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Salt-induced NO3 - uptake inhibition in cowpea roots is dependent on the ionic composition of the salt and its osmotic effect

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Biologia Plantarum

Abstract

Salinity remarkably inhibits NO3 - uptake but the mechanisms are not well understood. This study was addressed to elucidate the role of ionic and osmotic components of salinity on NO3 - influx and efflux employing classic kinetics involving a low affinity transport system (LATS) and a high affinity transport system (HATS). In the presence of KCl, NaCl, and Na2SO4 at 100 mM concentrations, in both LATS and HATS, Michaelis constant (Km) was similar for the three salts and maximum rate (Vmax) decreased as follows: KCl > NaCl > Na2SO4, compared to control indicating a non-competitive interaction with NO3 -. Unexpectedly, iso-osmotic solutions (osmotic potential Ψπ = -0.450) of polyethylene glycol (PEG, 17.84 %, v/v) and mannitol (100 mM) remarkably increased Km in both the LATS and the HATS, but Vmax did not change indicating a competitive inhibition. Under the PEG and mannitol treatments, Km and Vmax were higher than under the salt treatments. The salts increased slightly NO3 - efflux in the following order KCl > NaCl > Na2SO4. In contrast, mannitol strongly stimulated and the PEG inhibited NO3 - efflux. The obtained data reveal that salinity effects were not dependent on the anion type (Cl- versus SO4 2-) indicating a non-competitive inhibition mechanism between Cl- and NO3 -. In contrast, the cation types (K+ versus Na+) had a pronounced effect. The osmotic component is important to net NO3 - uptake affecting remarkably the influx in both LATS and HATS components of cowpea roots.

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Abbreviations

HATS:

high affinity transport system

Km :

Michaelis constant

LATS:

low affinity transport system

M-M:

Michaelis-Menten

PEG:

polyethylene glycol

Vmax :

maximum rate

Ψπ :

osmotic potential

References

  • Adamowicz, S., Le Bot, J.: Trends in modelling nitrate uptake. — Acta Horticult. 507: 231–239, 1999.

    Article  Google Scholar 

  • Andrews, M., Raven, J.A., Lea, P.J.: Do plants need nitrate? The mechanisms by which nitrogen form affects plants. — Ann. appl. Biol. 163: 174–199, 2013.

    Article  CAS  Google Scholar 

  • Aslam, M., Travis, R.L., Rains, W.D.: Evidence for substrate induction of a nitrate efflux system in barley roots. — Plant Physiol. 112: 1167–1175, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cachorro, P., Ortiz, A., Cerdá, A.: Implications of calcium nutrition on the response of Phaseolus vulgaris L. to salinity. — Plant Soil 159: 205–212, 1994.

    Article  CAS  Google Scholar 

  • Cerezo, M., García-Agustín, P., Primo-Millo, E.: Influence of chloride and transpiration on net 15NO3 - uptake rate by citrus roots. — Ann. Bot. 84: 117–120, 1999.

    Article  CAS  Google Scholar 

  • Chen, Z.H., Pottosin, I., Guin, T.A.: Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. — Plant Physiol. 145: 1714–1725, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarkson, D.T.: Mechanisms for N-uptake and their running costs; is there scope for more efficiency? - In: Lambers, H., Poorter, H., Van Veuren, M.M.I. (ed.): Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences. Pp. 221–235. Backhuys Publishers, Leiden 1998.

    Google Scholar 

  • Crawford, N.M., Glass, A.D.M.: Molecular and physiological aspects of nitrate uptake in plants. — Trends Plant Sci. 3: 389–395, 1998.

    Article  Google Scholar 

  • Dai, J., Duan, L., Dong, H.: Comparative effect of nitrogen forms on nitrogen uptake and cotton growth under salinity stress. — J. Plant Nutr. 38: 1530–1543, 2015.

    Article  CAS  Google Scholar 

  • Deanne-Drummond, C.E.: Biochemical and biophysical aspects of nitrate uptake and its regulation. - In: Abrol, Y.P.(ed.): Nitrogen in Higher Plants. Pp. 1–37. Somerset: Research Studies, Tauton 1993.

    Google Scholar 

  • Epstein, E.: Mineral Nutrition of Plants. Principles and Perspectives. - Wiley, New York 1972.

    Google Scholar 

  • Forde, B.G., Clarkson, D.T.: Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. — Adv. bot. Res. 30: 1–90, 1999.

    Article  CAS  Google Scholar 

  • Glass, A.D.M.: The apoplast: a kinetic perspective. In: Sattelmacher, B., Horst, W.J. (ed.): The Apoplast of Higher Plants: Compartment of Storage, Transport, and Reactions. The Significance of the Apoplast for the Mineral Nutrition of Higher Plants. Pp. 96. Springer-Verlag, Dordrecht 2007.

    Google Scholar 

  • Hoagland, D.R., Arnon, D.I.: The water culture method for growing plants without soil. — Calif. Agr. Exp. Sta. Bull. 347: 1–39, 1950.

    Google Scholar 

  • Ivashikina, N.V., Feyziev, Y.M.: Regulation of nitrate uptake in maize seedlings by accompanying cations. — Plant Sci. 131: 25–34, 1998.

    Article  CAS  Google Scholar 

  • Kaburagi, E., Yamada, M., Fujiyama, H.: Sodium, but not potassium, enhances root to leaf nitrate translocation in Swiss chard (Beta vulgaris L. var. Cicla). — Environ. exp. Bot. 112: 27–32, 2015.

    Article  CAS  Google Scholar 

  • Kong, X.Q., Gao, X.H., Sun, W., An, J., Zhang, H.: Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1. — Plant mol. Biol. 75: 567–578, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Li, R., Shi, F., Fukuda, K.: Interactive effects of salt and alkali stresses on seed germination, germination recovery, and seedling growth of a halophyte Spartina alterniflora (Poaceae). — South Afr. J. Bot. 76: 380–387, 2010.

    Article  Google Scholar 

  • Massa, D., Mattson, N.S., Lieth, H.: Effects of saline root environment (NaCl) on nitrate and potassium uptake kinetics for rose plants: a Michaelis-Menten modeling approach. — Plant Soil 318: 101–115, 2009.

    Article  CAS  Google Scholar 

  • Mata, C., Vemde, N., Clarkson, D.K., Martins-Loução, M.A., Lambers, H.: Influx, efflux and net uptake of nitrate in Quercus suber seedlings. — Plant Soil 221: 25–32, 2000.

    Article  CAS  Google Scholar 

  • Miller, A.J., Smith, S.J.: Nitrate transport and compartmentation in cereal root cells. — J. exp. Bot. 47: 843–854, 1996.

    Article  CAS  Google Scholar 

  • Miller, A.J., Fan, X., Orsel, M., Smith, S.J., Wells, D.M.: Nitrate transport and signaling. — J. exp. Bot. 58: 2297–2306, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Ouerghi, Z., Cornic, G., Roudani, M., Ayadi, A., Brulfert, J.: Effect of on photosynthesis of two species (Triticum durum and T. aestivum) differing in their sensitivity to salt stress. — J. Plant Physiol. 156: 135–340, 2000.

    Article  Google Scholar 

  • Ourry, A., Meslé, S.S., Boucaud, J.: Effect of osmotic stress (NaCl and polyethylene glycol) on nitrate uptake, translocation, storage and reduction in ryegrass (Lolium perene L.). — New Phytol. 120: 275–280, 1992.

    Article  CAS  Google Scholar 

  • Parker, J.L., Newstead, S.: Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. — Nature 507: 68–73, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peuke, A.D., Jeschke, W.D.: The characterization of inhibition of net nitrate uptake by salt in salt-tolerant barley (Hordeum vulgare L. cv. California Mauriot). — J. exp. Bot. 50: 1365–1372, 1999.

    Article  CAS  Google Scholar 

  • Ramos, J., López, M.J., Benlloch, M.: Effect of NaCl and KCl salts on the growth and solute accumulation of the halophyte Atriplex nummularia. — Plant Soil 259: 163–168, 2004.

    Article  CAS  Google Scholar 

  • Rubinigg, M., Posthumus, F., Ferschke, M., Elzenga, J.T.M., Stulen, I.: Effects of NaCl salinity on 15N-nitrate fluxes and specific root length in the halophyte Plantago maritima L. — Plant Soil 250: 201–213, 2003.

    Article  CAS  Google Scholar 

  • Santos, L.A., Santos, W.A., Sperandio, M.V.L., Bucher, C.A., Souza, S.R., Fernandes, M.S.: Nitrate uptake kinetics and metabolic parameters in two rice varieties grown in high and low nitrate. — J. Plant Nutr. 34: 988–1002, 2011.

    Article  CAS  Google Scholar 

  • Shen, B., Jensen, R.G., Bohnert, H.: Mannitol protects against oxidation by hydroxyl radicals. — Plant Physiol. 115: 527–532, 1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sassi-Aydi, S., Aydi, S., Abdelly, C.: Inorganic nitrogen nutrition enhances osmotic stress tolerance in Phaseolus vulgaris: lessons from a crought-sensitive cultivar. — Hort. Sci. 49: 550–555, 2014.

    Google Scholar 

  • Silveira, J.A.G., Melo, A.R.B., Viégas, R.A., Oliveira, J.T.A.: Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. — Environ. exp. Bot. 46: 171–179, 2001.

    Article  CAS  Google Scholar 

  • Silveira, J.A.G., Melo, A.R.B., Martins, M.O., Ferreira-Silva, S.L., Aragão, R.M., Silva, E.N., Viégas, R.A.: Salinity affects indirectly nitrate acquisition associated with glutamine accumulation in cowpea roots. — Biol Plant. 56: 575–580, 2012.

    Article  CAS  Google Scholar 

  • Sorgonà, A., Lupini, A., Mercati, F., Di Dio, L., Sunseri, F., Abenavoli, M.R.: Nitrate uptake along the maize primary root: an integrated physiological and molecular approach. — Plant Cell Environ. 34: 1127–1140, 2011.

    Article  PubMed  Google Scholar 

  • Tsay, Y.F., Chiu, C.C., Tsai, C.B., Ho, C.H., Hsu, P.K.: Nitrate transporters and peptide transporters. — FEBS Lett. 581: 2290–2300, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Wegner, L.H., Stefano, G., Shabala, L., Rossi, M., Mancuso, S., Shabala, S.: Sequential depolarization of root cortical and stellar cells induced by an acute shock–implications for Na+ and K+ transport into xylem vessels. — Plant Cell Environ. 34: 859–869, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Yang, T., Zhu, L., Wang, S., Gu, W., Huang, D., Xu, W., Jiang, A., Li, S.: Nitrate uptake kinetics of grapevine under root restriction. — Sci. Horticult. 111: 358–364, 2007.

    Article  CAS  Google Scholar 

  • Yuan, J.F., Tian, C.Y., Feng, G.: Effects of sodium on nitrate uptake and osmotic adjustament of Suaeda physophora. — J Arid Land 2: 190–196, 2010.

    Article  Google Scholar 

  • Zhao, F.J., Hamon, R.E., Lombi, E., Mclaughlin, M.J., Mcgrath, S.P.: Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi cauerulescens. — J. exp. Bot. 53: 535–543, 2002.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to J. A. G. Silveira.

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Aragão, R.M., Silva, E.N., Silva, P.C.C. et al. Salt-induced NO3 - uptake inhibition in cowpea roots is dependent on the ionic composition of the salt and its osmotic effect. Biol Plant 60, 731–740 (2016). https://doi.org/10.1007/s10535-016-0604-8

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  • DOI: https://doi.org/10.1007/s10535-016-0604-8

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