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A dynamic whole-plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium-nitrate interactions

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Abstract

The dynamics of ammonium (NH4 +) and nitrate (NO3 -) concentrations in the soil solution is an important determinant of the species composition of natural vegetation. A mathematical model of uptake, assimilation and translocation of NH4 + and NO3 - is presented to assess the performance of species with respect to NO3 -/NH4 + feeding characterised by physiologically defined parameters. Nitrate efflux is explicitly considered. The capacities of NO3 -, [U NM], and NH4 + influx, [U AM], and NO3 - reduction, [A NM], appear sufficient to characterise whole-plant N metabolism including NO3 - translocation. The parameter space made up by these parameters is represented by 276 parameter combinations (`species'). Simulated total net N uptake rate and C costs for uptake and assimilation per mole total net N taken up are used to decide on how a species profits or suffers from NO3 -+NH4 + mixtures relative to pure N forms with similar total N concentration for external concentrations up to 1.6 mM. Five response categories were identified and contrasted with categories defined by Bogner (1968) on the basis of experimental results on forest plants. The largest category comprises species that respond positively to NO3 - and positively or indifferently to NH4 +. These species have intermediate to high [U NM] and [A NM] and variable [U AM] and correspond to woodland edge species and forest plants on rich soil including typical `nitrophilic' species. This category fades into a group of species that respond positively to NO3 - and negatively to NH4 +. These species have high [U NM] and low [U AM] and [A NM]; several species from oak-hornbeam woodland (Carpinion) belong to this group. Many parameter combinations were found that responded positively to NH4 + and indifferently to NO3 -: low to medium [U NM], medium to high [U AM] and variable [A NM]. This category includes all heathland species. No species were found which responded negatively to NO3 -. The physiological background of differences between the categories is explained with respect to the equilibrium NO3 - concentration in roots, influx, efflux, translocation and assimilation of NO3 - and uptake and assimilation of NH4 +. The relationship between NO3 - accumulation capacity and morphology is discussed. Some slow-growing species with high [U NM] and low [A NM] use NO3 - mainly as an osmotic solute. Respiratory costs in roots of inherently slow-growing species are discussed with respect to patterns in NH4 + and NO3 - availabilities of their habitat.

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References

  • Al Gharbi A and Hipkin C R 1984 Studies on nitrate reductase in British angiosperms. 1. A comparison of nitrate reductase activity in ruderal, woodland-edge and woody species. New Phytol. 97, 629-639.

    Article  CAS  Google Scholar 

  • Aslam M, Travis R L and Huffaker R C 1994 Stimulation of nitrate and nitrite efflux by ammonium in barley (Hordeum vulgare L.) seedlings. Plant Physiol.106, 1293–1301.

    PubMed  CAS  Google Scholar 

  • Aslam M, Travis R L and Huffaker R C 1995 Effect of pH and calcium on short-term NO -3 fluxes in roots of barley seedlings. Plant Physiol. 108, 727–734.

    PubMed  CAS  Google Scholar 

  • Aslam M, Travis R L and Rains D W 1996 Evidence for substrate induction of a nitrate efflux system. Plant Physiol. 112, 1167–1175.

    PubMed  CAS  Google Scholar 

  • Blom-Zandstra M, Lampe J EM and Ammerlaan F HM 1988 C and N utilization of two lettuce genotypes during growth under nonvarying light conditions and after changing the light intensity. Physiol. Plant. 74, 147–153.

    Article  Google Scholar 

  • Bloom A J 1985 Wild and cultivated barleys show similar affinities for mineral nitrogen.Oecologia 65, 555–557.

    Article  Google Scholar 

  • Bloom A J, Sukrapanna S S and Warner R L 1992 Root respiration associated with ammonium and nitrate absorption and assimilation in barley. Plant Physiol. 99, 1294–1301.

    PubMed  CAS  Google Scholar 

  • Bogner W 1968 Experimentelle Prüfung von Waldbodenpflanzen auf ihre Ansprüche an die Form der Stickstoff-Ernährung. Mitt. Verein Forstl. Standortskunde Forstpflanzenzüchtung 18, 3–45.

    Google Scholar 

  • Bogner W and Dieterich H 1968 Weitere Kulturversuche mit variierter Stickstoff-Form und abgestufter Azidität. Mitt. Verein Forstl. Standortskunde Forstpflanzenzüchtung 18, 46–58.

    Google Scholar 

  • Clarkson D T 1993 Roots and the delivery of solutes to the xylem. Phil. Trans. R. Soc. London B 341, 5–17.

    Google Scholar 

  • Clarkson D T 1998 Mechanisms for N-uptake and their running costs; is there scope for more efficiency? In Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences. Ed. H Lambers, H Poorter and M M I van Vuuren. pp 221–235. Backhuys Publishers, Leiden.

    Google Scholar 

  • Crabtree R C and Bazzaz F A 1993 Seedling response of four birch species to simulated nitrogen deposition - ammonium versus nitrate. Ecol. Applic. 3, 315–321.

    Article  Google Scholar 

  • Cruz C, Lips S H and Martins-Loução M A 1993 Interactions between nitrate and ammonium during uptake by carob seedling and the effect of the form of earlier nitrogen nutrition.Physiol. Plant. 89, 544–551.

    Article  CAS  Google Scholar 

  • Daniel-Vedele F, Filleur S and Caboche M 1998 Nitrate transport: a key step in nitrate assimilation. Current Opinion in Plant Biology 1, 235–239.

    Article  PubMed  CAS  Google Scholar 

  • Deane-Drummond C E 1990 Biochemical and biophysical aspects of nitrate uptake and its regulation. In Nitrogen in Higher Plants. Ed. Y P Abrol. pp 1–37. Research Studies Press, Taunton.

    Google Scholar 

  • Deane-Drummond C E, Clarkson D T and Johnson C B 1980 The effect of differential root and shoot temperature on the nitrate reductase activity, assayed in vivo and in vitro in roots of Hordeum vulgare (barley). Planta 148, 455–461.

    CAS  Google Scholar 

  • Delhon P, Gojon A, Tillard P and Passama L 1996 Diurnal regulation of NO -3 uptake in soybean plants. III. Implication of the Dijkshoorn-Ben Zioni model in relation with the diurnal changes in NO -3 assimilation. J. Exp. Bot. 47, 885–892.

    CAS  Google Scholar 

  • Diekmann M and Falkengren-Grerup U 1998 A new species index for forest vascular plants: development of functional indices based on mineralization rates of various forms of soil nitrogen. J. Ecol. 86, 269–283.

    Article  CAS  Google Scholar 

  • Falkengren-Grerup U 1995 Interspecies differences in the preference of ammonium and nitrate in vascular plants. Oecologia 102, 305–311.

    Article  Google Scholar 

  • Falkengren-Grerup U and Lakkenborg-Kristensen H 1994 Importance of ammonium and nitrate to the performance of herb-layer species from deciduous forests in southern Sweden. Environ. Exp. Bot. 34, 31–38.

    Article  Google Scholar 

  • Farrar J F 1992 The whole plant: carbon partitioning during development. In Carbon Partitioning Within and Between Species. Eds C J Pollock, J F Farrar and A J Gordon. pp 163–179. BIOS Scientific Publishers, Oxford.

    Google Scholar 

  • Foyer C H, Valadier M H and Ferrario S 1995 Co-regulation of nitrogen and carbon assimilation in leaves. In Environment and Plant Metabolism. Ed. N Smirnoff. pp 17–33. BIOS Scientific Publishers, Oxford.

    Google Scholar 

  • Glass A D M, Shaff J E and Kochian L V 1992 Studies of the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiol. 99, 456–463.

    PubMed  CAS  Google Scholar 

  • Gojon A, Soussana J F, Passama L and Robin P 1986 Nitrate reduction in roots and shoots of barley (Hordeum vulgare L.) and corn (Zea mays L.) seedlings. I. 15N study. Plant Physiol. 82, 254–260.

    PubMed  CAS  Google Scholar 

  • Gojon A, Plassard C and Bussi C 1994 Root/shoot distribution of NO -3 -assimilation in herbaceous and woody species. In AWhole Plant Perspective on Carbon-nitrogen Interactions. Eds J Roy and E Garnier. pp 131–147. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Hofstra J J, Lanting L and De Visser R 1985 Metabolism of Urtica dioica as dependent on the supply of mineral nutrients.Physiol. Plant. 63, 13–18.

    Article  CAS  Google Scholar 

  • Högberg P, Johannisson C, Nicklasson H and Högbom L 1990 Shoot nitrate reductase activities of field-layer species in different forest types. I. Preliminary surveys in northern Sweden. Scand. J. For. Res. 5, 449–456.

    Google Scholar 

  • Hole D J, Emran A M, Fares Y and Drew M C 1990 Induction of nitrate transport in maize roots, and kinetics of influx, measured with nitrogen-13.Plant Physiol. 93, 642–647.

    PubMed  CAS  Google Scholar 

  • Kamminga-Van Wijk C and Prins H B A 1993 The kinetics of NH +4 and NO -3 uptake by douglas fir from single N-solutions and from solutions containing both NH +4 and NO -3 . Plant Soil 151, 91–96.

    CAS  Google Scholar 

  • King B J, Siddiqi M Y and Glass A D M 1992 Studies of the uptake of nitrate in barley. V. Estimation of root cytoplasmic nitrate concentration using nitrate reductase activity - implications for nitrate influx. Plant Physiol. 99, 1582–1589.

    PubMed  CAS  Google Scholar 

  • Kronzucker H J, Siddiqi M Y and Glass A D M 1995 Kinetics of NO -3 influx in spruce. Plant Physiol. 109, 319–326.

    PubMed  CAS  Google Scholar 

  • Kronzucker H J, Siddiqi M Y and Glass A D M 1996 Kinetics of NH +4 influx in spruce. Plant Physiol. 110, 773–779.

    PubMed  CAS  Google Scholar 

  • Kronzucker H J, Siddiqi M Y and Glass A D M 1997 Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385, 59–61.

    Article  CAS  Google Scholar 

  • Lainé P, Ourry A, Macduff J, Boucaud J and Salette J 1993 Kinetic parameters of nitrate uptake by different catch crop species: effects of low temperatures or previous nitrate starvation. Physiol. Plant. 88, 85–92.

    Article  Google Scholar 

  • Lambers H 1997 Oxidation of mitochondrial NADH and the synthesis of ATP. In PlantMetabolism. Eds D T Dennis, D H Turpin, D D Lefebvre and D B Layzell. pp 200–219. Addison Wesley Longman, Harlow.

    Google Scholar 

  • Lambers H, Chapin III F S and Pons T L 1998 Plant physiological ecology. Springer, New York.

    Google Scholar 

  • Lee R B and Drew M C 1989 Rapid, reversible inhibition of nitrate influx in barley by ammonium. J. Exp. Bot. 40, 741–752.

    CAS  Google Scholar 

  • Lee R B and Rudge K A 1986 Effects of nitrogen deficiency on the absorption of nitrate and ammonium by barley plants. Ann. Bot. 57, 471–486.

    Google Scholar 

  • Lee R B, Purves J V, Ratcliffe R G and Saker L R 1992 Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. J. Exp. Bot. 43, 1385–1396.

    CAS  Google Scholar 

  • Leeters E E J M, Hartholt J G, De VriesWand Boumans L JM 1994 Effects of acid deposition on 150 forest stands in the Netherlands. Assessment of the chemical compositions of foliage, soil, soil solution and groundwater on a national scale. Report 69.4. Winand Staring Centre, Wageningen.

    Google Scholar 

  • Li X Z and Oaks A 1993 Induction and turnover of nitrate reductase in Zea mays. Plant Physiol. 102, 1251–1257.

    PubMed  CAS  Google Scholar 

  • Macduff J H and Jackson S B 1992 Influx and efflux of nitrate and ammonium in Italian ryegrass and white clover roots: comparisons between effects of darkness and defoliation. J. Exp. Bot. 43, 525–535.

    CAS  Google Scholar 

  • Mäck G and Tischner R 1990 The effect of endogenous and externally supplied nitrate on nitrate uptake and reduction in sugarbeet seedlings. Planta 182, 169–173.

    Article  Google Scholar 

  • Mattsson M, Lundborg T and Larsson C M 1988 Nitrate utilization in barley: relations to nitrate supply and light/dark cycles. Physiol. Plant. 73, 380–386.

    Article  CAS  Google Scholar 

  • Merhaut D J and Darnell R L 1995 Ammonium and nitrate accumulation in containerized southern highbush blueberry plants.Hortscience 30, 1378–1381.

    Google Scholar 

  • Miflin B J 1974 The location of nitrite reductase and other enzymes related to amino acid biosynthesis in the plastids of root and leaves. Plant Physiol. 54, 550–555.

    Article  PubMed  CAS  Google Scholar 

  • Miller A J and Smith S J 1996 Nitrate transport and compartmentation in cereal root cells. J. Exp. Bot. 47, 843–854.

    CAS  Google Scholar 

  • Mistrik I and Ullrich C I 1996 Mechanism of anion uptake in plant roots: quantitative evaluation of H+/NO -3 and H+/H2PO -4 stoichiometries. Plant Physiol. Biochem. 34, 629–636.

    CAS  Google Scholar 

  • Oaks A 1994 Primary nitrogen assimilation in higher plants and its regulation. Can. J. Bot. 72, 739–750.

    CAS  Google Scholar 

  • Oaks A and Yamaya T 1990 Nitrogen assimilation in leaves and roots - a role for glutamate dehydrogenase. In Nitrogen in Higher Plants. Ed. Y P Abrol. pp 181–194. Research Studies Press, Taunton.

    Google Scholar 

  • Ohlson M and Högbom L 1993 Species-specific dynamics in nitrate reductase activity in coexisting swamp forest plants. J. Ecol. 81, 739–744.

    Article  CAS  Google Scholar 

  • Ovcharenko G A, Drobysheva N I, Khudyakova E M, Nikiforova T A and Izmailov S F 1993 Size of the metabolic pool of nitrate as criterion of its assimilation by the plant. Russ. Plant Physiol. 40, 58–61.

    Google Scholar 

  • Pearson J, Clough E C M and Kershaw J L 1989 Comparative study of nitrogen assimilation in woodland species. Ann. Sc. For. 46, 669s–672s.

    Google Scholar 

  • Penning de Vries F W T, Brunsting A H M and Van Laar H H 1974 Products, requirements and efficiency of biosynthesis: a quantitative approach. J. Theor. Biol. 45, 339–377.

    Article  PubMed  CAS  Google Scholar 

  • Peuke A D and Kaiser W M 1996 Nitrate or ammonium uptake and transport, and rapid regulation of nitrate reduction in higher plants. Progr. Bot. 57, 93–113.

    CAS  Google Scholar 

  • Rosnitschek-Schimmel I 1982 Effect of ammonium and nitrate supply on dry matter production and nitrogen distribution in Urtica dioica. Zeitschrift für Pflanzenphysiologie 108, 329–341.

    CAS  Google Scholar 

  • Scheromm P and Plassard C 1988 Nitrogen nutrition of nonmycorrhized maritime pine (Pinus pinaster) grown on nitrate or ammonium. Plant Physiol. Biochem. 26, 261–269.

    CAS  Google Scholar 

  • Scheurwater I, Clarkson D T, Purves J V, Van Rijt G, Saker L R, Welschen R and Lambers H 1999. Relatively large nitrate ef-flux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant Soil (in press).

  • Siddiqi M Y, Glass A D M, Ruth T J and Fernando M 1989 Studies of the regulation of nitrate influx by barley seedlings using 13NO -3 . Plant Physiol. 90, 806–813.

    PubMed  CAS  Google Scholar 

  • Siddiqi M Y, Glass A D M, Ruth T J and Rufty T W 1990 Studies of the uptake of nitrate in barley. I. Kinetics of 13NO -3 -influx. Plant Physiol. 93, 1426–1432.

    PubMed  CAS  Google Scholar 

  • Smirnoff N, Todd P and Stewart G R 1984 The occurrence of nitrate reduction in the leaves of woody plants. Ann. Bot. 54, 363–374.

    CAS  Google Scholar 

  • Sueyoshi K, Kleinhofs A and Warner R L 1995 Expression of NADH-specific and NAD(P)H-bispecific nitrate reductase genes in response to nitrate in barley. Plant Physiol. 107, 1303–1311.

    PubMed  CAS  Google Scholar 

  • Touraine B, Clarkson D T and Muller B 1994 Regulation of nitrate uptake at the whole plant level. In A Whole Plant Perspective on Carbon-nitrogen Interactions. Eds J Roy and E Garnier. pp 11–30. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Troelstra S R, Wagenaar R and Smant W 1995 Nitrogen utilization by plant species from acid heathland soils. I. Comparison between nitrate and ammonium nutrition. J. Exp. Bot. 46, 1103–1112.

    CAS  Google Scholar 

  • Ullrich C I and Guern J 1990 Ion fluxes and pH changes induced by trans-plasmalemma electron transfer and fuscicoccin in Lemna gibba L. (strain G1).Planta 180, 390–399.

    Article  CAS  Google Scholar 

  • Ullrich C I and Novacky A J 1990 Extra-and intracellular pH and membrane potential changes induced by K+, CL-, H2PO -4 and NO -3 uptake and fuscicoccin in root hairs of Limnobium stoloniferum. Plant Physiol. 94, 1561–1567.

    PubMed  CAS  Google Scholar 

  • Van der Leij M, Smith S J and Miller A J 1998 Remobilisation of vacuolar stored nitrate in barley root cells. Planta 205, 64–72.

    Article  CAS  Google Scholar 

  • Wang M Y, Glass A D M, Shaff J E and Kochian L V 1994 Ammonium uptake by rice roots. III. Electrophysiology. Plant Physiol. 104, 899–906.

    PubMed  CAS  Google Scholar 

  • Woo K C, Flügge U I and Heldt HW 1987 A two-translocator model for the transport of 2-oxoglutarate and glutamate in chloroplasts during ammonia assimilation in the light. Plant Physiol. 84, 624–632.

    PubMed  CAS  Google Scholar 

  • Woodall J and Forde B G 1996 Glutamine synthetase polypeptides in the roots of 55 legume species in relation to their climatic origin and the partitioning of nitrate assimilation. Plant Cell Environ. 19, 848–858.

    Article  CAS  Google Scholar 

  • Yu J and Woo K C 1988 Glutamine transport and the role of the glutamine translocator in chloroplasts.Plant Physiol. 88, 1048–1054.

    PubMed  CAS  Google Scholar 

  • Zhen R G and Leigh R A 1990 Nitrate accumulation by wheat (Triticum aestivum) in relation to growth and tissue N concentrations. Plant Soil 124, 157–160.

    Article  CAS  Google Scholar 

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Bijlsma, R., Lambers, H. & Kooijman, S. A dynamic whole-plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium-nitrate interactions. Plant and Soil 220, 49–69 (2000). https://doi.org/10.1023/A:1004779019486

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