Skip to main content
SpringerLink
Log in

Root uptake of inorganic and organic N chemical forms in two coexisting Mediterranean forest trees

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

Abstract

Background and aims

Plants differ in their ability to use different nitrogen (N) chemical forms, these differences can be related to their ecology and drive community structure. The capacity to uptake intact organic N has been observed in plants of several ecosystems. However, soil organic N uptake by Mediterranean plants is unknown despite organic N being abundant in Mediterranean ecosystems. We compare the uptake of different N forms in two widespread coexisting Mediterranean forest trees with contrasting ecophysiological characteristics: Quercus ilex and Pinus halepensis.

Methods

To estimate root uptake rate of each N form we used equimolar solutions (1 mM N) of 15NO3 −, 15NH4 + and 15N-13C glycine.

Results

NH4 + and glycine were taken up at a similar rate, but faster than NO3 − in both species. Intact dual labeled glycine was found in both species, demonstrating that both species can absorb intact organic N.

Conclusions

Despite their ecological differences, both species had similar preference for N forms suggesting no fundamental niche complementarity for N uptake. The higher preference for NH4 + and glycine over NO3 − possibly reflects adaptation to the differing proportions of N forms in Mediterranean soils.

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

Similar content being viewed by others

References

  • Aidar MPM, Schmidt S, Moss G et al (2003) Nitrogen use strategies of neotropical rainforest trees in threatened Atlantic Forest. Plant Cell Environ 26:389–399

    Article  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260

    Article  PubMed  Google Scholar 

  • Baquedano FJ, Castillo FJ (2006) Comparative ecophysiological effects of drought on seedling of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera and Quercus ilex. Trees 20:689–700

    Article  Google Scholar 

  • Bonilla D, Rodá F (1992) Soil nitrogen dynamics in a holm oak forest. Vegetatio 99:247–257

    Article  Google Scholar 

  • Boudsocq S, Niboyet A, Lata JC et al (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–69

    Article  CAS  PubMed  Google Scholar 

  • Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44

    Article  CAS  PubMed  Google Scholar 

  • Cruz C, Lips SH, Martins-Loução MA (1993) Interactions between nitrate and ammonium during uptake by carob seedlings and the effect of the form of earlier nitrogen nutrition. Physiol Plant 89:544–551

    Article  CAS  Google Scholar 

  • Delgado-Baquerizo M, Covelo F, Gallardo A (2011) Dissolved organic nitrogen in Mediterranean ecosystems. Pedosphere 21:309–318

    Article  CAS  Google Scholar 

  • Dias T, Clemente A, Martins-Loução MA et al (2014) Ammonium as a driving force of plant diversity and ecosystem functioning: observations based on 5 years´ manipulation of N dose and form in a Mediterranean ecosystem. PLoS One 9:e92517

    Article  PubMed  PubMed Central  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. PNAS 104:8902–8906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship. Ecology 87:1244–1255

    Article  PubMed  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 

  • Kielland K, McFarland J, Olson K (2006) Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288:297–307

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM, Britto DT (2003) Root ammonium transport efficiency as a determinant in forest colonization patterns: an hypothesis. Physiol Plant 117:164–170

    Article  CAS  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Li X, Rennenberg H, Simon J (2015) Competition for nitrogen between Fagus sylvatica and Acer pseudoplatanus seedlings depends on soil nitrogen availability. Front Plant Sci 6:1–11

    Google Scholar 

  • McKane RB, Johnson LC, Shaver GR et al (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  CAS  PubMed  Google Scholar 

  • Metcalfe RJ, Nault J, Hawkins BJ (2011) Adaptations to nitrogen form: comparing inorganic nitrogen and amino acid availability and uptake by four temperate forest plants. Can J For Res 1637:1626–1637

    Article  Google Scholar 

  • Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250(2):283–292

  • Nasholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal forests. Physiol Plant 111:419–426

    Article  CAS  PubMed  Google Scholar 

  • Näsholm T, Ekblad A, Nordin A et al (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916

    Article  Google Scholar 

  • Näsholm T, Huss-Danell K, Högberg P, Hogberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:1155–1161

    Article  Google Scholar 

  • Osone Y, Tateno M (2005) Nitrogen absorption by roots as a cause of interspecific variations in leaf nitrogen concentration and photosynthetic capacity. Funct Ecol 19:460–470

    Article  Google Scholar 

  • Pemán J, Navarro RM, Nicolás JL, et al. (2014) Producción y manejo de semillas y plantas forestales. OAPN. Ministerio de Agricultura, Alimentación y Medio Ambiente. Madrid

  • Persson J, Näsholm T (2001) A GC-MS method for determination of amino acid uptake by plants. Physiol Plant 113:352–358

    Article  CAS  PubMed  Google Scholar 

  • Persson J, Högberg P, Ekblad A et al (2003) Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137:252–257

    Article  PubMed  Google Scholar 

  • Sánchez-Gómez D, Valladares F, Zavala MA (2006) Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytol 170:795–806

    Article  PubMed  Google Scholar 

  • Sardans J, Rodà F, Peñuelas J (2006) Effects of a nutrient pulse supply on nutrient status of the Mediterranean trees Quercus ilex subsp. ballota and Pinus halepensis on different soils and under different competitive pressure. Trees 20:619–632

    Article  Google Scholar 

  • Schulz H, Härtling S, Stange CF (2011) Species-specific differences in nitrogen uptake and utilization by six European tree species. J Plant Nutr Soil Sci 174:28–37

    Article  CAS  Google Scholar 

  • Sharp Z (2005) Principles of Stable Isotope Geochemistry. Pearson/Prentice Hall, 2007

  • Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. W. H. Freeman, New York

    Google Scholar 

  • Song M, Zheng L, Suding KN et al (2015) Plasticity in nitrogen form uptake and preference in response to long-term nitrogen fertilization. Plant Soil 394:215–224

    Article  CAS  Google Scholar 

  • Svennerstam H, Jämtgård S, Ahmad I et al (2011) Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytol 191:459–467

    Article  CAS  PubMed  Google Scholar 

  • Uscola M, Oliet JA, Villar-Salvador P et al (2014a) Nitrogen form and concentration interactively affect the performance of two ecologically distinct Mediterranean forest trees. Eur J For Res 133:235–246

    Article  CAS  Google Scholar 

  • Uscola M, Villar-Salvador P, Oliet J, Warren CR (2014b) Foliar absorption and root translocation of nitrogen from different chemical forms in seedlings of two Mediterranean trees. Environ Exp Bot 104:34–43

    Article  CAS  Google Scholar 

  • Uscola M, Villar-Salvador P, Gross P, Maillard P (2015) Fast growth involves high dependence on stored resources in seedlings of Mediterranean evergreen trees. Ann Bot 115:1001–1013

    Article  PubMed  PubMed Central  Google Scholar 

  • Warren CR (2006) Potential organic and inorganic N uptake by six eucalyptus species. Funct Plant Biol 33:653

    Article  CAS  Google Scholar 

  • Warren CR (2012) Post-uptake metabolism affects quantification of amino acid uptake. New Phytol 193:522–531

    Article  CAS  PubMed  Google Scholar 

  • Warren CR, Adams MA (2002) Possible causes of slow growth of nitrate-supplied Pinus pinaster. Can J For Res 32:569–580

    Article  Google Scholar 

  • Zavala MA, Espelta JM, Retana J (2000) Constraints and trade-offs in Mediterranean plant communities: the case of holm oak-Aleppo pine forests. Bot Rev 66:119–149

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to C.N. R.G. F. “El Serranillo” (MAGRAMA) for cultivating the plants. This study was supported by a FPU-MEC grant to MU, and by projects AGL2006-12609-C02-01/FOR (ENCINUT), AGL2011-24296 ECOLPIN (MICIIN), CGL2014-53308-P SERAVI (MINECO) and Remedinal 3 (S2013/MAE-2719, CAM). CW was supported by a Future Fellowship from the Australian Research Council (FT100100024).

Author information

Author notes

  1. M. Uscola

    Present address: Hardwood Tree Improvement and Regeneration Center, Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, 47907-2061, USA

Authors and Affiliations

  1. Forest Ecology and Restoration Group, Departamento de Ciencias de la Vida, U.D. Ecología, Universidad de Alcalá, Apdo. 20, E-28805, Alcalá de Henares, Madrid, Spain

    M. Uscola & P. Villar-Salvador

  2. E.T.S. Ingenieros de Montes, Departamento de Sistemas y Recursos Naturales, Universidad Politécnica de Madrid, 28040, Madrid, Spain

    J. Oliet

  3. School of Life and Environmental Sciences, Heydon-Laurence Building A08, The University of Sydney, Sydney, NSW, 2006, Australia

    C. R. Warren

Authors
  1. M. Uscola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Villar-Salvador
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Oliet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. R. Warren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Uscola.

Additional information

Responsible Editor: Ad C. Borstlap.

Electronic supplementary material

ESM 1

(DOCX 38 kb)

Figure S1

a) Image showing the root growth of one year-old seedlings, in container-grown plants the plug is a mass build up with the roots that hold the substrate. In the seedlings used in the experiment a plug was formed the first year when cultivated in 0.3 L containers. When the seedling were transplanted to a larger pot (2.5 L pots) for the labeling experiment new fine roots protruded out of the plug and colonized the transplanting substrate. b) Picture of seedling at harvesting, the plug is delimited by the blue lines. (JPEG 39 kb)

High resolution image (TIFF 191 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uscola, M., Villar-Salvador, P., Oliet, J. et al. Root uptake of inorganic and organic N chemical forms in two coexisting Mediterranean forest trees. Plant Soil 415, 387–392 (2017). https://doi.org/10.1007/s11104-017-3172-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3172-6

Keywords

Search

Navigation