Skip to main content
SpringerLink
Log in

Nitrate transport processes in Fagus- Laccaria-Mycorrhizae

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The contribution of influx and efflux of NO3 - on NO3 - net uptake has been studied in excised mycorrhizae of 18–20 week old beech (Fagus sylvatica L.) trees. Net uptake rates of NO3 - followed uniphasic Michaelis-Menten kinetics in the concentration range between 10 μM and 1.0 mM external NO3 -, with an apparent Km of 88±7 μM, and a Vmax of 110±7 nmol g-1 root f.wt. h-1. The relative xylem loading of N, i.e. the portion of NO3 - taken up that was loaded into the xylem vessels as NO3 - plus reduced N, was constant over the concentration range tested (4.6–7.7%). NO3 - influx proceeded linearly with increasing external NO3 - supply. When the assumed regulators of net NO3 - uptake, i.e. NH4 + or L-glutamate, were applied together with NO3 -, net uptake rates of NO3 - decreased. This inhibitory effect was caused by a reduction of NO3 - influx rather than an enhanced efflux. The comparison of the present data with a recent study with non-mycorrhizal beech roots (Kreuzwieser et al., 1997; J. Exp. Bot. 48, 1431–1438) revealed that mycorrhization leads to reduced rates of NO3 - net uptake. This effect is caused by reduced influx plus enhanced efflux of NO3 - as compared with non-mycorrhizal beech roots.

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

Access this article

Log in via an institution

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

References

  • Abuzinadah R A, Finlay R D and Read D J 1986 The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. II. Utilization of proteins by mycorrhizal plants of Pinus contorta. New Phytol. 103, 495–506.

    Article  CAS  Google Scholar 

  • Abuzinadah R A and Read D J 1989 The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. IV. The utilization of peptides by birch (Betula pendula L.) infected with different mycorrhizal fungi. New Phytol. 112, 55–60.

    Article  CAS  Google Scholar 

  • Abuzinadah R A and Read D J 1986 The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of peptides and proteins by ectomycorrhizal fungi. New Phytol. 103, 481–493.

    Article  CAS  Google Scholar 

  • Abuzinadah R A and Read D J 1988 Amino acids as nitrogen sources for ectomycorrhizal fungi. Trans. British Mycol. Society 91, 473–479.

    CAS  Google Scholar 

  • Agerer R 1993 Colour atlas of ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch-Gmünd.

    Google Scholar 

  • Aguera E, De la Haba P, Fontes A G and Maldonado J M 1990 Nitrate and nitrite uptake and reduction by intact sunflower plants. Planta 182, 149–154.

    CAS  Google Scholar 

  • Alexander I J and Fairley R I 1986 Growth and nitrogen uptake rates of ectomycorrhizal spruce seedlings. In Proceedings of the First European Symposium on Mycorrhizae. Eds V Gianinazzi-Pearson and S Gianinazzi. pp 377–382. Inst. National de la Recherche Agronomique (INRA), Paris.

    Google Scholar 

  • Aslam M, Travis R L and Huffaker R C 1994 Stimulation of nitrate and nitrite efflux by ammonium in barley (Hordeum vulgare L.) seedlings. Plant Physiol. 106, 1293–1301.

    PubMed  CAS  Google Scholar 

  • Ayling S M 1993 The effect of ammonium ion on membrane potential and anion flux in roots of barley and tomato. Plant Cell Environ. 16, 297–303.

    Article  CAS  Google Scholar 

  • Boxman AW and Roelofs J G M 1988 Some effects of nitrate versus ammonium nutrition on the nutrient fluxes in Pinus sylvestris seedlings. Effects of mycorrhizal infection. Can. J. Bot. 66, 1091–1097.

    CAS  Google Scholar 

  • Carrodus B B 1966 Absorption of nitrogen by mycorrhizal roots of beech. I. Factors affecting the assimilation of nitrogen. New Phytol. 65, 358–371.

    Article  CAS  Google Scholar 

  • Carrodus B B 1967 Absorption of nitrogen by mycorrhizal roots of beech. II. Ammonium and nitrate as sources of nitrogen. New Phytol. 66, 1–4.

    Article  CAS  Google Scholar 

  • Chaillou S, Rideout J W, Raper C D and Morot-Gaudry J-F 1994 Responses of soybean to ammonium and nitrate supplied in combination to the whole root system or separately in a split-root system. Plant Physiol. 90, 259–268.

    Article  CAS  Google Scholar 

  • Clarkson D T, Gojon A, Saker L R, Wiersema P K, Purves J V, Tillard P, Arnold G M, Paans A J M, Vaalburg W and Stulen I 1996. Nitrate and ammonium influxes in soybean (Glycine max) roots: Direct comparison of N-13 and N-15 tracing. Plant Cell Environ. 19, 859–868.

    Article  CAS  Google Scholar 

  • Clement C R, Hopper M J, Jones L H P and Leaf E L 1978 The uptake of nitrate by Lolium perenne from flowing nutrient solution. II. Effect of light, defoliation and relationship of CO2 flux. J. Exp. Bot. 29, 1173–1183.

    CAS  Google Scholar 

  • Colpaert J V, Van Laere A and Van Assche J A 1996 Carbon and nitrogen allocation in ectomycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings. Tree Physiol. 16, 787–793.

    PubMed  CAS  Google Scholar 

  • Cooper K M and 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.

    CAS  Google Scholar 

  • Deane-Drummond C E and Glass A DM 1983 Short term studies of nitrate uptake into barley plants using ion-specific electrodes and 36ClO _3 . II. Regulation of NO _3 efflux by NH +4 Plant Physiol. 73, 105–110.

    PubMed  CAS  Google Scholar 

  • De la Haba P, Aguera E and Maldonado J M 1990 Differential effects of ammonium and tungsten on nitrate and nitrite uptake and reduction by sunflower plants. Plant Sci. 70, 21–26.

    Article  CAS  Google Scholar 

  • Doddema H and Telkamp G P 1979 Uptake of nitrate by mutants of Arabidopsis thaliana, disturbed in uptake or reduction of nitrate. II: Kinetics. Physiol. Plant. 45, 332–338.

    Article  CAS  Google Scholar 

  • Eltrop L and Marschner H 1996 Growth and mineral nutrition of non-mycorrhizal and mycorrhizal Norway spruce (Picea abies) seedlings grown in semi-hydroponic sand culture. I. Growth and mineral nutrient uptake in plants supplied with different forms of nitrogen. New Phytol. 133, 469–478.

    Article  CAS  Google Scholar 

  • Finlay R D, Ek H, Odham G and Söderström B 1989 Uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium and nitrate sources by internal ectomycorrhizal systems of Fagus sylvatica infected with Paxillus involutus. New Phytol. 113, 47–55.

    Article  CAS  Google Scholar 

  • Geßler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K and Rennenberg H 1997 Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol. 138, 275–286.

    Article  Google Scholar 

  • Geßler A, Schultze M, Schrempp S and Rennenberg H 1998 Interactions of phloem-translocated amino compounds with nitrate net uptake by the roots of beech (Fagus sylvatica) seedlings. J. Exp. Bot. 326, 1529–1537.

    Google Scholar 

  • Glass A D M and Siddiqi M Y 1995 Nitrogen absorption by plant roots. In Nitrogen Nutrition in Higher Plants. Eds H S Srivastava and R P Singh. pp 21–56. Associated Publishing Co. New Delhi.

    Google Scholar 

  • Hanes C S 1932 Studies on plants amylases I. The effect of starch concentration upon velocity of hydrolases by the amylases of germinated barley. Biochem. J. 26, 1406–1421.

    PubMed  CAS  Google Scholar 

  • Häussling M, Jorns C A, Lehmbecker G, Hecht-Buchholz C H and Marschner H 1988 Ion and water uptake in relation to root development in Norway spruce (Picea abies (L.) Karst.). J. Plant Physiol. 133, 486–491.

    Google Scholar 

  • Harley J L and Harley E L 1987 A check-list of mycorrhiza in the British flora. New Phytol. 105, (Suppl) 1–102.

    Article  Google Scholar 

  • Haynes R J and Goh K M 1978 Ammonium and nitrate nutrition of plants. Biol. Rev. 53, 465–510.

    Article  CAS  Google Scholar 

  • Herschbach C and Rennenberg H 1991 Influence of glutathione (GSH) on sulphate influx, xylem loading and exudation in excised tobacco roots. J. Exp. Bot. 42, 1021–1029.

    CAS  Google Scholar 

  • Hole D J, Emran A M, Fares Y and Drew M C 1990 Induction of nitrate transport in maize roots and kinetics of influx, measured with nitrogen-13. Plant Physiol. 93, 642–647.

    PubMed  CAS  Google Scholar 

  • Ingestad T, Arveby A S and Kähr M 1986 The influence of ectomycorrhiza on nitrogen nutrition and growth of Pinus sylvestris seedlings. Physiol. Plant. 68, 575–582.

    Article  Google Scholar 

  • Imsande J and Touraine B 1994 N demand and the regulation of nitrate uptake. Plant Physiol. 105, 3–7.

    PubMed  CAS  Google Scholar 

  • Jones M D, Durall D M and Tinker P B 1990 Phosphorus relationships and production of extramatrical hyphae by two types of willow ectomycorrhizas at different soil phosphorus levels. New Phytol. 115, 259–267.

    Article  CAS  Google Scholar 

  • Jones D L 1999 Amino acid biodegradation and its potential effects on orgnic nitrogen capture by plants. Soil Biol. Biochem. 31, 613–622.

    Article  CAS  Google Scholar 

  • Jongbloed R H, Clement JMAM and Borst-Pauwels 1991 Kinetics of NH +4 and K+ uptake by ectomycorrhizal fungi. Effect of NH +4 on K+ uptake. Plant Physiol. 83, 427–432.

    Article  CAS  Google Scholar 

  • Kamminga-Van Wijk C and Prins H B A 1993 The kinetics of NH +4 and NO _3 uptake by Douglas fir from single N-solutions containing both NH +4 and NO _3 . Plant Soil 151, 91–96.

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kreuzwieser J, Herschbach C and Rennenberg H 1996 Sulfate uptake and xylem loading of non-mycorrhizal excised roots of young Fagus sylvatica trees. Plant Physiol. Biochem. 34, 409–416.

    CAS  Google Scholar 

  • Kreuzwieser J, Herschbach C, Stulen I, Wiersema P, Vaalburg W and Rennenberg H 1997 Interactions of NH +4 and L-glutamate with NO _3 transport processes of non-mycorrhizal Fagus sylvatica roots. J. Exp. Bot. 48, 1431–1438.

    CAS  Google Scholar 

  • Kreuzwieser J and Rennenberg H 1998 Sulphate uptake and xylem loading of mycorrhizal beech roots. New Phytol. 140, 319–329.

    Article  CAS  Google Scholar 

  • Kronzucker H J, Siddiqi M Y and Glass A D M 1995 Kinetics of NO _3 influx in spruce. Plant Physiol. 109, 319–326.

    PubMed  CAS  Google Scholar 

  • Kronzucker H J, Glass A D M and Siddiqi M Y 1999 Inhibition of nitrate uptake by ammonium in barley. Analysis of component fluxes. Plant Physiol. 120, 283–291.

    Article  PubMed  CAS  Google Scholar 

  • Lajtha K 1994 Nutrient uptake in eastern deciduous tree seedlings. Plant Soil 160, 193–199.

    CAS  Google Scholar 

  • Larsson C M, Larsdson M, Purves J V and Clarkson D T 1991 Translocation and cycling through roots of recently absorbed nitrogen and sulphur in wheat (Triticum aestivum) during vegetative and generative growth. Physiol. Plant. 82, 345–352.

    Article  CAS  Google Scholar 

  • Lee R B and 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, 1753–1767.

    CAS  Google Scholar 

  • Lee R B and Drew M C 1989 Rapid, reversible inhibition of nitrate influx in barley by ammonium. J. Exp. Bot. 40, 741–752.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Mac Clure P R, Kochian L V, Spanswick R M and Shaff J E 1990 Evidence for co-transport of nitrate and protons in maize roots. I. Effects of nitrate on the membrane potential. Plant Physiol. 93, 281–289.

    Google Scholar 

  • Marschner H 1995 Mineral nutrition of higher plants. Academic press, London.

    Google Scholar 

  • Marschner H, Häussling M and George E 1991 Ammonium and nitrate uptake rates and rhizosphere pH in non-mycorrhizal roots of Norway spruce [Picea abies (L.) Karst.]. Trees 5, 14–21.

    Article  Google Scholar 

  • Martin F and Ben Driss Amraoui M1989 Partitioning of assimilated nitrogen in beech (Fagus sylvatica). In Forest Tree Physiology. Eds E Dreyer et al. pp 660–662s. Elsevier, Amsterdam.

    Google Scholar 

  • Marx D H 1969 The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. Phytopathology 59, 153–163.

    Google Scholar 

  • Muller B, Tillard P and Touraine B 1995 Nitrate fluxes in soybean seedling roots and their response to amino acids: an approach using 15N. Plant Cell Environ. 18, 1267–1279.

    Article  CAS  Google Scholar 

  • Muller B and Touraine B 1992 Inhibition of NO _3 uptake by various phloem-translocated amino acids in soybean seedlings. J. Exp. Bot. 43, 617–623.

    CAS  Google Scholar 

  • Murashige T and Skoog F 1962 A revised medium for rapid growth and bio assay with tobacco tissue cultures. Physiol. Plant. 15, 473–497.

    Article  CAS  Google Scholar 

  • Nylund J-E and Wallander H 1992 Ergosterol analysis as a mean of quantifying mycorrhizal biomass. In Methods in Microbiology. Vol 24. Eds JR Norris, DJ Read and AK Varma. pp 77–88. Academic Press, London.

    Google Scholar 

  • Pitman M G 1971 Uptake and transport of ions in barley seedlings. I. Estimation of chloride fluxes in cells of excised roots. Aust. J. Biol. Sci. 24, 407–421.

    CAS  Google Scholar 

  • Plassard C, Barry D, Eltrop L and Mousain D 1994 Nitrate uptake inmaritime pine (Pinus pinaster) and the ectomycorrhizal fungus Hebeloma cylindosporum: effect of ectomycorrhizal symbiosis. Can. J. Bot. 72, 189–197.

    Google Scholar 

  • Rao K P and Rains D W 1976 Nitrate absorption by barley. I. Kinetics and energetics. Plant Physiol. 57, 55–58.

    PubMed  CAS  Google Scholar 

  • Rao T P, Ito O and Matsuga R 1993 Differences in uptake kinetics of ammonium and nitrate in legumes and cereals. Plant Soil 154, 67–72.

    Article  CAS  Google Scholar 

  • Rawat S R, Silim N, Kronzucker H J, Siddiqi M Y and Glass A D M 1999 AtAMT1 gene expression and NH4+ uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant J 19, 143–152.

    Article  PubMed  CAS  Google Scholar 

  • Rygiewicz P T and Andersen C P 1994 Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 368, 58–60.

    Article  Google Scholar 

  • Rygiewicz P T, Bledsoe C S and Zasoski R J 1984a Effects of ectomycorrhizae and solution pH on [15N]ammonium uptake by coniferous seedlings. Can. J. For. Res. 14, 885–892.

    CAS  Google Scholar 

  • Rygiewicz P T, Bledsoe C S and Zasoski R J 1984b Effects of ectomycorrhizae and solution pH on [15N]nitrate uptake by coniferous seedlings. Can. J. For. Res. 14, 893–899.

    CAS  Google Scholar 

  • Rygiewicz P T and Bledsoe C S 1986 Effects of pre-treatment conditions on ammonium and nitrate uptake by Douglas fir seedlings. Tree Physiol. 1, 145–50.

    PubMed  CAS  Google Scholar 

  • Sarjala T 1991 Effect of mycorrhiza and nitrate nutrition on nitrate reductase activity in Scots pine seedlings. Physiol. Plant. 81, 89–94.

    Article  CAS  Google Scholar 

  • Seegmüller S, Schulte M, Herschbach C and Rennenberg H 1996 Interactive effects of mycorrhization and elevated atmospheric CO2 on sulphur nutrition of young pedunculate oak (Quercus robur L.) trees. Plant Cell Environ. 19, 418–426.

    Article  Google Scholar 

  • Scheromm P and Plassard C 1990 Nitrate nutrition of maritime pine (Pinus pinaster Soland in Ait.) ectomycorrhizal with Hebeloma cylindosporum. Romagn. New Phytol. 114, 93–98.

    Article  CAS  Google Scholar 

  • Schneider S, Geßler A, Weber P, Von Sengbusch D, Hanemann U and Rennenberg H 1996 Soluble N compounds in trees exposed to high loads of N a comparison of spruce (Picea abies [L.] Karst) and beech (Fagus sylvatica L.) grown under field conditions. New Phytol. 134, 103–114.

    Article  CAS  Google Scholar 

  • Schulze E D 1989 Air pollution and forest decline in a spruce (Picea abies) forest. Science 244, 776–783.

    CAS  PubMed  Google Scholar 

  • Siddiqi M Y, Glass A D M, Ruth T J and Fernando M 1989 Studies of the regulation of nitrate influx by barley seedlings using 13NO _3 . Plant Physiol. 90, 806–813.

    PubMed  CAS  Google Scholar 

  • Siddiqi M Y, Glass A D M, Ruth T J and Rufty TW1990 Studies of the uptake of nitrate in barley. I. Kinetics of 13NO _3 influx. Plant Physiol. 93, 1426–1432.

    Article  PubMed  CAS  Google Scholar 

  • Smith F A 1972 A comparison of the uptake of nitrate, chloride and phosphate by excised beech mycorrhizas. New Phytol. 71, 875–882.

    Article  CAS  Google Scholar 

  • Ter Steege M W, Stulen I, Wiersema P K, Paans A J M, Vaalburg W, Kuiper P J C and Clarkson D T 1998 Growth requirement for N as a criterion to assess the effects of physical manipulation on nitrate uptake fluxes in spinach. Physiol Plant. 103, 181–192.

    Article  CAS  Google Scholar 

  • Touraine B, Clarkson D T and Muller B 1994 Regulation of nitrate uptake at the whole plant level. In A Whole Plant Perspective on Carbon-Nitrogen Interactions. Eds J Roy and E Garnier. pp 11–30. SPB Academic Publishing bv, The Hague.

    Google Scholar 

  • Vaalburg W and Paans A M J 1983 Short-lived positron emitting radionuclides In Radionuclides Production II. Eds F Helms and L G Colombetti. pp 48–89. CRC Press, Boca Raton.

    Google Scholar 

  • Vézina L P, Margolis H A, MacAfee B J and Delaney S 1989 Changes in the activity of enzymes involved with primary nitrogen metabolism due to ectomycorrhizal symbiosis on jack pine seedlings. Physiol. Plant. 75, 55–62.

    Article  Google Scholar 

  • Wallander H and Nylund J E 1992 Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytol. 120, 495–503.

    Article  CAS  Google Scholar 

  • Wilcox H E 1991 Mycorrhizae. In The Plant Root, the Hidden Half. Eds Y Waisel, A Eshel and U Kafkafi. pp 731–765. Marcel Dekker, New York.

    Google Scholar 

  • Von Wiren N, Gazzarini S and Frommer W 1997 Regulation of mineral nitrogen uptake in plants. Plant Soil 196, 191–199.

    Article  CAS  Google Scholar 

  • Zhuo D, Okamoto M, Vidmar J J and Glass A D M 1999 Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J. 17, 563–568.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors
  1. Jürgen Kreuzwieser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ineke Stulen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Wiersema
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Willem Vaalburg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heinz Rennenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kreuzwieser, J., Stulen, I., Wiersema, P. et al. Nitrate transport processes in Fagus- Laccaria-Mycorrhizae. Plant and Soil 220, 107–117 (2000). https://doi.org/10.1023/A:1004775230952

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004775230952

Search

Navigation