitrogen source during detoxification of exogenous thiocyanate (SCN-) in Oryza sativa

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Thiocyanate (SCN−) is a nitrogen-containing pollutant, which can be involved in the nitrogen (N) cycle and interferes with plant growth. The current study highlights a new insight into the N (nitrate [NO3-] and ammonium [NH4+]) utilization ways in rice seedlings under SCN− exposure to clarify the interactive effect on uptake and assimilation between these N-containing chemicals. Phenotypically, relative growth rates (RGR) of NO3−-fed seedlings were significantly higher than NH4+-fed rice seedlings at the same SCN− concentration. Both N fertilizations have no significant influence on SCN− content and its assimilation in rice seedlings. However, significant accumulation of NO3− and NH4+ were detected in shoots prior to roots under SCN− stress. Enzymatic assay and mRNA analysis showed that the carbonyl sulfide (COS) pathway of SCN− degradation occurred in both roots and shoots of NO3−-fed seedlings but only evident in roots of NH4+-fed seedlings. Moreover, the effect of SCN− on the activity of nitrate reductase (NR), glutamine synthetase (GS), and glutamate synthase (GOGAT) was negligible in NO3−-fed seedlings, while GOGAT activity was significantly inhibited in shoots of NH4+-fed seedlings. Nitrogen use efficiency (NUE) estimation provided positive evidence in utilizing NO3− over NH4+ as the main N source to support rice seedling growth during detoxification of exogenous SCN−. Overall, SCN− pollution has unexpectedly changed the rice preference for N source which shifted from NH4+ to NO3−, suggesting that the interactions of SCN− with different N sources in terms of uptake and assimilation in rice plants should not be overlooked, especially at the plant N nutritional level.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Data availability

The datasets supporting the conclusions of this article can be obtained from the corresponding author on reasonable request.

References

  • Biase A, Wei V, Kowalski MS, Bratty M, Hildebrand M, Jabari P, Devlin TR, Oleszkiewicz JA (2020) Ammonia, thiocyanate, and cyanate removal in an aerobic up-flow submerged attached growth reactor treating gold mine wastewater. Chemosphere 243:125395

    Google Scholar 

  • Boening DW, Chew CM (1999) A critical review: General toxicity and environmental fate of three aqueous cyanide ions and associated ligands. Water Air Soil Pollut 109:67–79

    CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    CAS  Google Scholar 

  • Cai HM, Xiao JH, Zhang QF, Lian XM (2010) Co-suppressed glutamine synthetase2 gene modifies nitrogen metabolism and plant growth in rice. Chin Sci Bull 55:876–886

    Google Scholar 

  • Chanh TT, Tsutsumi M, Kurihara K (1981) Comparative-study on the response of Indica and Japonica rice plants to ammonium and nitrate nitrogen. Soil Sci Plant Nutr 27:83–92

    Google Scholar 

  • Ebbs SD, Piccinin RC, Goodger JQD, Kolev SD, Woodrow IE, Baker AJM (2008) Transport of ferrocyanide by two eucalypt species and sorghum. Inter J Phytorem 10:343–357

    CAS  Google Scholar 

  • Fan XR, Xie D, Chen JG, Lu HY, Xu YL, Ma C, Xu GH (2014) Over-expression of OsPTR6 in rice increased plant growth at different nitrogen supplies but decreased nitrogen use efficiency at high ammonium supply. Plant Sci 227:1–11

    CAS  Google Scholar 

  • Fraisier V, Gojon A, Tillard P, Daniel-Vedele F (2000) Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source. Plant J 23:489–496

    CAS  Google Scholar 

  • Gajewska E, Sklodowska M (2009) Nickel-induced changes in nitrogen metabolism in wheat shoots. J Plant Physiol 166:1034–1044

    CAS  Google Scholar 

  • Gould WD, King M, Mohapatra BR, Cameron RA, Kapoor A, Koren DW (2012) A critical review on destruction of thiocyanate in mining effluents. Miner Eng 34:38–47

    Google Scholar 

  • Hachiya T, Noguchi K (2011) Integrative response of plant mitochondrial electron transport chain to nitrogen source. Plant Cell Rep 30:195–204

    CAS  Google Scholar 

  • Han M, Wong JL, Su T, Beatty PH, Good AG (2016) Identification of nitrogen use efficiency genes in barley: searching for QTLs controlling complex physiological traits. Front Plant Sci 7:1587

    Google Scholar 

  • Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of Macronutrients. In: Marschner P (ed) Marschner’s Mineral nutrition of higher plants, 3rd edn. Academic Press, San Diego, pp 135–189

    Google Scholar 

  • Ho CH, Tsay YF (2010) Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13:604–610

    CAS  Google Scholar 

  • Hou WF, Xue XX, Li XK, Khan MR, Yan JY, Ren T, Cong RH, Lu J (2019) Interactive effects of nitrogen and potassium on: grain yield, nitrogen uptake and nitrogen use efficiency of rice in low potassium fertility soil in China. Field Crop Res 236:14–23

    Google Scholar 

  • Hussain S, Yin HQ, Peng SB, Khan FA, Khan F, Sameeullah M, Hussain HA, Huang JL, Cui KH, Nie LX (2016) Comparative transcriptional profiling of primed and non-primed rice seedlings under submergence stress. Front Plant Sci 7:1125

    Google Scholar 

  • Islam MS (2019) Sensing and uptake of nitrogen in rice plant: a molecular view. Rice Sci 26:343–355

    Google Scholar 

  • Jeong YS, Chung JS (2006) Biodegradation of thiocyanate in biofilm reactor using fluidized-carriers. Process Biochem 41:701–707

    CAS  Google Scholar 

  • Kant S (2018) Understanding nitrate uptake, signaling and remobilisation for improving plant nitrogen use efficiency. Semin Cell Dev Biol 74:89–96

    CAS  Google Scholar 

  • Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509

    CAS  Google Scholar 

  • Katz U, Lau KR, Ramos MMP, Ellory JC (1982) Thiocyanate transport across fish intestine (Pleuronectes platessa). J Membr Biol 66:9–14

    CAS  Google Scholar 

  • Li H, Hu B, Wang W, Zhang ZH, Liang Y, Gao XK, Li P, Liu YQ, Zhang LH, Chu CC (2016) Identification of microRNAs in rice root in response to nitrate and ammonium. J Genet Genomics 43:651–661

    Google Scholar 

  • Lin YJ, Yu XZ, Li YH, Yang L (2020) Inhibition of the mitochondrial respiratory components (Complex I and Complex III) as stimuli to induce oxidative damage in Oryza sativa L. under thiocyanate exposure. Chemosphere 243:125472

    CAS  Google Scholar 

  • Ling QL, Feng YX, Lu CJ, Lin YJ, Yu XZ (2021) Genetic variation and gene expression of anthocyanin synthesis and transport related enzymes in Oryza sativa against thiocyanate. Plant Physiol Biochem 160:18–26

    CAS  Google Scholar 

  • Marchi L, Degola F, Polverini E, Terce-Laforgue T, Dubois F, Hirel B, Restivo FM (2013) Glutamate dehydrogenase isoenzyme 3 (GDH3) of Arabidopsis thaliana is regulated by a combined effect of nitrogen and cytokinin. Plant Physiol Biochem 73:368–374

    CAS  Google Scholar 

  • Marchi L, Polverini E, Degola F, Baruffini E, Restivo FM (2014) Glutamate dehydrogenase isoenzyme 3 (GDH3) of Arabidopsis thaliana is less thermostable than GDH-1 and GDH2 isoenzymes. Plant Physiol Biochem 83:225–231

    CAS  Google Scholar 

  • Mactavish RM, Cohen RA (2017) Water column ammonium concentration and salinity influence nitrogen uptake and growth of Spartina alterniflora. J Exp Mar Biol Ecol 488:52–59

    CAS  Google Scholar 

  • Pan JX, Wei CH, Fu BB, Ma JD, Preis S, Wu HZ, Zhu S (2018) Simultaneous nitrite and ammonium production in an autotrophic partial denitrification and ammonification of wastewaters containing thiocyanate. Bioresour Technol 252:20–27

    CAS  Google Scholar 

  • Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. Proc Natl Acad Sci U S A 105:4524–4529

    CAS  Google Scholar 

  • Raper E, Stephenson T, Fisher R, Anderson DR, Soares A (2019) Characterisation of thiocyanate degradation in a mixed culture activated sludge process treating coke wastewater. Bioresour Technol 288:121524

    CAS  Google Scholar 

  • Rossinioliva S, Abreu MM, Santos ES, Leidi EO (2020) Soil-plant system and potential human health risk of Chinese cabbage and oregano growing in soils from Mn- and Fe-abandoned mines: microcosm assay. Environ Geochem Health 42:4073–4086

    CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    CAS  Google Scholar 

  • Sun L, Ma Y, Li B, Xiao C, Xiong Z (2018) Nitrogen fertilizer in combination with an ameliorant mitigated yield-scaled greenhouse gas emissions from a coastal saline rice field in southeastern china. Environ Sci Pollut Res 25(16):15896–15908

    CAS  Google Scholar 

  • Takayanagi S, Takagi Y, Araki R, Hasegawa H (2011) High-affinity nitrate uptake by rice (Oryza sativa) coleoptiles. J Plant Res 124:305–309

    CAS  Google Scholar 

  • Tang DD, Liu MY, Zhang QF, Ma LF, Shi YZ, Ruan JY (2020) Preferential assimilation of NH4+ over NO3- in tea plant associated with genes involved in nitrogen transportation, utilization and catechins biosynthesis. Plant Sci 291:110369

    CAS  Google Scholar 

  • Van Eerd LL, Hoagland RE, Zablotowicz RM, Hall JC (2003) Pesticide metabolism in plants and microorganisms. Weed Sci 51:472–495

    Google Scholar 

  • Wang YM, Wang P, Hao XZ, Zhou DM, Li JZ (2017) Effect of different nitrogen forms on the toxicity of Zn in wheat seedling root: a modeling analysis. Environ Sci Pollut Res 24(2017):18896–18906

    CAS  Google Scholar 

  • Wongkiew S, Hu Z, Chandran K, Lee JW, Khanal SK (2017) Nitrogen transformations in aquaponic systems: A review. Aquac Eng 76:9–19

    Google Scholar 

  • Xie HL, Jiang RF, Zhang FS, Mcgrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318(1-2):205–215

    CAS  Google Scholar 

  • Xiong ZT, Liu C, Geng B (2006) Phyotoxic effects of copper on nitrogen metabolism and plant growth in Brassica pekinensis Rupr. Ecotoxicol Environ Saf 64:273–280

    CAS  Google Scholar 

  • Xuan W, Beeckman T, Xu GH (2017) Plant nitrogen nutrition: Sensing and signaling. Curr Opin Plant Biol 39:57–65

    CAS  Google Scholar 

  • Yamaya T, Kusano M (2014) Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. J Exp Bot 65:5519–5525

    CAS  Google Scholar 

  • Yu XZ, Zhang FZ (2012) Activities of nitrate reductase and glutamine synthetase in rice seedlings during cyanide metabolism. J Hazard Mater 225-226:190–194

    CAS  Google Scholar 

  • Yu XZ, Zhang FZ, Li F (2012) Phytotoxicity of thiocyanate to rice seedlings. Bull Environ Contam Toxicol 88:703–706

    CAS  Google Scholar 

  • Yu XZ, Zhang FZ (2013) Effects of exogenous thiocyanate on mineral nutrients, antioxidative responses and free amino acids in rice seedlings. Ecotoxicology 22:752–760

    CAS  Google Scholar 

  • Yu XZ, Lin YJ, Shen PP, Zhang Q, Gupta DK (2019a) Molecular evidences on transport of thiocyanate into rice seedlings and assimilation by 13C and 15N labelling and gene expression analyses. Int Biodeterior Biodegrad 139:11–17

    CAS  Google Scholar 

  • Yu XZ, Lei SY, Lin YJ, Zhang Q (2019b) Interaction of cyanate uptake by rice seedlings with nitrate assimilation: gene expression analysis. Environ Sci Pollut Res 26:20208–20218

    CAS  Google Scholar 

  • Zar JH (1999) Biostatistical Analysis, 4rd edition. Prentice Hall, New Jersey. pp, 231–261.

  • Zhang Q, Feng YX, Yu XZ, Zhang H, Liang YP (2020) Effects of nitrogen fertilization on removal kinetics of thiocyanate (SCN−) in rice seedlings. Int J Environ Sci Technol 17:4291–4298

    CAS  Google Scholar 

  • Zhao XQ, Shi WM (2006) Expression analysis of the glutamine synthetase and glutamate synthase gene families in young rice (Oryza sativa) seedlings. Plant Sci 170:748–754

    CAS  Google Scholar 

  • Zhao XQ, Zhao SP, Shi WM (2008) Enhancement of NH4+ uptake by NO3- in relation to expression of nitrate-induced genes in rice (Oryza sativa) roots. Pedosphere 18:86–91

    CAS  Google Scholar 

  • Zhu FH, Huang MM, Jiao JJ, Zhuang P, Mao L, Zhang Y (2019) Environmental exposure to perchlorate, nitrate, and thiocyanate in relation to obesity: a population-based study. Environ Int 133:105191

    CAS  Google Scholar 

Download references

Acknowledgements

We wish to acknowledge Dr. Sarita Tiwari for assisting in language rectification.

Funding

This work was financially supported by the National Natural Science Foundation of China (No: 41761094).

Author information

Author notes

  1. Yu-Juan Lin and Yu-Xi Feng contributed equally to this work.

Authors and Affiliations

  1. College of Environmental Science & Engineering, Guilin University of Technology, Guilin, 541004, People’s Republic of China

    Yu-Juan Lin, Yu-Xi Feng & Xiao-Zhang Yu

Authors
  1. Yu-Juan Lin
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Yu-Xi Feng
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Xiao-Zhang Yu
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

Conceptualization, methodology, supervision, writing-reviewing and editing, and funding acquisition, Xiao-Zhang Yu; investigation, data analysis, visualization, and software, Yu-Juan Lin; writing-original draft preparation and visualization, Yu-Xi Feng. All of the authors contributed to the final review of the manuscript.

Corresponding author

Correspondence to Xiao-Zhang Yu.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

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

Supplementary information

ESM 1

(DOC 2564 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, J., Feng, YX. & Yu, XZ. The importance of utilizing nitrate (NO3−) over ammonium (NH4+) as nitrogen source during detoxification of exogenous thiocyanate (SCN-) in Oryza sativa. Environ Sci Pollut Res 29, 5622–5633 (2022). https://doi.org/10.1007/s11356-021-15959-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15959-z

Keywords