Skip to main content
Log in

Nitrate induction in spruce: an approach using compartmental analysis

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Using 13NO 3 -efflux analysis, the induction of nitrate uptake by externally supplied nitrate was monitored in roots of intact Picea glauca (Moench) Voss. seedlings over a 5-d period. In agreement with our earlier studies, efflux analysis revealed three compartments, which have been identified as surface adsorption, apparent free space, and cytoplasm. While induction of nitrate uptake was pronounced, NO 3 fluxes in induced plants were decidedly lower and the induction response was slower than in other species. Influx rose from 0.1 μmol·g−1·h−1 (measured at 100 μM [NO 3 o) in uninduced plants to a maximum of 0.5 μmol·g−1h−1 after 3 d of exposure to 100 μM [NO 3 o and declined to 0.3–0.4 μmol·g−1h−1 at the end of the 5-d period. Efflux remained relatively constant around 0.02-0.04 μmol·g−1h−1, but its percentage with respect to influx declined from initially high values (around 30%) to steady-state values of 4–7%. Cytoplasmic [NO 3 ] ranged from the low micromolar in uninduced plants to a maximum of 2 mM in plants fully induced at 100 μM [NO 3 ]o. In-vivo root nitrate reductase activity (NRA) was measured over the same time period, and was found to follow a similar pattern of induction as influx. The maximum response in NRA slightly preceded that of influx. It increased from 25 nmol·g−1·h−1 without prior exposure to NO 3 to peak values around 150 nmol· g−1h−1 after 2 d of exposure to 100 μM [NO 3 ]o. Subsequently, NRA declined by about 50%. The dynamics of flux partitioning to reduction, to the vacuole, the xylem, and to efflux during the induction process are discussed.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

[NO 3 cyt :

cytoplasmic NO 3 concentration

[NO 3 ]free space :

NO 3 concentration in the cell wall free space

[NO 3 ]o :

NO 3 concentration in the external solution

NRA:

nitrate reductase activity

φ:

NO 3 flux (for subscripts, see Materials and methods)

References

  • Aslam, M., Travis, R.L., Huffaker, R.C. (1992) Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiol. 99, 1124–1133

    Google Scholar 

  • Aslam, M., Travis, R.L., Huffaker, R.C. (1993) Comparative induction of nitrate and nitrite uptake and reduction systems by ambient nitrate and nitrite in intact roots of barley (Hordeum vulgare L.) seedlings. Plant Physiol. 102, 811–819

    Google Scholar 

  • Breteler, H., Siegerist, M. (1984) Effect of ammonium on nitrate utilization by roots of dwarf bean. Plant Physiol. 75, 1099–1103

    Google Scholar 

  • Chapin, F.S. III, van Cleve, K., Tyron, P.R. (1986) Relationship of ion absorption to growth rate in taiga trees. Oecologia 69, 238–242

    Google Scholar 

  • Clarkson, D.T. (1986) Regulation of the absorption and release of nitrate by plant cells. In: Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants, pp. 3–27, Lambers, H., Neeteson, J.J., Stulen, I., eds. Martinus Nijhoff, Boston

    Google Scholar 

  • Clarkson, D.T., Lüttge, U. (1991) II. Mineral nutrition: Inducible and repressible nutrient transport systems. Progr. Bot. 52, 61–83

    Google Scholar 

  • Cooper, H.D., Clarkson, D.T. (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals — A possible mechanism integrating shoot and root in the regulation of nutrient uptake. J. Exp. Bot. 40, 753–762

    Google Scholar 

  • Cram, W.J. (1968) Compartmentation and exchange of chloride in carrot root tissue. Biochim. Biophys. Acta 163, 339–353

    Google Scholar 

  • Dhugga, K.S., Waines, J.G., Leonard, R.T. (1988) Correlated induction of nitrate uptake and membrane polypeptides in corn roots. Plant Physiol. 87, 120–125

    Google Scholar 

  • Glass, A.D.M., Siddiqi, M.Y. (1994) Nitrogen absorption by plant roots. In: Nitrogen nutrition of higher plants, pp. 21–55, Srivastava, H.S., Singh, R.P., eds. Assoc. Publ. Co., New Delhi, in press

    Google Scholar 

  • Goldstein, A.H., Hunziker, A.D. (1985) Induction of high affinity nitrate and ammonium transport systems in wheat. J. Plant Nutr. 8, 721–730

    Google Scholar 

  • Goyal, S.S., Huffaker, R.C. (1986) A novel approach and a fully automated microcomputer-based system to study kinetics of NO 3 , NO2 and NH +4 transport simultaneously by intact wheat seedlings. Plant Cell Environ. 9, 209–215

    Google Scholar 

  • Heimer, Y.M., Filner, P. (1971) Regulation of the nitrate assimilation pathway in cultured tobacco cells. III. The uptake system. Biochim. Biophys. Acta 230, 362–372

    Google Scholar 

  • Ingemarsson, B., Oscarson, P., ap Ugglas, M., Larsson, C.-M. (1987) Nitrogen utilization in Lemna. II. Studies of nitrate uptake using 13NO 3 . Plant Physiol. 85, 860–864

    Google Scholar 

  • Jackson, W.A., Fiesher, D., Hageman, R.H. (1973) Nitrate uptake by dark grown corn seedlings. Plant Physiol. 51, 120–127

    Google Scholar 

  • King, B.J., Siddiqi, M.Y., Glass, A.D.M. (1992) Studies of the uptake of nitrate in barley. V. Estimation of root cytoplasmic nitrate concentration using nitrate reductase activity — implications for nitrate influx. Plant Physiol. 99, 1582–1589

    Google Scholar 

  • King, B.J., Siddiqi, M.Y., Ruth, T.J., Warner, R.L., Glass, A.D.M. (1993) Feedback regulation of nitrate influx in barley roots by nitrate, nitrite and ammonium. Plant Physiol. 102, 1279–1286

    Google Scholar 

  • Kronzucker, H.J., Siddiqi, M.Y., Glass, A.D.M. (1995) Compartmentation and flux characteristics of nitrate in spruce. Planta 196, 674–682

    CAS  Google Scholar 

  • Lavoie, N., Vézina, L.-P., Margolis, H.A. (1992) Absorption and assimilation of nitrate and ammonium ions by Jack pine seedlings. Tree Physiol. 11, 171–183

    Google Scholar 

  • Lee, R.B., Clarkson, D.T. (1986) Nitrogen-13 studies of nitrate fluxes in barley roots. I. Compartmental analysis from measurements of 13N efflux. J. Exp. Bot. 37, 1753–1756

    Google Scholar 

  • Lee, R.B., Drew, M.C. (1986) Nitrogen-13 studies of nitrate fluxes in barley roots. II. Effect of plant N-status on the kinetic parameters of nitrate influx. J. Exp. Bot. 37, 1768–1779

    Google Scholar 

  • Lee, R.B., Purves, J.V., Ratcliffe, R.G., Saker, L.R. (1992) Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. J. Exp. Bot. 43, 1385–1396

    Google Scholar 

  • Lee, R.B., Rudge, K.A. (1986) Effects of nitrogen deficiency on the absorption of nitrate and ammonium by barley plants. Ann. Bot. 57, 471–486

    Google Scholar 

  • MacKown, C.T., McClure, P.R. (1988) Development of accelerated net nitrate uptake. Plant Physiol. 87, 162–166

    Google Scholar 

  • Mäck, G., Tischner, R. (1986) Nitrate uptake and reduction in sugarbeet seedlings. In: Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants, pp. 33–36, Lambers, H., Neetson, J.J., Stulen, I., eds. Martinus Nijhoff, Boston

    Google Scholar 

  • Mattson, M., Johansson, E., Lundborg, T., Larsson, M., Larsson, C.-M. (1991) Nitrogen utilization in N-limited barley during vegetative and generative growth. I. Growth and nitrate uptake kinetics in vegetative cultures grown at different relative addition rates of nitrate-N. J. Exp. Bot. 42, 197–205

    Google Scholar 

  • Meeks, J.C. (1993) 13N techniques. In: Nitrogen isotope techniques, pp. 273–303, Knowles, R., Blackburn, T.H., eds. Academic Press, Inc., San Diego, Cal.

    Google Scholar 

  • Minotti, P.L., Williams, D.C., Jackson, W.A. (1969) Nitrate uptake by wheat as influenced by ammonium and other cations. Crop Sci. 9, 9–14

    Google Scholar 

  • Muller, B., Touraine, B. (1992) Inhibition of NO 3 uptake by various phloem-translocated amino acids in soybean seedlings. J. Exp. Bot. 43, 617–623

    Google Scholar 

  • Ni, M., Beevers, L. (1994) Nitrate-induced polypeptides in membranes from corn seedling roots. J. Exp. Bot. 45, 355–365

    Google Scholar 

  • Peuke, A.D., Tischner, R. (1991) Nitrate uptake and reduction of aseptically cultivated spruce seedlings, Picea abies (L.) Karst. J. Exp. Bot. 42, 723–728

    Google Scholar 

  • Schmidt, B., Strack, D., Weidner, M. (1991) Nitrate reductase in needles, roots and trunk wood of spruce trees [Picea abies (L.) Karst.]. Trees 5, 215–226

    Google Scholar 

  • Siddiqi, M.Y., Glass, A.D.M., Ruth, T.J., Fernando, M. (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO 3 . Plant Physiol. 90, 806–813

    Google Scholar 

  • Siddiqi, M.Y., Glass, A.D.M., Ruth, T.J. (1991) Studies of the uptake of nitrate in barley. III. Compartmentation of NO 3 . J. Exp. Bot. 42, 1455–1463

    Google Scholar 

  • Solomonson, L.P., Barber, M.J. (1990) Assimilatory nitrate reductase: functional properties and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 225–253

    Google Scholar 

  • Tischner, R., Waldeck, B., Goyal, S.S., Rains, W.D. (1993) Effect of nitrate pulses on the nitrate-uptake rate, synthesis of mRNA coding for nitrate reductase, and nitrate-reductase activity in the roots of barley seedlings. Planta 189, 533–537

    Google Scholar 

  • Vitousek, P.M., Melillo, J.M. (1979) Nitrate losses from disturbed forests: Patterns and mechanisms. Forest Sci. 25, 605–619

    Google Scholar 

  • Walker, N.A., Pitman, M.G. (1976) Measurement of fluxes across membranes. In: Encyclopedia of plant physiology, vol. 2, part A, pp. 93–126, Lüttge, U., Pitman, M.G., eds., Springer Verlag, Berlin

    Google Scholar 

  • Warner, R.L., Huffaker, R.C. (1989) Nitrate transport is independent of NADH and NADPH nitrate reductase in barley seedlings. Plant Physiol. 91, 947–953

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony D. M. Glass.

Additional information

The research was supported by an Natural Sciences and Engineering Research Council, Canada, grant to Dr. A.D.M. Glass and by a University of British Columbia Graduate Fellowship to Herbert J. Kronzucker. Our thanks go to Dr. M. Adam and Mr. P. Culbert at the particle accelerator facility TRIUMF on the University of British Columbia campus for providing 13N, to Drs. R.D. Guy and S. Silim for providing plant material, and to Dr. M.Y. Wang, Mr. J. Bailey, Mr. J. Mehroke and Mr. J. Vidmar for essential assistance in experiments.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kronzucker, H.J., Glass, A.D.M. & Yaeesh Siddiqi, M. Nitrate induction in spruce: an approach using compartmental analysis. Planta 196, 683–690 (1995). https://doi.org/10.1007/BF00197332

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197332

Key words

Navigation