Photosynthesis Research

, Volume 83, Issue 2, pp 239–250 | Cite as

Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply

  • Pia Walch-Liu
  • Sophie Filleur
  • Yinbo Gan
  • Brian G. Forde


During their life cycle, plants must be able to adapt to wide variations in the supply of soil nitrogen (N). Changes in N availability, and in the relative concentrations of NO3and NH4+, are known to have profound regulatory effects on the N uptake systems in the root, on C and N metabolism throughout the plant, and on root and shoot morphology. Optimising the plant’s responses to fluctuations in the N supply requires co-ordination of the pathways of C and N assimilation, as well as establishment of the appropriate allocation of resources between root and shoot growth. Achieving this integration of responses at the whole plant level implies long-distance signaling mechanisms that can communicate information about the current availability of N from root-to-shoot, and information about the C/N status of the shoot in the reverse direction. In this review we will discuss recent advances which have contributed to our understanding of these long-range signaling pathways.


abscisic acid auxin cytokinin leaf expansion nitrate nodulation root development shoot: root ratio 



abscisic acid


ATP/ADP isopentenyltransferase


ionotropic glutamate receptor


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  1. Beck, EH 1996Regulation of shoot/root ratio by cytokinins from roots in Urtica dioica: opinionPlant Soil185312Google Scholar
  2. Beveridge, CA, Murfet, IC, Kerhoas, L, Sotta, B, Miginiac, E, Rameau, C 1997The shoot controls zeatin riboside export from pea roots: evidence from the branching mutant rms4Plant J11339345CrossRefGoogle Scholar
  3. Beveridge, CA, Gresshoff, PM, Rameau, C, Turnbull, CGN 2003Additional signaling compounds are required to orchestrate plant developmentJ Plant Growth Regul221524CrossRefGoogle Scholar
  4. Bhalerao, RP, Eklof, J, Ljung, K, Marchant, A, Bennett, M, Sandberg, G 2002Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlingsPlant J29325332CrossRefPubMedGoogle Scholar
  5. Brenner, ED, Martinez-Barboza, N, Clark, AP, Liang, QS, Stevenson, DW, Coruzzi, GM 2000Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonistPlant Physiol12416151624CrossRefPubMedGoogle Scholar
  6. Caba, JM, Centeno, ML, Fernandez, B, Gresshoff, PM, Ligero, F 2000Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild typePlanta21198104PubMedGoogle Scholar
  7. Carroll, BJ, McNeil, DL, Gresshoff, PM 1985Isolation and properties of soybean (Glycine max (L) Merr.) mutants that nodulate in the presence of high nitrate concentrationsProc Natl Acad Sci USA8241624166Google Scholar
  8. Chen, CM, Ertl, JR, Leisner, SM, Chang, CC 1985Localization of cytokinin biosynthetic sites in pea plants and carrot rootsPlant Physiol78510513Google Scholar
  9. Chiu, JC, Brenner, ED, DeSalle, R, Nitabach, MN, Holmes, TC, Coruzzi, GM 2002Phylogenetic and expression analysis of the glutamate receptor like gene family in Arabidopsis thalianaMol Biol Evol1910661082PubMedGoogle Scholar
  10. Choi, DS, Lee, Y, Cho, HT, Kende, H 2003Regulation of expansin gene expression affects growth and development in transgenic rice plantsPlant Cell1513861398CrossRefPubMedGoogle Scholar
  11. Cline, MG 1991Apical dominanceBot Rev57318358Google Scholar
  12. Cluis, CP, Mouchel, CF, Hardtke, CS 2004The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathwaysPlant J38332347CrossRefPubMedGoogle Scholar
  13. Collier, MD, Fotelli, MN, Nahm, M, Kopriva, S, Rennenberg, H, Hanke, DE, Gessler, A 2003Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level: interactions between cytokinins and soluble N compoundsPlant Cell Environ2615491560CrossRefGoogle Scholar
  14. Cooper, HD, Clarkson, DT 1989Cycling of amino nitrogen and other nutrients between shoots and roots in cereals: a possible mechanism integrating shoot and root in the regulation of nutrient uptakeJ Exp Bot40753762Google Scholar
  15. Crawford, NM 1995Nitrate: nutrient and signal for plant growthPlant Cell7859868CrossRefPubMedGoogle Scholar
  16. Davenport, R 2002Glutamate receptors in plantsAnn Bot90549557CrossRefPubMedGoogle Scholar
  17. Deeken, R, Geiger, D, Fromm, J, Koroleva, O, Ache, P, Langenfeld-Heyser, R, Sauer, N, May, ST, Hedrich, R 2002Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of ArabidopsisPlanta216334344CrossRefPubMedGoogle Scholar
  18. Dennison, KL, Spalding, EP 2000Glutamate-gated calcium fluxes in ArabidopsisPlant Physiol12415111514CrossRefPubMedGoogle Scholar
  19. Downie, JA, Parniske, M 2002Plant biology: fixation with regulationNature420369370CrossRefPubMedGoogle Scholar
  20. Dubos, C, Huggins, D, Grant, GH, Knight, MR, Campbell, MM 2003A role for glycine in the gating of plant NMDA-like receptorsPlant J35800810CrossRefPubMedGoogle Scholar
  21. Faiss, M, Zalubilova, J, Strnad, M, Schmulling, T 1997Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plantsPlant J12401415CrossRefPubMedGoogle Scholar
  22. Ferguson, BJ, Mathesius, U 2003Signaling interactions during nodule developmentJ Plant Growth Regul224772CrossRefGoogle Scholar
  23. Ferrario-Mery, S, Masclaux, C, Suzuki, A, Valadier, MH, Hirel, B, Foyer, CH 2001Glutamine and α-ketoglutarate are metabolite signals involved in nitrate reductase gene transcription in untransformed and transformed tobacco plants deficient in ferredoxin-glutamine-α-ketoglutarate aminotransferasePlanta213265271CrossRefPubMedGoogle Scholar
  24. Fischer, WN, Loo, DDF, Koch, W, Ludewig, U, Boorer, KJ, Tegeder, M, Rentsch, D, Wright, EM, Frommer, WB 2002Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acidsPlant J29717731CrossRefPubMedGoogle Scholar
  25. Foo, E, Turnbull, CGN, Beveridge, CA 2001Long-distance signaling and the control of branching in the rms1 mutant of peaPlant Physiol126203209CrossRefPubMedGoogle Scholar
  26. Forde, BG 2002Local and long-range signaling pathways regulating plant responses to nitrateAnnu Rev Plant Biol53203224CrossRefPubMedGoogle Scholar
  27. Forde, BG, Clarkson, DT 1999Nitrate and ammonium nutrition of plants: physiological and molecular perspectivesAdv Bot Res30190Google Scholar
  28. Forde, BG, Lorenzo, H 2001The nutritional control of root developmentPlant Soil2325168CrossRefGoogle Scholar
  29. Franco-Zorrilla, JM, Martin, AC, Solano, R, Rubio, V, Leyva, A, Paz-Ares, J 2002Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in ArabidopsisPlant J32353360CrossRefPubMedGoogle Scholar
  30. Gansel, X, Munos, S, Tillard, P, Gojon, A 2001Differential regulation of the NO3 and NH4+ transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plantPlant J26143155CrossRefPubMedGoogle Scholar
  31. Gawronska, H, Deji, A, Sakakibara, H, Sugiyama, T 2003Hormone-mediated nitrogen signaling in plants: implication of participation of abscisic acid in negative regulation of cytokinin-inducible expression of maize response regulatorPlant Physiol Biochem41605610CrossRefGoogle Scholar
  32. Glass, ADM, Britto, DT, Kaiser, BN, Kinghorn, JR, Kronzucker, HJ, Kumar, A, Okamoto, M, Rawat, S, Siddiqi, MY, Unkles, SE, Vidmar, JJ 2002The regulation of nitrate and ammonium transport systems in plantsJ Exp Bot53855864CrossRefPubMedGoogle Scholar
  33. Gresshoff, PM 1993Molecular genetic analysis of nodulation genes in soybeanPlant Breeding Rev11275318Google Scholar
  34. Hemerly, AS, Ferreira, P, Engler, JD, Vanmontagu, M, Engler, G, Inze, D 1993Cdc2a expression in Arabidopsis Is linked with competence for cell divisionPlant Cell517111723CrossRefPubMedGoogle Scholar
  35. Hsieh, M-H, Lam, H-M, Loo, FJ, Coruzzi, G 1998A PII-like protein in Arabidopsis: putative role in nitrogen sensingProc Natl Acad Sci USA951396513970CrossRefPubMedGoogle Scholar
  36. Imsande, J, Touraine, B 1994N demand and the regulation of nitrate uptakePlant Physiol10537PubMedGoogle Scholar
  37. Kakimoto, T 2003Perception and signal transduction of cytokininsAnnu Rev Plant Biol54605627CrossRefPubMedGoogle Scholar
  38. Kang, JM, Turano, FJ 2003The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thalianaProc Natl Acad Sci USA10068726877CrossRefPubMedGoogle Scholar
  39. Kehr, J 2003Single cell technologyCurr Opin Plant Biol6617621CrossRefPubMedGoogle Scholar
  40. Kim, SA, Kwak, JM, Jae, SK, Wang, MH, Nam, HG 2001Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plantsPlant Cell Physiol427484CrossRefPubMedGoogle Scholar
  41. Korolev, AV, Tomos, AD, Bowtell, R, Farrar, JF 2000Spatial and temporal distribution of solutes in the developing carrot taproot measured at single-cell resolutionJ Exp Bot51567577CrossRefPubMedGoogle Scholar
  42. Krusell, L, Madsen, LH, Sato, S, Aubert, G, Genua, A, Szczyglowski, K, Duc, G, Kaneko, T, Tabata, S, Bruijn, F, Pajuelo, E, Sandal, N, Stougaard, J 2002Shoot control of root development and nodulation is mediated by a receptor-like kinaseNature420422426CrossRefPubMedGoogle Scholar
  43. Lam, H-M, Chiu, J, Hsieh, M-H, Meisel, L, Oliveira, IC, Shin, M, Coruzzi, G 1998Glutamate receptor genes in plantsNature396125126CrossRefPubMedGoogle Scholar
  44. Lejay, L, Tillard, P, Lepetit, M, Olive, FD, Filleur, S, Daniel-Vedele, F, Gojon, A 1999Molecular and functional regulation of two NO 3 uptake systems by N- and C-status of Arabidopsis plantsPlant J18509519CrossRefPubMedGoogle Scholar
  45. Lejay, L, Gansel, X, Cerezo, M, Tillard, P, Muller, C, Krapp, A, von, Wiren N, Daniel-Vedele, F, Gojon, A 2003Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinasePlant Cell1522182232CrossRefPubMedGoogle Scholar
  46. Li, Y, Jones, L, McQueen-Mason, S 2003Expansins and cell growthCurr Opin Plant Biol6603610CrossRefPubMedGoogle Scholar
  47. Limpens, E, Bisseling, T 2003Signaling in symbiosisCurr Opin Plant Biol6343350CrossRefPubMedGoogle Scholar
  48. Lipson, D, Nasholm, T 2001The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystemsOecologia128305316CrossRefGoogle Scholar
  49. Madden, DR 2002The structure and function of glutamate receptor ion channelsNat Rev Neurosci391101CrossRefPubMedGoogle Scholar
  50. Malone, M, Herron, M, Morales, MA 2002Continuous measurement of macronutrient ions in the transpiration stream of intact plants using the meadow spittlebug coupled with ion chromatographyPlant Physiol13014361442CrossRefPubMedGoogle Scholar
  51. Martin, AC, Pozo, JC, Iglesias, J, Rubio, V, Solano, R, Pena, A, Leyva, A, Paz-Ares, J 2000Influence of cytokinins on the expression of phosphate starvation responsive genes in ArabidopsisPlant J24559567CrossRefPubMedGoogle Scholar
  52. McDonald, AJS, Davies, WJ 1996Keeping in touch: responses of the whole plant to deficits in water and nitrogen supplyAdv Bot Res22229300Google Scholar
  53. Miyawaki, K, Matsumoto-Kitano, M, Kakimoto, T 2004Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitratePlant J37128138CrossRefPubMedGoogle Scholar
  54. Moore, B, Zhou, L, Rolland, F, Hall, Q, Cheng, WH, Liu, YX, Hwang, I, Jones, T, Sheen, J 2003Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signalingScience300332336CrossRefPubMedGoogle Scholar
  55. Moorhead, GBG, Smith, CS 2003Interpreting the plastid carbon, nitrogen, and energy status A role for PIIPlant Physiol133492498CrossRefPubMedGoogle Scholar
  56. Morris, SE, Turnbull, CGN, Murfet, IC, Beveridge, CA 2001Mutational analysis of branching in pea Evidence that Rms1 and Rms5 regulate the same novel signalPlant Physiol12612051213CrossRefPubMedGoogle Scholar
  57. Nakajima, K, Benfey, PN 2002Signaling in and out: control of cell division and differentiation in the shoot and rootPlant Cell14S265S276PubMedGoogle Scholar
  58. Nishimura, R, Hayashi, M, Wu, GJ, Kouchi, H, Imaizumi-Anraku, H, Murakami, Y, Kawasaki, S, Akao, S, Ohmori, M, Nagasawa, M, Harada, K, Kawaguchi, M 2002aHAR1 mediates systemic regulation of symbiotic organ developmentNature420426429CrossRefGoogle Scholar
  59. Nishimura, R, Ohmori, M, Fujita, H, Kawaguchi, M 2002bA Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulationProc Natl Acad Sci USA991520615210CrossRefGoogle Scholar
  60. Orsel, M, Filleur, S, Fraisier, V, Daniel-Vedele, F 2002Nitrate transport in plants: which gene and which controlJ Exp Bot53825833CrossRefPubMedGoogle Scholar
  61. Oyama, T, Shimura, Y, Okada, K 1997The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotylGenes Dev1129832995PubMedGoogle Scholar
  62. Paul, MJ, Foyer, CH 2001Sink regulation of photosynthesisJ Exp Bot5213831400CrossRefPubMedGoogle Scholar
  63. Peng, LT, Jiang, YM, Yang, SZ 2002Plant polypeptide signals: properties and functionsProg Biochem Biophys29877880Google Scholar
  64. Peuke, AD, Jeschke, WD, Hartung, W 1994The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L III Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress.J Exp Bot45741747Google Scholar
  65. Ponder, KL, Watson, RJ, Malone, M, Pritchard, J 2002Mineral content of excreta from the spittlebug Philaenus spumarius closely matches that of xylem sapNew Phytol153237242CrossRefGoogle Scholar
  66. Rashotte, AM, Carson, SDB, To, JPC, Kieber, JJ 2003Expression profiling of cytokinin action in arabidopsisPlant Physiol13219982011CrossRefPubMedGoogle Scholar
  67. Rawat, SR, Silim, SN, Kronzucker, HJ, Siddiqi, MY, Glass, ADM 1999AtAMT1 gene expression and NH4+ uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levelsPlant J19143152CrossRefPubMedGoogle Scholar
  68. Ribnicky, DM, Cooke, TJ, Cohen, JD 1998A microtechnique for the analysis of free and conjugated indole-3-acetic acid in milligram amounts of plant tissue using a benchtop gas chromatograph mass spectrometerPlanta20417CrossRefPubMedGoogle Scholar
  69. Riou-Khamlichi, C, Huntley, R, Jacqmard, A, Murray, JAH 1999Cytokinin activation of Arabidopsis cell division through a D-type cyclinScience28315411544CrossRefPubMedGoogle Scholar
  70. Samuelson, ME, Larsson, CM 1993Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N-assimilation and comparison with ammoniumPlant Sci937784CrossRefGoogle Scholar
  71. Scheible, WR, Lauerer, M, Schulze, ED, Caboche, M, Stitt, M 1997Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobaccoPlant J11671691CrossRefGoogle Scholar
  72. Schmelz, EA, Engelberth, J, Alborn, HT, O’Donnell, P, Sammons, M, Toshima, H, Tumlinson, JH 2003Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plantsProc Natl Acad Sci USA1001055210557CrossRefPubMedGoogle Scholar
  73. Searle, IR, Men, AE, Laniya, TS, Buzas, DM, Iturbe-Ormaetxe, I, Carroll, BJ, Gresshoff, PM 2003Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinaseScience299109112CrossRefPubMedGoogle Scholar
  74. Smith, CS, Weljie, AM, Moorhead, GBG 2003Molecular properties of the putative nitrogen sensor PII from Arabidopsis thalianaPlant J33353360CrossRefPubMedGoogle Scholar
  75. Takei, K, Sakakibara, H, Taniguchi, M, Sugiyama, T 2001Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulatorPlant Cell Physiol428593CrossRefPubMedGoogle Scholar
  76. Takei, K, Takahashi, T, Sugiyama, T, Yamaya, T, Sakakibara, H 2002Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokininJ Exp Bot53971977CrossRefPubMedGoogle Scholar
  77. Taniguchi, M, Kiba, T, Sakakibara, H, Ueguchi, C, Mizuno, T, Sugiyama, T 1998Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrateFEBS Lett429259262CrossRefPubMedGoogle Scholar
  78. Tomos, AD, Sharrock, RA 2001Cell sampling and analysis (SiCSA): metabolites measured at single cell resolutionJ Exp Bot52623630CrossRefPubMedGoogle Scholar
  79. Turnbull, CGN, Booker, JP, Leyser, HMO 2002Micrografting techniques for testing longdistance signalling in ArabidopsisPlant J32255262CrossRefPubMedGoogle Scholar
  80. Werf, A, Nagel, OW 1996Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose: opinionPlant Soil1852132Google Scholar
  81. Wagner, BM, Beck, E 1993Cytokinins in the perennial herb Urtica dioica L as Influenced by its nitrogen status.Planta190511518CrossRefGoogle Scholar
  82. Walch-Liu, P, Neumann, G, Bangerth, F, Engels, C 2000Rapid effects of nitrogen form on leaf morphogenesis in tobaccoJ Exp Bot51227237CrossRefPubMedGoogle Scholar
  83. Walch-Liu, P, Neumann, G, Engels, C 2001Response of shoot and root growth to supply of different nitrogen forms is not related to carbohydrate and nitrogen status of tobacco plantsZ Pflanz Bodenk16497103CrossRefGoogle Scholar
  84. Wang, XB, Wu, P, Xia, M, Wu, ZC, Chen, QS, Liu, FY 2002Identification of genes enriched in rice roots of the local nitrate treatment and their expression patterns in split-root treatmentGene29793102CrossRefPubMedGoogle Scholar
  85. Weiner, H, Blechschmidtschneider, S, Mohme, H, Eschrich, W, Heldt, HW 1991Phloem transport of amino acids: comparison of amino acid contents of maize leaves and of the sieve tube exudatePlant Physiol Biochem291923Google Scholar
  86. Werner, T, Motyka, V, Strnad, M, Schmulling, T 2001Regulation of plant growth by cytokininProc Natl Acad Sci USA981048710492CrossRefPubMedGoogle Scholar
  87. Wilkinson, S, Davies, WJ 2002ABA-based chemical signalling: the co-ordination of responses to stress in plantsPlant Cell Environ25195210CrossRefPubMedGoogle Scholar
  88. Winter, H, Lohaus, G, Heldt, HW 1992Phloem transport of amino acids in relation to their cytosolic levels in barley leavesPlant Physiol999961004Google Scholar
  89. Wopereis, J, Pajuelo, E, Dazzo, FB, Jiang, QY, Gresshoff, PM, Bruijn, FJ, Stougaard, J, Szczyglowski, K 2000Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotypePlant J2397114CrossRefPubMedGoogle Scholar
  90. Zhang, HM, Jennings, A, Barlow, PW, Forde, BG 1999Dual pathways for regulation of root branching by nitrateProc Natl Acad Sci USA9665296534CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Pia Walch-Liu
    • 1
  • Sophie Filleur
    • 1
  • Yinbo Gan
    • 1
    • 2
  • Brian G. Forde
    • 1
  1. 1.Department of Biological SciencesLancaster UniversityLancasterUK
  2. 2.Centre for Novel Agricultural ProductsUniversity of YorkYorkUK

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