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Prospects for improving nitrogen use efficiency: Insights given by 15N-labelling experiments

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Abstract

In higher plants, recent advances in plant molecular genetics, combined with modern physiological and biochemical studies, have expanded our understanding of the regulatory mechanisms controlling the primary steps of inorganic nitrogen assimilation and the subsequent biochemical pathways involved in nitrogen supply and recycling for higher plant metabolism, growth and development. In this presentation, we describe improvements in our understanding of the molecular controls of nitrogen assimilation through the use of transgenic plants and the study of genetic variability in model and crop species. To illustrate this research programme, the physiological impact of modified gene expression, using either transgenic plants or different genotypes, was studied using 15N-labelling experiments in order to monitor the influx of nitrate or ammonia and its subsequent incorporation into amino acids.

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References

  • Amarashinge BHRR, Debruxelles GL, Braddon M, Onyeocha I, Forde G & Udvardi MK (1998) Regulation of GMNRT2 expression and nitrate transport activity in roots of soybean (Glycine max.) Planta 206: 44–52.

    PubMed  Google Scholar 

  • Bauer D, Biehler K, Fock H, Carrayol E, Hirel B, Migge A & Becker T (1997) A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiol. Plant. 99: 241–248.

    Google Scholar 

  • Borell A, Hammer G & Van Oosterom E (2001) Stay-green: a consequence of the balance between supply and demand for nitrogen during grain filling. Ann. Appl. Biol. 138: 91–95.

    Google Scholar 

  • Brugière N, Dubois F, Limami A, Lelandais M, Roux Y, Sangwan R & Hirel B (1999) Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell 11: 1995–2011.

    PubMed  Google Scholar 

  • Brugière N, Dubois F, Masclaux C, Sangwan R & Hirel B (2000) Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol. Planta 21 1: 519–527.

    Google Scholar 

  • Carvalho H, Pereira S, Sunkel C, & Salema R (1992). Detection of a cytosolic glutamine synthetase in leaves of Nicotiana tabacum L. by immunocytochemical methods. Plant Physiol. 100: 1591–1594.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Cliquet JB, Deléens E, Bousser A, Martin M, Lescure JC, Prioul JL, Mariotti A & Morot-Gaudry JF (1990) Estimation of C and N allocation during stalk elongation by 13C and 15N tracing in Zea mays L. Plant Physiol. 92: 79–87.

    Google Scholar 

  • Cooper HD & Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and root in the regulation of nutrient uptake. J. Exp. 40: 753–762.

    Google Scholar 

  • Coruzzi M & Zhou L (2001) Carbon and nitrogen sensing and signalling in plants: emerging 'matrix effects'. Curr. Op. Plant Biol. 4: 247–253.

    Google Scholar 

  • Cren M & Hirel B (1999) Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol. 40: 1187–1193.

    Google Scholar 

  • Fuentes S1, Allen DJ, Ortiz-Lopez A & Hernàndez G (2001) Overexpression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J. Exp. Bot. 52: 1071–1081.

    PubMed  Google Scholar 

  • Drouet JL & Bonhomme R (1999) Do changes in local leaf irradiance explain changes to leaf nitrogen within row maize canopies? Ann. Bot. 84: 61–69.

    Google Scholar 

  • Forde BG & Clarkson DT (1999) Nitrate and ammonium nutrition of plants: Physiological and molecular perspectives. Adv. Bot. Res. 30: 1–90.

    Google Scholar 

  • Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim. Biophys. Acta. 1465: 219–235.

    PubMed  Google Scholar 

  • Fraisier V, Gojon A, Tillard P & Daniel-Vedele F (2000) Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: Evidence for post-transcriptional regulation by a reduced nitrogen source. Plant J. 23: 489–496.

    PubMed  Google Scholar 

  • Fraisier V, Dorbe MF & Daniel-Vedele F (2001) Identification and expression analyses of two genes encoding putative low-affinity nitrate transporters from Nicotiana plumbaginifolia. Plant Mol. Biol. 45: 181–190.

    PubMed  Google Scholar 

  • Gastal F & Lemaire G (2002) N uptake and distribution in crops: an agronomical and ecophysiolopgical perspective. J. Exp. Bot. 53: 789–799.

    PubMed  Google Scholar 

  • Glass ADM, Shaff JE & Kochian LV (1992) Studies of the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiol. 99: 456–463.

    Google Scholar 

  • Glass ADM & Siddiqi MY (1995) Nitrogen absorption by plant roots. In: Srivastava HS, Singh RP (ed) Nitrogen Nutrition in Higher Plants (pp. 21–56). Associated Publishing Company, New Delhi.

    Google Scholar 

  • Gojon A, Dapoigny L, Lejay L, Tillard P & Rufty TW Jr (1998) Effects of the modification of nitrate reductase expression on NO143–01 uptake and reduction in Nicotiana plants. Plant Cell Environ. 21: 43–53.

    Google Scholar 

  • Guo FQ, Wang R, Chen M & Crawford NM (2001) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13: 1761–1777.

    PubMed  Google Scholar 

  • Harrison J, Brugière N, Phillipson B, Ferrario-Méry S, Becker T, Limami A & Hirel B (2000) Manipulating the pathway of ammonia assimilation through genetic manipulation and breeding. Consequences on plant physiology and development. Plant Soil 221: 81–93.

    Google Scholar 

  • Hell & Hillebrand (2001) plant concepts for mineral acquisition and allocation. Curr. Op. Plant Biol. 12: 161–168.

    Google Scholar 

  • Hirel B & Lea PJ (2001) Ammonia assimilation. In: Springer INRA (ed) Plant Nitrogen (pp. 79–99).

  • Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M & Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol. 125: 1258–1270.

    PubMed  Google Scholar 

  • Huang N-C, Liu K-H, Lo H-J & Tsay Y-F (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11: 1381–1392.

    PubMed  Google Scholar 

  • Ismande J & Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol. 105: 3–7.

    PubMed  Google Scholar 

  • Kamachi K, Yamaya T, Hayakawa T, Mae T & Ojima K (1992) Vascular bundle-specific localization of cytosolic glutamine synthetase in rice leaves. Plant Physiol. 99: 1481–1486.

    Google Scholar 

  • Kawakami N & Watanabe A (1988) Senescence-specific increase in cytosolic glutamine synthetase and its mRNA in radish cotyledons. Plant Physiol. 88: 1430–1434.

    Google Scholar 

  • Knight TJ & Langston-Unkeffer PJ (1988) Enhancement of symbiotic dinitrogen fixation by a toxin-releasing plant pathogen. Science 241: 951–954.

    Google Scholar 

  • Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F & Gojon A (1999) Molecular and functional regulation of two NO143–02 uptake systems by N-and C-status of Arabidospsis plants. Plant J. 18: 509–519.

    PubMed  Google Scholar 

  • Limami A, Phillipson B, Ameziane R, Pernollet N, Jiang Q, Roy R, Deleens E, Chaumont-Bonnet M, Gresshoff PM & Hirel B (1999) Does root glutamine synthetase control plant biomass production in Lotus japonicus L. Planta 209: 495–502.

    PubMed  Google Scholar 

  • Liu K-H, Huang C-Y & Tsay Y-F (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involving multiple phases of nitrate uptake. Plant Cell 11: 865–874.

    PubMed  Google Scholar 

  • Ma BL & Dwyer LM (1998) Nitrogen uptake and use in two contrasting maize hybrids differing in leaf senescence. Plant Soil. 199: 283–291.

    Google Scholar 

  • Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis and yield. In: Ando T et al. (eds) Plant Nutrition for Sustainable Food Production and Environment. (pp. 51–60). Kluwer Academic Publishers, Japan.

    Google Scholar 

  • Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, & Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211: 510–518.

    PubMed  Google Scholar 

  • Masclaux C, Quilleré I, Gallais A & Hirel B (2001) The challenge of remobilisation in plant nitrogen economy. A survey of physioagronomic and molecular approaches. Ann. Appl. Biol. 138: 69–81.

    Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler R Höberg M & Höberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392: 914–916.

    Article  Google Scholar 

  • Nussaume L, Vincentz M, Meyer C, Boutin JP & Caboche M (1995) Post-transcriptional regulation of nitrate reductase by light is abolished by N-terminal deletion. Plant Cell 7: 611–621.

    PubMed  Google Scholar 

  • Oaks A (1992) A re-evaluation of nitrogen assimilation in roots. Bioscience February. (pp. 103–110).

  • Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T & Sato T (2001) Mapping QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J. Exp. Bot. 52: 1209–1217.

    PubMed  Google Scholar 

  • Ono F, Frommer WB & Von Wiren N (2000) coordinated diurnal regulation of low-and high-affinity nitrate transporters in tomato. Plant Biol. 2: 17–23.

    Google Scholar 

  • Orsel M, Filleur S, Fraisier V & Daniel-Vedele F (2002) Nitrate transport in plants: which gene and which control? J. Exp. Bot. 53: 825–833.

    PubMed  Google Scholar 

  • Pérez-Garcia A, Canovas FM, Gallardo, F, Hirel B & de Vicente A (1995) Differential expression of glutamine synthetase isoforms in detached leaflets infected with Pseudomonas syringae pv. tomato. Mol. Plant Mic. Interac. 8: 96–103.

    Google Scholar 

  • Quesada A, Galvàn A & Fernàndez E (1994) Identification of nitrate transporter genes in Chlamydomonas reinhardtii. Plant J. 5: 407–419.

    PubMed  Google Scholar 

  • Quillere I, Dufossé C, Roux Y, Foyer Ch, Caboche M & Morot-Gaudry JF (1994) The effect of NR gene expression on growth and nitrogen metabolism of Nicotiana plumbaginifolia plants. J. Exp. Bot. 45: 1205–1211.

    Google Scholar 

  • Raush BL, Basten C & Buckler ES (2002) Quantitative analysis of growth response to varying nitrogen sources in Arabidopsis thaliana. Theor. Appl. Genet. 104: 743–750.

    PubMed  Google Scholar 

  • Salsac L, Chaillou S, Morot-Gaudry JF, Lesaint C & Jolivet E (1987) Nitrate and ammonium nutrition in plants. Plant Physiol. Biochem. 25: 805–812.

    Google Scholar 

  • Shulze W, Shulze ED, Pate JS & Gillison AN (1997) The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephallotus follicularis and Darlingtonia californica. Oecologia 112: 464–471.

    Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ & Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13 NO143–03. Plant Physiol. 90: 806–813.

    Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ & Rufty TW(l990) Studies of the uptake of nitrate in barley. I. Kinetics of 13 NO143–03 influx. Plant Physiol. 93: 1426–1432.

    Google Scholar 

  • Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Sceible WR & Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J. Exp. Bot. 53:959–970.

    PubMed  Google Scholar 

  • Temple SJ, Bagga S & Sengupta-Gopalan C (1994) Can glutamine synthetase activity be modulated in transgenic plants by the use of recombinant DNA technology? Transgenic Plants and Biochemistry. Biochem. Soc. Trans. 22: 915–920.

    PubMed  Google Scholar 

  • Trueman LJ, Richardson A & Forde BG (1996) Molecular cloning of higher plant homologues of the high affinity nitrate transporters of Chlamydomonas and Aspergillus nidulans. Gene 175: 223–231.

    PubMed  Google Scholar 

  • Unkles SE, Hawker KL, Grieve C, Campbell EI, Montague P & Kinghorn JR (1991) cnrA encodes a nitrate transporter in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 88: 204–208.

    PubMed  Google Scholar 

  • Vincent R, Fraisier V, Chaillou S, Limami M.A, Deléens E, Phillipson B, Douat C, Boutin JP & Hirel B (1997) Overexpression of a soybean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus corniculatus L. plants triggers changes in ammonium assimilation and plant development. Planta 201: 424–433.

    PubMed  Google Scholar 

  • Vincentz M & Caboche M (1991) Constitutive expression of nitrate reductase allows normal growth and development of Nicotiana plumbaginifolia plants. EMBO J. 10: 1027–1035.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Unité de Nutrition Azotée des Plantes, I.N.R.A., R.D. 10, 78026, Versailles Cedex, France

    Bertrand Hirel

  2. U.M.R. Physiologie Moléculaire des Semences. U.F.R. Sciences, 2 Bd. Lavoisier, 49045, Angers Cedex 01, France

    Anis M. Limami

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  1. Bertrand Hirel
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  2. Anis M. Limami
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Correspondence to Bertrand Hirel.

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Hirel, B., Limami, A.M. Prospects for improving nitrogen use efficiency: Insights given by 15N-labelling experiments. Phytochemistry Reviews 2, 133–144 (2003). https://doi.org/10.1023/B:PHYT.0000004186.60917.d4

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  • DOI: https://doi.org/10.1023/B:PHYT.0000004186.60917.d4

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