, Volume 142, Issue 4, pp 627–635 | Cite as

Preferential uptake of soil nitrogen forms by grassland plant species

  • Alexandra Weigelt
  • Roland Bol
  • Richard D. Bardgett
Ecosystem Ecology


In this study, we assessed whether a range of temperate grassland species showed preferential uptake for different chemical forms of N, including inorganic N and a range of amino acids that commonly occur in temperate grassland soil. Preferential uptake of dual-labelled (13C and 15N) glycine, serine, arginine and phenylalanine, as compared to inorganic N, was tested using plants growing in pots with natural field soil. We selected five grass species representing a gradient from fertilised, productive pastures to extensive, low productivity pastures (Lolium perenne, Holcus lanatus, Anthoxanthum odoratum, Deschampsia flexuosa, and Nardus stricta). Our data show that all grass species were able to take up directly a diversity of soil amino acids of varying complexity. Moreover, we present evidence of marked inter-species differences in preferential use of chemical forms of N of varying complexity. L. perenne was relatively more effective at using inorganic N and glycine compared to the most complex amino acid phenylalanine, whereas N. stricta showed a significant preference for serine over inorganic N. Total plant N acquisition, measured as root and shoot concentration of labelled compounds, also revealed pronounced inter-species differences which were related to plant growth rate: plants with higher biomass production were found to take up more inorganic N. Our findings indicate that species-specific differences in direct uptake of different N forms combined with total N acquisition could explain changes in competitive dominance of grass species in grasslands of differing fertility.


Amino acids Grasses Stable isotopes Lolium perenne 



We thank Helen Quirk for laboratory assistance. This work was supported by a grant from the Biotechnology and Biological Sciences Research Council awarded to R.B. (34/D10205). We are grateful to David Wardle and two anonymous reviewers for providing critical comments on an earlier version of the manuscript.


  1. Alef K, Kleiner D (1986) Arginine ammonification, a simple method to estimate the microbial activity potential in soils. Soil Biol Biochem 18:233–235CrossRefGoogle Scholar
  2. Bajwa R, Read DJ (1985) The biology of mycorrhiza in the Ericaceae IX. Peptides as nitrogen sources for the ericoid endophyte and for mycorrhizal and non-mycorrhizal plants. New Phytol 101:459–467Google Scholar
  3. Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic nitrogen inputs to temperate grasslands. Ecology 84:1277–1287Google Scholar
  4. Blaudez D, Botton B, Dizengremel P, Chalot M (2001) The fate of [14C] glutamate and [14C] malate in birch roots is strongly modified under inoculation with Paxillus involutus. Plant Cell Environ 24:449–457CrossRefGoogle Scholar
  5. Chapin FS III, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361:150–153CrossRefGoogle Scholar
  6. Cliquet JB, Murray PJ, Boucaud J (1997) Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne. New Phytol 137:345–349CrossRefGoogle Scholar
  7. Falkengren-Grerup U, Månsson KF, Olsson MO (2000) Uptake capacity of amino acids by ten grasses and forbs in relation to soil acidity and nitrogen availability. Environ Exp Bot 44:207–219CrossRefPubMedGoogle Scholar
  8. Henry HAL, Jefferies RL (2003a) Interactions in the uptake of amino acids, ammonium and nitrate ions in the Arctic salt-marsh grass, Puccinella phryganodes. Plant Cell Environ 26:419–428Google Scholar
  9. Henry HAL, Jefferies RL (2003b) Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed Arctic salt marsh. J Ecol 91:627–636CrossRefGoogle Scholar
  10. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol 139:479–494CrossRefGoogle Scholar
  11. Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820CrossRefGoogle Scholar
  12. Kielland K (1994) Amino acid absorption by arctic plants: implication for plant nutrition and nitrogen cycling. Ecology 75:2373–2383Google Scholar
  13. Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98CrossRefGoogle Scholar
  14. Lipson DA, Monson RK (1998) Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events. Oecologia 113:406–414CrossRefGoogle Scholar
  15. Lipson DA, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316CrossRefGoogle Scholar
  16. Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fertil Soils 29:257–261CrossRefGoogle Scholar
  17. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetterk EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 413:68–71CrossRefGoogle Scholar
  18. Miller AE, Bowman WD (2002) Variation in nitrogen-15 natural abundance and nitrogen uptake traits among co-occurring alpine species: do species partition by nitrogen form? Oecologia 130:609–616CrossRefGoogle Scholar
  19. Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292CrossRefGoogle Scholar
  20. Näsholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal forests. Physiol Plant 111:419–426CrossRefPubMedGoogle Scholar
  21. Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916CrossRefGoogle Scholar
  22. Näsholm T, Huss-Danell K, Högberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:1155–1161Google Scholar
  23. Näsholm T, Huss-Danell K, Högberg P (2001) Uptake of glycine by field grown wheat. New Phytol 150:59–63CrossRefGoogle Scholar
  24. Nordin A, Högberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132CrossRefGoogle Scholar
  25. Öhlund J, Näsholm T (2001) Growth of conifer seedlings on organic and inorganic nitrogen sources. Tree Physiol 21:1319–1326PubMedGoogle Scholar
  26. Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 33:651–657CrossRefGoogle Scholar
  27. Persson J, Näsholm T (2001) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4:434–438CrossRefGoogle Scholar
  28. Raab TK, Lipson DA, Monson RK (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosuroides: implications for the alpine nitrogen cycle. Oecologia 108:488–494CrossRefGoogle Scholar
  29. Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil processes. Ecology 80:2408–2419Google Scholar
  30. Rodwell JS (1992) Grasslands and montane communities. Cambridge University Press, CambridgeGoogle Scholar
  31. Schiller P, Heilmeier H, Hartung W (1998) Uptake of amino acids by the aquatic resurrection plant Chameagigas intrepidus and its implication for N nutrition. Oecologia 117:63–69CrossRefGoogle Scholar
  32. Schimel JP, Chapin FS III (1996) Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147Google Scholar
  33. Schmidt S, Stewart GR (1999) Glycine metabolism by plant roots and its occurrence in Australian plant communities. Aust J Plant Physiol 26:253–264Google Scholar
  34. Schobert C, Köckenberger W, Komor E (1988) Uptake of amino acids by plants from soil: a comparative study with castor bean seedlings grown under natural and axenic soil conditions. Plant Soil 109:181–188Google Scholar
  35. Streeter TC, Bol R, Bardgett RD (2000) Amino acids as a nitrogen source in temperate upland grasslands: the use of dual labelled (13C, 15N) glycine to test for direct uptake by dominant grasses. Rapid Commun Mass Spectrom 14:1351–1355CrossRefPubMedGoogle Scholar
  36. Stribley DP, Read DJ (1980) The biology of mycorrhiza in the Ericaceae. VII. The relationship between mycorrhizal infection and the capacity to utilize simple and complex organic nitrogen sources. New Phytol 86:365–371Google Scholar
  37. Thornton B (2001) Uptake of glycine by non-mycorrhizal Lolium perenne. J Exp Bot 52:1315–1322CrossRefPubMedGoogle Scholar
  38. Turnbull MH, Schmidt S, Erskine PD, Richards S, Stewart GR (1996) Root adaption and nitrogen source acquisition in natural ecosystems. Tree Physiol 16:941–948PubMedGoogle Scholar
  39. Weigelt A, King R, Bol R, Bardgett RD (2003) Inter-specific variability in organic nitrogen uptake of three temperate grassland species. J Plant Nutr Soil Sci 166:606–611CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Alexandra Weigelt
    • 3
  • Roland Bol
    • 2
  • Richard D. Bardgett
    • 1
  1. 1.Institute of Environmental and Natural SciencesLancaster UniversityLancasterUK
  2. 2.Soil Science and Environmental Quality TeamInstitute of Grassland and Environmental ResearchOkehamptonUK
  3. 3.Chair of BiogeographyUniversity of BayreuthBayreuthGermany

Personalised recommendations