Trees

, Volume 29, Issue 4, pp 1069–1078 | Cite as

Interspecific variation in leaf–root differences in δ15N among three tree species grown with either nitrate or ammonium

Original Paper

Key message

Interspecific variation in nitrogen isotope composition of roots and leaves of tree seedlings grown in a steady-state nitrogen environment reflects known variation in sites of assimilation and nitrogen source preference in three tree species.

Abstract

As a time-integrated measure of nitrogen use, discrimination against the heavier stable isotope (15N) during the uptake and assimilation of inorganic nitrogen has the potential to provide information on interspecific differences in inorganic nitrogen source preference. Here, nitrogen isotope composition (δ15N) at natural abundance was measured for the roots and shoots from seedlings of three forest tree species: Populus tremuloides (aspen), Pinus contorta var. latifolia (pine) and Picea glauca (spruce). The seedlings were grown hydroponically with low (0.1 mM) or high (1.5 mM) concentrations of NO3 or NH4+, or in sand with NO3, NH4+ or an equal mix of NO3 and NH4+ (0.1 mM). Whole-plant nitrogen isotope discrimination was observed in hydroponically grown seedlings but not in sand culture. Differences in δ15N between shoots and roots were greater in aspen when grown with NO3 (3.02 ‰) than with NH4+ (1.27 ‰). There were no significant differences between the δ15N of leaves and roots for pine and spruce on either source. Although whole-plant nitrogen isotope discrimination was not observed in sand culture, shoot δ15N was, again, greater than root δ15N for NO3-grown aspen. Interspecific variation in nitrogen isotope discrimination was observed in both hydroponics and sand culture. The differences in nitrogen isotope composition under steady-state conditions indicate that interspecific differences in nitrogen source preference are consistent with previous experiments using alternative methods to identify differences in nitrogen uptake and assimilation in the same tree species.

Keywords

Nitrogen Source preference Isotope discrimination Nitrate Ammonium Hydroponics 

References

  1. Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9:511–519Google Scholar
  2. Ariz I, Cruz C, Moran JF, González-Moro MB, García-Olaverri C, González-Murua C, Aparicio-Tejo PM (2011) Depletion of the heaviest stable N isotope is associated with NH4 +/NH3 toxicity in NH4 +-fed plants. BMC Plant Biol 11:83PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bauer D, Biehler K, Fock H, Carrayol E, Hirel B, Migge A, Becker TW (1997) A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiol Plant 99(2):241–248CrossRefGoogle Scholar
  4. Bedard-Haughn A, Van Groenigen JW, Van Kessel C (2003) Tracing 15N through landscapes: potential uses and precautions. J Hydrol 272(1):175–190CrossRefGoogle Scholar
  5. Bergersen FJ, Peoples MB, Turner GL (1988) Isotopic discriminations during the accumulation of nitrogen by soybeans. Funct Plant Biol 15(3):407–420Google Scholar
  6. Britto DT, Siddiqi MY, Glass AD, Kronzucker HJ (2001) Futile transmembrane NH4+ cycling: a cellular hypothesis to explain ammonium toxicity in plants. PNAS 98(7):4255–4258PubMedCentralPubMedCrossRefGoogle Scholar
  7. Cawse PA (1967) The determination of nitrate in soil solution by ultraviolet spectrometry. Analyst 92:311–315CrossRefGoogle Scholar
  8. Comstock J (2001) Steady-state isotopic fractionation in branched pathways using plant uptake of NO3 as an example. Planta 214(2):220–234. doi:10.1007/s004250100602 PubMedCrossRefGoogle Scholar
  9. Dijkstra P, Williamson C, Menyailo O, Doucett R, Koch G, Hungate BA (2003) Nitrogen stable isotope composition of leaves and roots of plants growing in a forest and a meadow. Isotopes Environ Health Stud 39:29–39PubMedCrossRefGoogle Scholar
  10. Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6(3):121–126PubMedCrossRefGoogle Scholar
  11. Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR (1996) Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant Cell Environ 19(11):1317–1323. doi:10.1111/j.1365-3040.1996.tb00010.x CrossRefGoogle Scholar
  12. Gessler A, Rienks M, Rennenberg H (2000) NH3 and NO2 fluxes between beech trees and the atmosphere—correlation with climatic and physiological parameters. New Phytol 147:539–560CrossRefGoogle Scholar
  13. Glass ADM, Britto DT, Kaiser BN et al (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864PubMedCrossRefGoogle Scholar
  14. Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–985CrossRefGoogle Scholar
  15. Högberg P, Johannisson C, Högberg MN (2014) Is the high 15N natural abundance of trees in N-loaded forests caused by an internal ecosystem N isotope redistribution or a change in the ecosystem N isotope mass balance? Biogeochem 117:351–358CrossRefGoogle Scholar
  16. Husted S, Schjoerring JK, Nielsen KH, Nemitz E, Sutton MA (2000) Stomatal compensation points for ammonia in oilseed rape plants under field conditions. Agric For Meterol 105(4):371–383CrossRefGoogle Scholar
  17. Johnson JE, Berry JA (2013) The influence of leaf-atmosphere NH3 (g) exchange on the isotopic composition of nitrogen in plants and the atmosphere. Plant Cell Environ 36(10):1783–1801PubMedCrossRefGoogle Scholar
  18. Johnson CM, Stout PR, Broyer TC, Carlton AB (1957) Comparative chlorine requirements of different plant species. Plant Soil 8:337–353CrossRefGoogle Scholar
  19. Kalcsits L, Guy RD (2013a) Whole plant and organ level nitrogen isotope discrimination indicates modification of partitioning of assimilation, fluxes and allocation of nitrogen in knockout lines of Arabidopsis thaliana. Physiol Plant 149:249–259PubMedCrossRefGoogle Scholar
  20. Kalcsits LA, Guy RD (2013b) Quantifying remobilization of pre-existing nitrogen from cuttings to new growth of woody plants using 15N at natural abundance. Plant Methods 9:27PubMedCentralPubMedCrossRefGoogle Scholar
  21. Kalcsits LA, Buschhaus HA, Guy RD (2014) Nitrogen isotope discrimination as an integrated measure of nitrogen fluxes, assimilation and allocation in plants. Physiol Plant 151(3):293–304PubMedCrossRefGoogle Scholar
  22. Karsh KL, Granger J, Kritee K, Sigman DM (2014) Eukaryotic assimilatory nitrate reductase fractionates N and O isotopes with a ratio near unity. Environ Sci Technol 46:5727–5735CrossRefGoogle Scholar
  23. Kolb KJ, Evans RD (2003) Influence of nitrogen source and concentration on nitrogen isotopic discrimination in two barley genotypes (Hordeum vulgare L.). Plant Cell Environ 3:1431–1440CrossRefGoogle Scholar
  24. Kronzucker HJ, Siddiqi MY, Glass AD (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385(6611):59–61CrossRefGoogle Scholar
  25. Li H, Li M, Luo J, Cao X, Qu L, Gai Y, Luo ZB (2012) N-fertilization has different effects on the growth, carbon and nitrogen physiology, and wood properties of slow-and fast-growing Populus species. J Exp Bot 63(17):6173–6185PubMedCentralPubMedCrossRefGoogle Scholar
  26. Luo J, Li H, Liu T, Polle A, Peng C, Luo ZB (2013) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64(14):4207–4224PubMedCentralPubMedCrossRefGoogle Scholar
  27. Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (1998) Induction of nitrate uptake and nitrate reductase activity in trembling aspen and lodgepole pine. Plant Cell Environ 21(10):1039–1046CrossRefGoogle Scholar
  28. Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (1999) A comparative study of fluxes and compartmentation of nitrate and ammonium in early-successional tree species. Plant Cell Environ 22(7):821–830CrossRefGoogle Scholar
  29. Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (2002) A comparative study of fluxes and compartmentation of nitrate and ammonium in early-successional tree species. Plant Cell Environ 22:821–830CrossRefGoogle Scholar
  30. Peuke AD (2010) Correlations in concentrations, xylem and phloem flows, and partitioning of elements and ions in intact plants. A summary and statistical re-evaluation of modelling experiments in Ricinus communis. J Exp Bot 61:635–655PubMedCrossRefGoogle Scholar
  31. Peuke AD, Gessler A, Rennenberg H (2006) The effect of drought on C and N stable isotopes in different fractions of leaves, stems and roots of sensitive and tolerant beech ecotypes. Plant Cell Environ 29(5):823–835. doi:10.1111/j.1365-3040.2005.01452.x PubMedCrossRefGoogle Scholar
  32. Peuke AD, Gessler A, Tcherkez G (2013) Experimental evidence for diel δ15N-patterns in different tissues, xylem and phloem saps of castor bean (Ricinus communis L.). Plant Cell Environ 36:2219–2228PubMedCrossRefGoogle Scholar
  33. Prescott CE, Hope GD, Blevins LL (2003) Effect of gap size on litter decomposition and soil nitrate concentrations in a high-elevation spruce fir forest. Can J For Res 33(11):2210–2220CrossRefGoogle Scholar
  34. Pritchard ES, Guy RD (2005) Nitrogen isotope discrimination in white spruce fed with low concentrations of ammonium and nitrate. Trees Struct Funct 19:89–98CrossRefGoogle Scholar
  35. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16(3):153–162. doi:10.1016/S0169-5347(00)02098-X PubMedCrossRefGoogle Scholar
  36. Schjoerring JK, Husted S, Mack G, Mattson M (2002) The regulation of ammonium translocation in plants. J Exp Bot 53:883–890PubMedCrossRefGoogle Scholar
  37. Solorzano L (1969) Determination of ammonia in natural waters by the phenol-hypochlorite method. Limnol Oceanogr 1969(14):799–801CrossRefGoogle Scholar
  38. Tcherkez G, Hodges M (2008) How stable isotopes may help to elucidate primary nitrogen metabolism and its interaction with (photo) respiration in C(3) leaves. J Exp Bot 59:1685–1693PubMedCrossRefGoogle Scholar
  39. Waser NA, Yu Z, Yin K, Nielsen B, Harrison PJ, Turpin DH, Calvert SE (1999) Nitrogen isotopic fractionation during a simulated diatom spring bloom: importance of N-starvation in controlling fractionation. Marine Ecol Prog Ser 179:291–296CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Lee A. Kalcsits
    • 1
    • 2
    • 3
  • Xiangjia Min
    • 1
    • 4
  • Robert D. Guy
    • 1
  1. 1.Department of Forest and Conservation SciencesUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Biology, Centre for Forest BiologyUniversity of VictoriaVictoriaCanada
  3. 3.Department of Horticulture, WSU Tree Fruit Research and Extension CenterWashington State UniversityWenatcheeUSA
  4. 4.Department of Biological Sciences, Center for Applied Chemical BiologyYoungstown State UniversityYoungstownUSA

Personalised recommendations