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NO3/NH4+ ratios affect nutritional homeostasis and production of Tanzania guinea grass under Cu toxicity

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Abstract

Nitrogen (N) can alleviate metal toxicity. However, as of yet, there have been no studies showing the efficacy of NO3/NH4+ in mitigating Cu toxicity. The objective of this study was to evaluate the Cu toxicity on the nutritional and productive attributes of Panicum maximum cv. Tanzania as well as the role of NO3 and NH4+ ratios in nutritional homeostasis. The experiment was conducted using 3 × 4 factorial treatments arranged in a randomized complete block design with three replicates. The treatments were three NO3/NH4+ ratios (100/0, 70/30, and 50/50) and four Cu rates (0.3, 250, 500, and 1000 μmol L−1) in nutrient solution. Copper concentrations in the diagnostic leaves (DL) were highest in plants grown under 70/30 NO3/NH4+ ratios and a Cu rate of 1000 μmol L−1. In this combination, it was observed that DL had higher concentrations of NH4+, greater glutamine synthetase activity, lower chlorophyll concentration (SPAD value), and lower shoot dry mass, suggesting high disorders of nutritional homeostasis. Plants receiving N in the form of NO3 and 1000 Cu μmol L−1 showed that DL had lower concentrations of Cu, higher concentration of chlorophyll, higher NO3 concentration, higher nitrate reductase activity, and higher NO3 accumulation in the roots, suggesting a reduction in disorders of nutritional homeostasis. The disorders on mineral uptake, N assimilation, and biomass production caused by Cu toxicity are shown to be affected by NO3/NH4+ ratios, and N supply via NO3 allowed for better homeostasis of the forage grass.

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References

  • Bazihizina N, Colzi I, Giorni E, Mancuso S, Gonnelli C (2015) Photosynthesizing on metal excess: copper differently induced changes in various photosynthetic parameters in copper tolerant and sensitive Silene paradoxa L. populations. Plant Sci 232:67–76. https://doi.org/10.1016/j.plantsci.2014.12.015

    Article  CAS  Google Scholar 

  • Chen LM, Kao CH (1998) Relationship between ammonium accumulation and senescence of detached rice leaves caused by excess copper. Plant Soil 200:169–173. https://doi.org/10.1023/A:1004369518777

    Article  CAS  Google Scholar 

  • Cheng M, Wang P, Kopittke PM, Wang A, Sale PWG, Tang C (2016) Cadmium accumulation is enhanced by ammonium compared to nitrate in two hyperaccumulators, without affecting speciation. J Exp Bot 67:5041–5050

    Article  CAS  Google Scholar 

  • Costa MCG, Cunha IML, Jorge LAC, Araújo ICS (2014) Public-domain software for root image analysis. Rev. Bras. Ciência do Solo 38:1359–1366

    Article  Google Scholar 

  • Darnell RL, Hiss SA (2006) Uptake and assimilation of nitrate and iron in two vaccinium species as affected by external nitrate concentration. J Am Soc Hortic Sci 131:5–10

    CAS  Google Scholar 

  • Elliott WH (1952) Isolation of glutamine synthetase and glutamotransferase from green peas. J Biol Chem 201:661–672

    Google Scholar 

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Stamford, p 400

    Google Scholar 

  • Gilabel AP, Nogueirol RC, Garbo AI, Monteiro FA (2014) The role of sulfur in increasing guinea grass tolerance of copper phytotoxicity. Water Air Soil Pollut 225:1806–1816. https://doi.org/10.1007/s11270-013-1806-8

    Article  CAS  Google Scholar 

  • Hamlin RL, Barker AV (2006) Influence of ammonium and nitrate nutrition on plant growth and zinc accumulation by Indian mustard. J Plant Nutr 29:1523–1541. https://doi.org/10.1080/01904160600837709

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949

    Article  CAS  Google Scholar 

  • Heldt HW (2005) Plant biochemistry, 3rd edn. Elsevier, Amsterdam, p 630

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soils. California Agricultural Experimental Station, Berkeley, p 347

    Google Scholar 

  • Lavres Junior J, Santos Junior JDG, Monteiro FA (2010) Nitrate reductase activity and SPAD readings in leaf tissues of guinea grass submitted to nitrogen and potassium rates. Rev Bras Ciência do Solo 34:801–809. https://doi.org/10.1590/S0100-06832010000300022

    Article  Google Scholar 

  • Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646. https://doi.org/10.1105/tpc.110.075242

    Article  CAS  Google Scholar 

  • Mulder EG, Boxma R, Veen WLV (1969) The effect of molybdenum and nitrogen deficiencies on nitrate reduction in plant tissues. Plant Soil 10:335–355

    Article  Google Scholar 

  • Paulose B, Chhikara S, Coomey J, Jung H, Vatamaniuk O (2013) A γ-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25:4580–4595

    Article  CAS  Google Scholar 

  • Ramirez CO, Mora SI, Trejo J, Pantoja O (2011) PvAMT1;1, a highly selective ammonium transporter that functions as H+/NH4 + symporter. J Biol Chem 286:31113–31122. https://doi.org/10.1074/jbc.M111.261693

    Article  CAS  Google Scholar 

  • Sancenón V, Puig S, Mira H, Thiele DJ, Peñarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587. https://doi.org/10.1023/A:1022345507112

    Article  Google Scholar 

  • Santos JHS, De Bona FD, Monteiro FA (2013) Growth and productive responses of tropical grass Panicum maximum to nitrate and ammonium supply. Rev Bras Zootec 42:622–628. https://doi.org/10.1590/S1516-35982013000900003

    Article  Google Scholar 

  • Sarruge JR, Haag HP (1974) Chemical analysis in plants. ESALQ, Piracicaba, p 56 (in portuguese)

    Google Scholar 

  • SAS Institute (2008) SAS/STAT: Qualification tools user’s guide, version 9.2 Cary

  • Silveira CP, Monteiro FA (2010) Macronutrients concentrations in Tanzania guinea grass diagnostic leaves supplied with nitrogen and calcium rates. Rev Bras Zootec 39:736–745. https://doi.org/10.1590/S1516-35982010000400006 (in Portuguese)

    Article  Google Scholar 

  • Silveira CP, Monteiro FA (2011) Influence of nitrogen and calcium fertilizations on morphological and productive characteristics of Tanzania guineagrass roots grown in nutrient solution. Rev Bras Zootec 40:47–52. https://doi.org/10.1590/S1516-35982011000100007 (in portuguese)

    Article  Google Scholar 

  • Sonoda Y, Ikeda A, Saiki S, Yamaya T (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1;1 – 1;3 ) in rice. Plant Cell Physiol 44:726–734. https://doi.org/10.1093/pcp/pcg083

    Article  CAS  Google Scholar 

  • Tedesco MJ, Volkweiss SJ, Bohnen H (1985) Soil analysis, plant and other materials. UFRGS. Soil department, Porto Alegre, p 188 (in portuguese)

    Google Scholar 

  • Weber MB, Schat H, Maarel WMTBVD (1991) The effect of copper toxicity on the contents of nitrogen compounds in Silene vulgaris (Moench) Garcke. Plant Soil 133:101–109. https://doi.org/10.1007/BF00011904

    Article  CAS  Google Scholar 

  • Werner JC, Paulino VT, Cantarella H, Andrade NO, Quaggio JA (1996) Forages. In: Van Raij B, Cantarella H, Quaggio JA, Furlani AMC (eds) Recommendation of fertilization and limming for the São Paulo state, 2nd edn. Agronomic institute of Campinas & IAC foundation, Campinas, pp 263–273

  • Xiong ZT, Liu C, Geng B (2006) Phytotoxic effects of copper on nitrogen metabolism and plant growth in Brassica pekinensis Rupr. Ecotoxicol Environ Saf 64:273–280. https://doi.org/10.1016/j.ecoenv.2006.02.003

    Article  CAS  Google Scholar 

  • Xu Q, Qiu H, Chu W, Fu Y, Cai S, Min H, Sha S (2013) Copper ultrastructural localization, subcellular distribution, and phytotoxicity in Hydrilla verticillata (L.f.). Royle. Environ Sci Pollut Res 20:8672–8679. https://doi.org/10.1007/s11356-013-1828-1

    Article  CAS  Google Scholar 

  • Zhang GB, Yi HY, Gong JM (2014a) The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–3998. https://doi.org/10.1105/tpc.114.129296

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

Download references

Acknowledgments

The authors thank: FAPESP for the fellowship granted to the first author in the second year of his Master’s program (grant no. 2015/20625-0); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the fellowship granted to the first author in the first year of his Master’s program and to the third author (grant no. 306403/2013-7), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the fellowship granted during the first 2 months to the first author in his Master’s program, and to the second author.

Funding

This study was financed by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grant no. 2015/20624-4).

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Correspondence to Francisco Antonio Monteiro.

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Responsible editor: Elena Maestri

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de Souza Junior, J.C., Nogueirol, R.C. & Monteiro, F.A. NO3/NH4+ ratios affect nutritional homeostasis and production of Tanzania guinea grass under Cu toxicity. Environ Sci Pollut Res 25, 14083–14096 (2018). https://doi.org/10.1007/s11356-018-1541-1

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