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.
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References
Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287
Bremner JM (1965) Inorganic forms of nitrogen. Methods of soil analysis, vol 2. American Society of Agronomy, Black C A. Madison, pp 1179–1237
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 17:837–842
Campanella L, Grecentini G, Avino P (1999) Chemical composition and nutritional evaluation of some natural and commercial food products based on Spirulina. Analusis 27:533–540
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 199–206
Chapin III FS, Moilainen L, Kielland K (1993) Preferential use of organic acid N by a non-mycorrhizal arctic sedge. Nature 361:150–153
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):158–169
Chinese Soil Taxonomy Research Group (1995) Chinese soil taxonomy. Science Press, Beijing, China, pp 58–147
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 21:773–778
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):1275–1282
Hendrix DL (1984) Sugar uptake by cotton tissues. Plant Physiol 74:16–20
Jones DL (1999) Amino acid degradation and its potential effects on organic nitrogen capture by plants. Soil Biol Biochem 31:613–622
Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219
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 37:413–423
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 36:749–756
Kalembasa SJ, Jenkinson DSA (1973) Comparative study of titrimetric and gravimetric methods for determination of organic carbon in soil. J Sci Food Agri 24:1085–1090
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 45:1106–1112
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
Kielland K (1994) Amino acids absorption by arctic plants: implications for plant nutrition and N cycling. Ecology 75:2373–2383
Kuzyakov Y, Jones DL (2006) Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biol Biochem (in press)
Kuzyakov Y, Ehrensberger H, Stahr K (2001) Carbon partitioning and below-ground translocation by Lolium perenne. Soil Biol Biochem 33:61–74
Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316
Lipson DA, Raab TK, Schmidt K, Monson K (2001) An empirical model of amino acid transformations in an alpine soil. Soil Biol Biochem 33:189–198
Maynard AB, Loosli JK (1969) Animal nutrition. McGraw-Hill, New York
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 34:373–385
Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292
Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36
Narasimha DLR, Venkataraman GS, Duggal SK, Eggum BO (1982) Nutritional quality of the blue-green alga Spirulina platensis geitler. J Sci Food Agric 33:456–460
Näsholm T, Persson J (2001) Plant acquisition of organic N in boreal forests. Physiol Plant 111:419–426
Näsholm T, Ekbladm A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic N. Nature 392:914–916
Näsholm T, Huss-Danell K, Högberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:1155–1161
Nordin A, Högberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132
Persson J, Näsholm T (2003) Regulation of amino acid uptake by carbon and nitrogen in Pinus sylvestris. Planta 217:309–315
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 137:252–257
Pruden G, Powlson DS, Jenkinson DS (1985) The measurement of 15N in soil and plant material. Fert Res 6:205–218
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 108:488–494
Raab TK, Lipson DA, Monson RM (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil process. Ecology 80:2408–2419
Schimel JP, Chapin III FE (1996) Tundra plant uptake of amino acid and NH +4 nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602
Schmidt EL, Putnam HD, Paul EA (1960) Behaviour of free amino acids in soil. Soil Sci Soc Am Proc 24:107–109
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 164:383–388
Wallenda T, Read DJ (1999) Kinectics of amino acid uptake by ectomycorrhizal roots. Plant Cell Eviron 22:179–187
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 131–162
Wang YQ, Shan AS (2003) Application of Spirulina in animal agriculture. Food Res 10:22–24
Weigelt A, Bol R, Bardgett R (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635
WRB (1998) World reference base for soil resources. FAO/ISRIC/ISSS, Rome
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 69:5–10
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, France
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 51–62
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.
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Xu, X., Ouyang, H., Kuzyakov, Y. et al. Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285, 221–231 (2006). https://doi.org/10.1007/s11104-006-9007-5
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DOI: https://doi.org/10.1007/s11104-006-9007-5