Plant and Soil

, Volume 285, Issue 1–2, pp 221–231 | Cite as

Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China

  • Xingliang Xu
  • Hua Ouyang
  • Yakov Kuzyakov
  • Andreas Richter
  • Wolfgang Wanek
ORIGINAL PAPER

Abstract

Though the potential of plants to take up organic N (e.g., amino acids) is well established, the true significance of organic N acquisition to plant N nutrition has not yet been quantified under field conditions. Here we demonstrate that organic N contributes significantly to the annual N uptake of three dominant plant species (Kobresia humilis, Saussurea superba and Stipa aliena) of alpine meadows on the Tibet Plateau, China. This was achieved by using double-labelled (14C and 15N) algae as a source for slow and continuous release of amino acids, and tracing both labels in the above- and below-ground plant biomass. Four months after addition of algae, between 0.5% and 2.6% of 14C and 5% and 14% of 15N from added algae were recovered in the plants, which translate into an uptake of organic N between 0.3 mg N m−2 and 1.5 mg N m−2. The calculated contribution of organic N to total N uptake was estimated to range between 21% and 35% for K. humilis, and between 13% and 21% for S. aliena and S. superba, respectively, implying that organic N uptake by grassland plants is quantitatively significant under field conditions in the studied alpine meadows. This finding has important ecological implications with regard to competition for organic N between microorganisms and plant roots.

Keywords

Organic N uptake 1415Alpine grassland N acquisition Spirulina 

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Notes

Acknowledgements

This research was supported by National Basic Research program of China (Grant No. 2005CB422005) and a fellowship for Dr. Xu awarded by the DAAD-K. C. Wong Foundation. We also thank Martin Werth for his help in improving this paper.

References

  1. 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
  2. Bremner JM (1965) Inorganic forms of nitrogen. Methods of soil analysis, vol 2. American Society of Agronomy, Black C A. Madison, pp 1179–1237Google Scholar
  3. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  4. Campanella L, Grecentini G, Avino P (1999) Chemical composition and nutritional evaluation of some natural and commercial food products based on Spirulina. Analusis 27:533–540CrossRefGoogle Scholar
  5. Cao GM, Zhang JX (2001) Soil nutrition and substance cycle of Kobresia meadow. In: Zhou XM (ed) Alpine Kobresia meadows in China. Science Press, Beijing, pp 199–206Google Scholar
  6. Chapin III FS, Moilainen L, Kielland K (1993) Preferential use of organic acid N by a non-mycorrhizal arctic sedge. Nature 361:150–153CrossRefADSGoogle Scholar
  7. Chen B, Zhou XM (1995) Analyses of niche breadths and overlaps of several plant species in three Kobresia communities of an alpine meadow. Acta Phytoecol Sin 22(3):158–169Google Scholar
  8. Chinese Soil Taxonomy Research Group (1995) Chinese soil taxonomy. Science Press, Beijing, China, pp 58–147Google Scholar
  9. Davidson EA, Eckert RW, Hart SC, Firestone MK (1989) Direct extraction of microbial biomass nitrogen from forest and grassland soils of California. Soil Biol Biochem 21:773–778CrossRefGoogle Scholar
  10. Heidi-Jayne H, Gabrielle W, David SW (2005) Cluster roots of Leucadendron laureolum (Proteaceae) and Lupinus albus (Fabaceae) take up glycine intact: an adaptive strategy to low mineral nitrogen in soils? Ann Bot 96(7):1275–1282CrossRefGoogle Scholar
  11. Hendrix DL (1984) Sugar uptake by cotton tissues. Plant Physiol 74:16–20PubMedCrossRefGoogle Scholar
  12. Jones DL (1999) Amino acid degradation and its potential effects on organic nitrogen capture by plants. Soil Biol Biochem 31:613–622CrossRefGoogle Scholar
  13. Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219CrossRefGoogle Scholar
  14. Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol Biochem 37:413–423CrossRefGoogle Scholar
  15. Jones DL, Shannon D, Murphy DV, Farrar J (2004) Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biol Biochem 36:749–756CrossRefGoogle Scholar
  16. Kalembasa SJ, Jenkinson DSA (1973) Comparative study of titrimetric and gravimetric methods for determination of organic carbon in soil. J Sci Food Agri 24:1085–1090Google Scholar
  17. Kassim GJ, Martin JP, Haider K (1981) Incorporation of a wide variety of organic substrate carbons into soil biomass as estimated by fumigation procedures. Soil Sci Soc Am J 45:1106–1112CrossRefGoogle Scholar
  18. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefGoogle Scholar
  19. Kielland K (1994) Amino acids absorption by arctic plants: implications for plant nutrition and N cycling. Ecology 75:2373–2383CrossRefGoogle Scholar
  20. Kuzyakov Y, Jones DL (2006) Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biol Biochem (in press)Google Scholar
  21. Kuzyakov Y, Ehrensberger H, Stahr K (2001) Carbon partitioning and below-ground translocation by Lolium perenne. Soil Biol Biochem 33:61–74CrossRefGoogle Scholar
  22. Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316CrossRefGoogle Scholar
  23. Lipson DA, Raab TK, Schmidt K, Monson K (2001) An empirical model of amino acid transformations in an alpine soil. Soil Biol Biochem 33:189–198CrossRefGoogle Scholar
  24. Maynard AB, Loosli JK (1969) Animal nutrition. McGraw-Hill, New YorkGoogle Scholar
  25. Merilä P, Smolander A, Strömmer R (2002) Soil nitrogen transformations along a primary succession transect on the land-uplift coast in western Finland. Soil Biol Biochem 34:373–385CrossRefGoogle Scholar
  26. 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
  27. Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36CrossRefGoogle Scholar
  28. Narasimha DLR, Venkataraman GS, Duggal SK, Eggum BO (1982) Nutritional quality of the blue-green alga Spirulina platensis geitler. J Sci Food Agric 33:456–460PubMedGoogle Scholar
  29. Näsholm T, Persson J (2001) Plant acquisition of organic N in boreal forests. Physiol Plant 111:419–426PubMedCrossRefGoogle Scholar
  30. Näsholm T, Ekbladm A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic N. Nature 392:914–916CrossRefADSGoogle Scholar
  31. Näsholm T, Huss-Danell K, Högberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:1155–1161CrossRefGoogle Scholar
  32. 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
  33. Persson J, Näsholm T (2003) Regulation of amino acid uptake by carbon and nitrogen in Pinus sylvestris. Planta 217:309–315PubMedGoogle Scholar
  34. Persson J, Högberg P, Ekblad A, Högberg MN, Nordgren A, Näsholm T (2003) Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137:252–257PubMedCrossRefGoogle Scholar
  35. Pruden G, Powlson DS, Jenkinson DS (1985) The measurement of 15N in soil and plant material. Fert Res 6:205–218CrossRefGoogle Scholar
  36. Raab TK, Lipson DA, Monson RM (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine Kobresia myosuroides: implications for the alpine N cycle. Oecologia 108:488–494CrossRefGoogle Scholar
  37. Raab TK, Lipson DA, Monson RM (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil process. Ecology 80:2408–2419CrossRefGoogle Scholar
  38. Schimel JP, Chapin III FE (1996) Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147CrossRefGoogle Scholar
  39. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602Google Scholar
  40. Schmidt EL, Putnam HD, Paul EA (1960) Behaviour of free amino acids in soil. Soil Sci Soc Am Proc 24:107–109CrossRefGoogle Scholar
  41. Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388CrossRefGoogle Scholar
  42. Wallenda T, Read DJ (1999) Kinectics of amino acid uptake by ectomycorrhizal roots. Plant Cell Eviron 22:179–187CrossRefGoogle Scholar
  43. Wang QJ, Shi SB (2001) Biomass and productive mechanism of Kobresia meadow. In: Zhou XM (ed) Alpine Kobresia meadows in China. Science Press, Beijing, China, pp 131–162Google Scholar
  44. Wang YQ, Shan AS (2003) Application of Spirulina in animal agriculture. Food Res 10:22–24Google Scholar
  45. Weigelt A, Bol R, Bardgett R (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635PubMedCrossRefGoogle Scholar
  46. WRB (1998) World reference base for soil resources. FAO/ISRIC/ISSS, RomeGoogle Scholar
  47. Xu XL, Ouyang H, Cao GM, Pei ZY, Zhou CP (2004) Uptake of organic nitrogen by eight dominant plant species in Kobresia meadows. Nutr Cycl Agroecosyst 69:5–10CrossRefGoogle Scholar
  48. Zarouk C (1966) Contribution A Lȁ9etude Dȁ9une cyanophyceae. (Influence de divers facteurs physiques el chimiques sur la croissance et la photosynthese de Spirulina maxima (Setch et Gardna) Geitler. PhD Thesis, University of Paris, FranceGoogle Scholar
  49. Zhou XM (2001) Main types and their distribution patterns of Kobresia meadow. In: Zhou XM (ed) Alpine Kobresia meadows in China. Science Press, Beijing, China, pp 51–62Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Xingliang Xu
    • 1
    • 2
  • Hua Ouyang
    • 1
  • Yakov Kuzyakov
    • 2
    • 4
  • Andreas Richter
    • 3
  • Wolfgang Wanek
    • 3
  1. 1.Institute of Geographical Sciences & Natural Resources ResearchThe Chinese Academy of SciencesBeijingPR China
  2. 2.Institute of Soil Science and Land EvaluationUniversity of HohenheimStuttgartGermany
  3. 3.Department of Chemical Ecology and Ecosystem ResearchVienna Ecology Centre University of ViennaWienAustria
  4. 4.Department of Agroecosystem ResearchUniversity of BayreuthD-95440 BayreuthGermany

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