Skip to main content
SpringerLink
Log in

Light affects competition for inorganic and organic nitrogen between maize and rhizosphere microorganisms

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Effects of light on the short term competition for organic and inorganic nitrogen between maize and rhizosphere microorganisms were investigated using a mixture of amino acid, ammonium and nitrate under controlled conditions. The amount and forms of N added in the three treatments was identical, but only one of the three N forms was labeled with 15N. Glycine was additionally labeled with 14C to prove its uptake by maize and incorporation into microbial biomass in an intact form. Maize out-competed microorganisms for \(^{15} {\text{NO}}_3^ - \) during the whole experiment under low and high light intensity. Microbial uptake of 15N and 14C was not directly influenced by the light intensity, but was indirectly related to the impact the light intensity had on the plant. More \(^{15} {\text{NH}}_4^ + \) was recovered in microbial biomass than in plants in the initial 4 h under the two light intensities, although more 15N-glycine was incorporated into microbial biomass than in plants in the initial 4 h under low light intensity. Light had a significant effect on \(^{15} {\text{NO}}_3^ - \) uptake by maize, but no significant effects on the uptake of \(^{15} {\text{NH}}_4^ + \) or 15N-glycine. High light intensity significantly increased plant uptake of \(^{15} {\text{NO}}_3^ - \) and glycine 14C. Based on 14C to 15N recovery ratios of plants, intact glycine contributed at least 13% to glycine-derived nitrogen 4 h after tracer additions, but it contributed only 0.5% to total nitrogen uptake. These findings suggest that light intensity alters the competitive relationship between maize roots and rhizosphere microorganisms and that C4 cereals such as maize are able to access small amounts of intact glycine. We conclude that roots were stronger competitor than microorganisms for inorganic N, but microorganisms out competed plants during a short period for organic N, which was mineralized into inorganic N within a few hours of application to the soil and was thereafter available for root uptake.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–55

    CAS  Google Scholar 

  • Anderson TH, Domsch KH (1985) Determination of ecophysiological maintenance carbon requirements of soil microorganisms in a dormant state. Biol Fert Soils 1:81–89

    Article  CAS  Google Scholar 

  • Aslam M, Travis RL, Huffaker RC (1992) Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiol 99:1124–1133

    PubMed  CAS  Google Scholar 

  • Bardgett RD, Steeter TC, Bol R (2003) Soil microorganisms compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1387

    Article  Google Scholar 

  • Baligar V, Fagerian NK, Paiva AQ, Silveiraa A, Pomellaa WV, Machado RCR (2006) Light intensity effects on growth and micronutrient uptake by tropical legume crops. J Plant Nutr 29:1959–1974

    Article  CAS  Google Scholar 

  • Beevers L, Schrader LE, Flesher D, Hageman RH (1965) Role of light and nitrate in the induction of nitrate reductase in radish cotyledons and maize seedlings. Plant Physiol 40:691–698

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chapin FS III, Moilanen L, Kielland K (1993) Preferential usage of organic nitrogen for growth by a nonmycorrhizal sedge. Nature 361:150–152

    Article  CAS  Google Scholar 

  • Cheng XM, Bledsoe CS (2004) Competition for inorganic and organic N by blue oak (Quercus douglasii) seedlings, an annual grass, and soil microorganisms in a pot study. Soil Biol Biochem 36:135–144

    Article  CAS  Google Scholar 

  • Chintu R, Zaharah A (2003) Nitrogen uptake of maize (Zea mays. L) from isotope-labeled biomass of Paraserianthes falcataria grown under controlled conditions. Agroforest Syst 57:101–107

    Article  Google Scholar 

  • De Montard FX, Rapey H, Delpy R, Massey P (1999) Competition for light, water and nitrogen in an association of hazel (Corylus avellana L.) and cocksfoot (Dactylis glomerata L.). Agroforest Syst 43:135–150

    Article  Google Scholar 

  • FAO (2000) FAOSTAT, Database Records, http://apps.fao.org./page/form?collection

  • Glass ADM, Siddiqi MY (1995) Nitrogen Absorption by plant roots. In: Srivastava H, Singh R (eds) Nitrogen nutrition in higher plants. Associated, New Dehli, India, pp 21–56

    Google Scholar 

  • Grime JP (1979) Plant strategies and vegetation processes. Wiley, Chichester, UK

    Google Scholar 

  • Haynes RJ (1986) Mineral nitrogen in the plant-soil System. Academic, Orlando, FL, USA

    Google Scholar 

  • Henry HAL, Jefferies RL (2003) Interactions in the uptake of amino acids, ammonium and nitrate ions in the Arctic salt-marsh grass, Puccinellia phryganodes. Plant Cell Environ 26:419–428

    Article  CAS  Google Scholar 

  • Hodge A, Stewart GR, Robinson D, Griffiths BS, Fitter AH (1999) Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biol Biochem 31:1517–1530

    Article  CAS  Google Scholar 

  • Holt JS (1995) Plant-response to light—a potential tool for weed management. Weed Sci 43(3):474–482

    CAS  Google Scholar 

  • Jackson LE, Schimel JP, Firestone MK (1989) Short-term partitioning of ammonium and nitrate between plants and microorganisms in an annual grassland. Soil Biol Biochem 21:409–415

    Article  Google Scholar 

  • Jaeger CH III, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms In an alpine ecosystem. Ecology 80:1883–1891

    Article  Google Scholar 

  • Joergensen RG (1996) The fumigation–extraction method to estimate soil microbial biomass: calibration of the K EC values. Soil Biol Biochem 28:25–31

    Article  CAS  Google Scholar 

  • Jones DL (1999) Amino acid degradation and its potential effects on organic nitrogen capture by plants. Soil Biol Biochem 31:613–622

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Amino acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163:1–12

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480

    Article  CAS  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    Article  Google Scholar 

  • Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383

    Article  Google Scholar 

  • Kirkham D, Bartholomew WV (1954) Equations for following nutrients transformations in soil, utilizing tracer data. Soil Sci Soc Am Proc 18:33–34

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33(14):1915–1925

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Cheng W (2004) Photosynthesis controls of CO2 efflux from maize rhizosphere. Plant Soil 263(1):85–99

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Demin V (1998) CO2 efflux by rapid decomposition of low molecular organic substances in soils. Sci Soils 3:2

    Article  Google Scholar 

  • Lillo C (1994) Light regulation of nitrate reductase in green leaves of higher plants. Physiol Plantarum 90:616–620

    Article  CAS  Google Scholar 

  • 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 113:406–414

    Article  Google Scholar 

  • Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microorganisms for specific amino acids. Biol Fert Soil 29:257–261

    Article  CAS  Google Scholar 

  • Loomis RS, Connor DJ (1992) Crop ecology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Matsumoto S, Ae N, Yamagata M (2000) Possible direct uptake of organic nitrogen from soil by chingensai (Brassica campestris L.) and carrot (Daucus carota L.). Soil Biol Biochem 32:1301–1310

    Article  CAS  Google Scholar 

  • McFarland JW, Ruess RW, Kielland K, Doyle AP (2002) Cycling dynamics of \({\text{NH}}_4^ + \) and amino acid nitrogen in soils of a deciduous boreal forest ecosystems. Ecosystems 5:775–788

    CAS  Google Scholar 

  • Meharg AA (1994) A critical review of labelling techniques used to quantify rhizosphere carbon-flow. Plant Soil 166:55–62

    Article  CAS  Google Scholar 

  • Melin E, Nilsson H (1953) Transfer of labeled nitrogen from glutamic acid to pine seedlings through the mycelium of Boletus variegatus (Sw) Fr. Nature 171:134

    Article  PubMed  CAS  Google Scholar 

  • Mengel K, Kirkby EA (1987) Principles of plant nutrition. International Potash Institute, Place of publication, p 366

  • Meshram SU, Shende ST (1982) Total nitrogen uptake by maize with Azotobacter inoculation. Plant Soil 69:275–280

    Article  CAS  Google Scholar 

  • Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Article  CAS  Google Scholar 

  • Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88(7):1832–1840

    Article  PubMed  Google Scholar 

  • Näsholm T, Huss-Danell K, Högberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:115–1161

    Google Scholar 

  • Näsholm T, Huss-Danell K, Högberg P (2001) Uptake of glycine by field grown wheat. New Phytol 150:59–63

    Article  Google Scholar 

  • Näsholm T, Ekbladm A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic N. Nature 392:914–916

    Article  Google Scholar 

  • Nordin A, Schmidt IK, Shaver GR (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85:955–962

    Article  Google Scholar 

  • Okamoto M, Okada K (2004) Differential responses of growth and nitrogen uptake to organic nitrogen in four gramineous crops. J Experim Bot 55:1577–1585

    Article  CAS  Google Scholar 

  • Olff H, Huisman J, Van Tooren BF (1993) Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. J Ecol 81:693–706

    Article  Google Scholar 

  • 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 33:651–657

    Article  CAS  Google Scholar 

  • Passarge J, Hol S, Escher M, Huisman J (2006) Competition for nutrients and light: stable coexistence, alternative stable states, or competitive exclusive? Ecology 76:57–72

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil progresses. Ecology 80(7):2408–2419

    Google Scholar 

  • Raghuram N, Chandok MR, Sopory SK (1999) Light regulation of nitrate reductase gene expression in maize involves a G-protein. Mol Cell Biol Res Commun 2:86–90

    Article  PubMed  CAS  Google Scholar 

  • Raven JA (2003) Can plants rely on nitrate? Trends Plant Sci 8:314–315

    Article  PubMed  CAS  Google Scholar 

  • Schimel JP, Chapin FS III (1996) Tundra plant uptake of amino acid and \({\text{NH}}_4^ + \) nitrogen in situ: plants compete well for amino acid N. Ecology 77:2142–2147

    Article  Google Scholar 

  • Schimel JP, Jackson LE, Firestone MK (1989) Spatial and temporal effects on plant–microbial competition for inorganic nitrogen in a California annual grassland. Soil Biol Biochem 21:1059–1066

    Article  CAS  Google Scholar 

  • Schippers P, Kropff MJ (2001) Competition for light and nitrogen among grassland species: a simulation analysis. Funct Ecol 15:155–164

    Article  Google Scholar 

  • Schortemeyer M, Feil B, Stamp P (1993) Root morphology and nitrogen uptake of maize simultaneously supplied with ammonium and nitrate in a split-root system. Ann Bot 72:107–115

    Article  CAS  Google Scholar 

  • Shobert C, Komor E (1987) Amino acid uptake by Ricinus communis roots: characterisation and physiological significance. Plant Cell Environ 10:493–500

    Article  Google Scholar 

  • Smith JL, Paul EA (1990) The significance of soil microbial biomass estimations. In: Bollag J, Stotzky G (eds) Soil biochemistry. Marcel Dekker, New York, pp 357–393

    Google Scholar 

  • Sollins P, Glassman C, Paul EA, Swantson C, Lajtha K, Heil JW, Elliott ET (1999) Soil carbon and nitrogen pools and fractions. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 89–105

    Google Scholar 

  • Stange CF, Spott O, Apelt B, Russow R (2007) Automated and rapid online determination of 15N abundance and concentration of ammonium, nitrite or nitrate in aqueous samples by the SPINMAS technique. Isot Environ Healt S 43(3):227–236

    Article  CAS  Google Scholar 

  • Strengbom J, Näsholm T, Ericson L (2004) Light, not nitrogen, limits growth of the grass Deschampsia flexuosa in boreal forests. Can J Bot 82:430–435

    Article  Google Scholar 

  • Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant Cell Environ 28:813–821

    Article  CAS  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press

  • Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton

  • Uren NC (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. The rhizosphere. Marcel Dekker, New York, pp 19–40

    Google Scholar 

  • Virtanen AI, Linkola H (1946) Organic nitrogen compounds as nitrogen nutrition for higher plants. Nature 157:515

    Article  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and sea: how can it occur? Biogeochemistry 5:7–34

    Article  Google Scholar 

  • Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635

    Article  PubMed  Google Scholar 

  • Xu XL, Ouyang H, Cao GM, Pei ZY, Zhou CP (2004) Uptake of organic nitrogen by eight dominant plant species in Kobreasia meadows. Nutr Cycl Agroecosys 69:5–10

    Article  CAS  Google Scholar 

  • Xu XL, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant species in an alpine meadow on the Tibet Plateau, China. Plant Soil 285:221–231

    Article  CAS  Google Scholar 

  • Yamagata M, Ae N (1999) Direct acquisition of organic N by crops. JARQ 33:13–21

    Google Scholar 

  • Yano Y, McDowell WH, Kinner NE (1998) Quantification of biodegradable dissolved organic carbon in soil solution with flow-through bioreactors. Soil Sci Soc Am J 62:1556–1564

    Article  CAS  Google Scholar 

  • Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant-microbe competition for nitrogen in northern hardwood forests. Ecology 71:651–656

    Article  Google Scholar 

  • Zogg GP, Zak DR, Pregitzer KS, Burton AJ (2000) Microbial immobilization and the retention of anthropogenic nitrate in a northern hardwood forest. Ecology 81:1858–1866

    Article  Google Scholar 

Download references

Acknowledgements

We kindly thank DAAD K. C. Wong Fellowships for awarding Dr. Xu a fellowship to support this study in University of Hohenheim (Germany). The German Research Foundation supported the study. We also thank the two anonymous reviewers for their helpful comments and Rebecca Hood for language improvement.

Author information

Authors and Affiliations

  1. Institute of Soil Science and Land Evaluation, University of Hohenheim, Emil-Wolff-Strasse 27, 70599, Stuttgart, Germany

    Xingliang Xu & Yakov Kuzyakov

  2. Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources Research, The Chinese Academy of Sciences, P.O. Box 9719, Beijing, 100101, People’s Republic of China

    Xingliang Xu

  3. Helmholtz Centre for Environmental Research-UFZ, Department of Soil Physics, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany

    Claus Florian Stange

  4. Department of Chemical Ecology and Ecosystem Research, Vienna Ecology Centre University of Vienna, Althanstrasse 14, A-1090, Wien, Austria

    Andreas Richter & Wolfgang Wanek

  5. Department of Agroecosystem Research, University of Bayreuth, 95440, Bayreuth, Germany

    Yakov Kuzyakov

Authors
  1. Xingliang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claus Florian Stange
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreas Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wolfgang Wanek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yakov Kuzyakov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingliang Xu.

Additional information

Responsible Editor: Angela Hodge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, X., Stange, C.F., Richter, A. et al. Light affects competition for inorganic and organic nitrogen between maize and rhizosphere microorganisms. Plant Soil 304, 59–72 (2008). https://doi.org/10.1007/s11104-007-9519-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-007-9519-7

Keywords

Search

Navigation