Plant and Soil

, Volume 226, Issue 2, pp 275–285

Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi

  • Heidi-Jayne Hawkins
  • Anders Johansen
  • Eckhard George


New information on N uptake and transport of inorganic and organic N in arbuscular mycorrhizal fungi is reviewed here. Hyphae of the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe (BEG 107) were shown to transport N supplied as 15N-Gly to wheat plants after a 48 h labelling period in semi-hydroponic (Perlite), non-sterile, compartmentalised pot cultures. Of the 15N supplied to hyphae in pot cultures over 48 h, 0.2 and 6% was transported to plants supplied with insufficient N or sufficient N, respectively. The increased 15N uptake at the higher N supply was related to the higher hyphal length density at the higher N supply. These findings were supported by results from in vitro and monoxenic studies. Excised hyphae from four Glomus isolates (BEG 84, 107, 108 and 110) acquired N from both inorganic (15NH415NO3, 15NO3 or 15NH4+) and organic (15N-Gly and 15N-Glu, except in BEG 84 where amino acid uptake was not tested) sources in vitro during short-term experiments. Confirming these studies under sterile conditions where no bacterial mineralisation of organic N occurred, monoxenic cultures of Glomus intraradices Schenk and Smith were shown to transport N from organic sources (15N-Gly and 15N-Glu) to Ri T-DNA transformed, AM-colonised carrot roots in a long-term experiment. The higher N uptake (also from organic N) by isolates from nutrient poor sites (BEG 108 and 110) compared to that from a conventional agricultural field implied that ecotypic differences occur. Although the arbuscular mycorrhizal isolates used contributed to the acquisition of N from both inorganic and organic sources by the host plants/roots used, this was not enough to increase the N nutritional status of the mycorrhizal compared to non-mycorrhizal hosts.

arbuscular mycorrhiza Daucus carota Glomus mosseae Glomus intraradices monoxenic culture N uptake Triticum aestivum 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abuarghub S M and Read D J 1988 The biology of mycorrhiza in the Ericaceae. XII. Quantitative analysis of individual free amino acids in relation to time and depth in the soil profile. New Phytol. 108, 433–441.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. Ames, R N, Reid C P P, Porter L K and Cambardella C 1983 Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol. 95, 381–396.CrossRefGoogle Scholar
  4. Bago B, Vierheilig H, Piché Y and Azcó n-Aguilar C 1996 Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol. 133, 273–280.CrossRefGoogle Scholar
  5. Bécard G and Fortin J A 1988 Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211–218.CrossRefGoogle Scholar
  6. Bush D R 1993 Proton-coupled sugar and amino acid transporters in plants. Ann. Rev. Plant Physiol. Plant Molec. Biol. 44, 513–542.CrossRefGoogle Scholar
  7. Chabot S, Bécard G and Piché Y 1992 Life cycle of Glomus intraradix in root organ culture. Mycologia 84, 315–321.Google Scholar
  8. Chalot M, Brun A, Botton B and Söderström B 1996 Kinetics, energetics and specificity of a general amino acid transporter from the ectomycorrhizal fungus Paxillus involutus. Microbiol. 142, 1749–1756.CrossRefGoogle Scholar
  9. Chapin F S III, Moilanen L and Kielland K 1993 Preferential use of organic nitrogen for growth by a non-mycorrhizal artic sedge. Nature 361, 150–153.CrossRefGoogle Scholar
  10. Chen A, Chambers S M and Cairney J W G 1999 Utilisation of organic nitrogen and phosphorus sources by mycorrhizal endophytes of Woollsia pungens (Cav.) F. Muell. (Epacridaceae). Mycorrhiza 8, 181–187.CrossRefGoogle Scholar
  11. Doner L W and Bécard G 1991 Solubilization of gellan gels by chelation of cations. Biotech. Tech. 5, 25–28.CrossRefGoogle Scholar
  12. Doner L W and Douds D D 1995 Purification of commercial gellan to monovalent cation salts results in acute modification of solution and gel-forming properties. Carb. Res. 273, 225–233.CrossRefGoogle Scholar
  13. Fischer W-N, André B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K and Frommer W B 1998 Amino acid transport in plants. Trends Plant Sci. 3, 188–195.CrossRefGoogle Scholar
  14. Frey B and Schüepp H 1993 Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol. 124, 221–230.CrossRefGoogle Scholar
  15. Frommer W B, Kwart M, Hirner B, Fischer W N, Hummel S and Ninnemann O 1994 Transporters for nitrogenous compounds in plants. Plant Mol. Biol. 26, 1651–1670.PubMedCrossRefGoogle Scholar
  16. George E, Häussler K, Vetterlein D, Gorgus E and Marschner H 1992 Water and nutrient translocation by hyphae of Glomus mosseae. Can. J. Bot. 70, 2130–2137.Google Scholar
  17. Giovannetti M and Mosse B 1980 An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500.CrossRefGoogle Scholar
  18. Hawkins H-J and George E 1999 Effect of nitrogen status on the contribution of arbuscular mycorrhizal hyphae to plant nitrogen uptake. Physiol. Plant. 105, 694–700.CrossRefGoogle Scholar
  19. Hewitt E J 1966 Sand andWater Culture Methods Used in the Study of Plant Nutrition, 2nd revised edition, Commonwealth Bureau of Horticulture and Plantation Crops, East Malling, Technical Communication No. 22, Commonwealth Agriculture Bureau, Farnham Royal, UK. pp 431–432.Google Scholar
  20. Huang C and Huang C P 1996 Application of Aspergillus oryzae and Rhizopus oryzae for Cu (II) removal. Wat. Res. 9, 1985–1990.CrossRefGoogle Scholar
  21. Jensen E S 1991 Evaluation of automated analysis of 15N and total N in plant material and soil. Plant Soil 133, 83–92.CrossRefGoogle Scholar
  22. Johansen A, Jakobsen I and Jensen E S 1992 Hyphal transport of 15N-labelled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol. 122, 281–288.CrossRefGoogle Scholar
  23. Johansen A, Jakobsen I and Jensen E S 1993 External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. III. Hyphal transport of 32P and 15N. New Phytol. 124, 61–68.CrossRefGoogle Scholar
  24. Johansen A, Jakobsen I and Jensen E S 1994 Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels. Plant Soil 160, 1–9.CrossRefGoogle Scholar
  25. Johansen A, Finlay R and Olsson P A 1996 Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 133, 705–712.CrossRefGoogle Scholar
  26. Joner E J and Johansen A 2000 Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi. Mycol. Res. 104, 81–86.CrossRefGoogle Scholar
  27. Jones D L and Durrah P R 1993 Amino acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163, 1–12.Google Scholar
  28. Kielland K 1995 Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry. 31, 85–98.CrossRefGoogle Scholar
  29. Koske R E and Gemma J N 1989 A modified procedure for staining roots to detect VA mycorrhizas. Mycol. Res. 92, 486–505.Google Scholar
  30. Li X-L, George E and Marschner H 1991 Phosphorus depletion and pH decrease at the root- soil and hyphae- soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol. 119, 397–404CrossRefGoogle Scholar
  31. Lipson D A, Schadt CW, Schmidt S K and Monson R K 1999 Ectomycorrhizal transfer of amino acid-nitrogen to the alpine sedge Kobresia myosuroides. New Phytol. 142, 163–167.CrossRefGoogle Scholar
  32. Marschner H 1995 Mineral Nutrition of Higher Plants. Academic Press, London, UK. pp 229–312.Google Scholar
  33. McClure P R, Kochian L V, Spanswick R M and Shaff J E 1990 Evidence for cotransport of nitrate and protons in maize roots. II. Measurement of NO3+ and H+ fluxes with ion selective microelectrodes. Plant Physiol. 93, 290–294.PubMedGoogle Scholar
  34. Monreal C M and McGill W B 1985 Centrifugal extraction and determination of free amino acids in soil solutions by TLC using tritiated 1-fluoro-2,4-dinitrobenzene. Soil Biol. Biochem. 17, 533–539.CrossRefGoogle Scholar
  35. Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M and Högberg P 1998 Boreal forest plants take up organic nitrogen. Nature 392, 914–916.CrossRefGoogle Scholar
  36. Ozinga W A, Van Andel J and McDonnell-Alexander M P 1997 Nutritional soil heterogeneity and mycorrhiza as determinants of plant species diversity. Acta Bot. Neerl. 46, 237–254.Google Scholar
  37. Pearson J N and Jakobsen I 1993 The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P. New Phytol. 124, 489–494.CrossRefGoogle Scholar
  38. Read D J 1996 The structure and function of the ericoid mycorrhizal root. Ann. Bot. 77, 365–374.CrossRefGoogle Scholar
  39. Redecker D, Thierfelder H and Werner D 1995 A new cultivation system for arbuscular mycorrhizal fungi on glass beads. Angew. Bot. 69, 189–191.Google Scholar
  40. Roos W 1989 Kinetic properties, nutrient-dependent regulation and energy coupling of amino acid transport systems in Pennicillum cyclopium. Biochem. Biophys. Acta 978, 119–133.PubMedGoogle Scholar
  41. Sabbah S and Tal M 1990 Development of callus and suspension cultures of potato resistant to NaCl and mannitol and their response to stress. Plant Cell, Tiss. Org. Cult 21, 119–128.CrossRefGoogle Scholar
  42. Schobert C and Komor E 1987 Amino acid uptake by Ricinus communis roots: Characterization and physiological significance. Plant Cell Environ. 10, 493–500.CrossRefGoogle Scholar
  43. Scheller E 1996 Aminosäuregehalte von Ap-und Ah-Horizonten verschiedener Böden und deren Huminsäuren-und Fulvosäuren-Fraktion. Mitt. Dt. Bodenk. Ges. 81, 201–204.Google Scholar
  44. Smith S E, Gianinazzi-Pearson V, Koide R and Cairney J W G 1994 Nutrient transport in mycorrhizas: structure, physiology, and consequences for efficiency of the symbiosis. Plant Soil 159, 103–113.CrossRefGoogle Scholar
  45. Sophianopoulou V and Diallinas G 1995 Amino acid transporters of lower eukaryotes: regulation, structure and topogenesis. FEMS Microbiol. Rev. 16, 53–75.PubMedCrossRefGoogle Scholar
  46. St.-Arnaud M, Hamel C, Vimard B and Caron M, Fortin J A 1996 Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Myc. Res. 100, 328–332.CrossRefGoogle Scholar
  47. Tobar R M, Azcó n R and Barea J M 1994a The improvement of plant N acquisition from an ammonium-treated, droughtstressed soil by the fungal symbiont in arbuscular mycorrhizae. Mycorrhiza 4, 105–108.CrossRefGoogle Scholar
  48. Tobar R M, Azcó n R and Barea J M 1994b Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol. 126, 119–122.CrossRefGoogle Scholar
  49. Väre H, Vestberg M and Ohtonen 1997 Shifts in mycorrhiza and microbial activity along an oroartic altitudinal gradient in northern Fennoscandia. Artic Alp. Res. 93–104.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Heidi-Jayne Hawkins
    • 1
  • Anders Johansen
    • 2
  • Eckhard George
    • 3
  1. 1.Institute of Plant NutritionHohenheim UniversityStuttgartGermany
  2. 2.Department of Ecology and Molecular BiologyThe Royal Veterinary and Agricultural UniversityFrederiksberg C, CopenhagenDenmark
  3. 3.Institute of Plant NutritionHohenheim UniversityStuttgartGermany

Personalised recommendations