Skip to main content
SpringerLink
Log in

Molecular Mechanisms of Urea Transport in Plants

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Urea is a soil nitrogen form available to plant roots and a secondary nitrogen metabolite liberated in plant cells. Based on growth complementation of yeast mutants and “in-silico analysis”, two plant families have been identified and partially characterized that mediate membrane transport of urea in heterologous expression systems. AtDUR3 is a single Arabidopsis gene belonging to the sodium solute symporter family that cotransports urea with protons at high affinity, while members of the tonoplast intrinsic protein (TIP) subfamily of aquaporins transport urea in a channel-like manner. The following review summarizes current knowledge on the membrane localization, energetization and regulation of these two types of urea transporters and discusses their possible physiological roles in planta.

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.
Fig. 3.

Similar content being viewed by others

References

  • Bailey C.J., D. Boulter 1971. Urease, a typical seed protein of the Leguminosae. In: Chemotaxonomy of the Leguminosae. J. Harborne, D. Boulter, B. Turner, eds. Academic Press, New York pp 485–502

    Google Scholar 

  • Barkla B.J., R. Vera-Estrella, O. Pantoja, H.H. Kirch, H.J. Bohnert 1999. Aquaporin localization – how valid are the TIP and PIP labels?. Trends Plant Sci. 4:86–88

    Article  PubMed  Google Scholar 

  • Beitz E., B. Wu, L.M. Holm, J.F. Schultz, T. Zeuthen 2006. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia and protons. Proc. Natl. Acad. Sci. USA 103:269–274

    Article  PubMed  CAS  Google Scholar 

  • Bradley D.P., M.A. Morgan, P. O´Toole 1989. Uptake and apparent utilization of urea and ammonium nitrate in wheat seedlings. Fertil. Res. 20:41–49

    Article  CAS  Google Scholar 

  • Carter C., S. Pan, J. Zouhar, E.L. Avila, T. Girke, N.V. Raikhel 2004. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell. 16:3285–3303

    Article  PubMed  CAS  Google Scholar 

  • Cho B.C., M.G. Park, J.H. Shim, F. Azam 1996. Significance of bacteria in urea dynamics in coastal surface waters. Mar. Ecol. Prog. Ser. 142:19–26

    Google Scholar 

  • Cooper T.G., R. Sumrada 1975. Urea transport in Saccharomyces cerevisiae. J. Bacteriol. 121:571–576

    PubMed  CAS  Google Scholar 

  • Dalal R.C. 1985. Distribution, salinity, kinetic and thermodynamic characteristics of urease activity in a vertisol profile. Aust. J. Soil Res. 23:49–60

    Article  Google Scholar 

  • Daniels M.J., F. Chaumont, T.E. Mirkov, M.J. Chrispeels 1996. Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell. 8:587–599

    Article  PubMed  CAS  Google Scholar 

  • Eckert M., A. Biela, F. Siefritz, R. Kaldenhoff 1999. New aspects of plant aquaporin regulation and specificity. J. Exp. Bot. 50:1541–1545

    Article  CAS  Google Scholar 

  • ElBerry H.M., M.L. Majumdar, T.S. Cunningham, R.A. Sumrada, T.G. Cooper 1993. Regulation of the urea active transporter gene (DUR3) in Saccharomyces cerevisiae. J. Bacteriol. 175:4688–4698

    PubMed  CAS  Google Scholar 

  • Faye L., J.S. Greenwood, M. Chrispeels 1986. Urease in jack bean seeds is a cytosolic protein. Planta 168:579–585

    Article  CAS  Google Scholar 

  • Fu D., A. Libson, L.J.W. Miercke, C. Weitzman, P. Nollert, J. Krucinski, R.M. Stroud 2000. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–486

    Article  PubMed  CAS  Google Scholar 

  • Galluci E., C. Micelli, C. Lippe 1971. Non-electrolyte permeability across thin lipid membranes. Arch. Int. Physiol. Biochem. 79:881–887

    Google Scholar 

  • Gaudin R., J. Dupuyu, P. Bournat 1987. Suivi du contenue en azote de la solution du sol d’une rizière après placement d’urée. Agron. Trop. 42:13–19

    Google Scholar 

  • Gazzarrini S., L. Lejay, A. Gojon, O. Ninnemann, W.B. Frommer, N. von Wirén 1999. Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–947

    Article  PubMed  CAS  Google Scholar 

  • Gerbeau P., J. Guclu, P. Ripoche, C. Maurel 1999. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J. 18:577–587

    Article  PubMed  CAS  Google Scholar 

  • Holland M.A., J.D. Griffin, L.E. Meyer-Bothling, J.C. Polacco 1987. Developmental genetics of the soybean urease isozymes. Dev. Genet. 8:375–387

    Article  CAS  Google Scholar 

  • Ishibashi K., S. Sasaki, K. Fushimi, S. Uchida, M. Kuwahara, H. Saito, T. Furukawa, K. Nakajima, Y. Yamaguchi, T. Gojobori, F. Marumo 1994. Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc. Natl. Acad. Sci. USA 91:6269–6273

    Article  PubMed  CAS  Google Scholar 

  • Johanson U., M. Karlsson, I. Johansson, S. Gustavsson, S. Sjovall, L. Fraysse, A.R. Weig, P. Kjellbom 2001. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126:1358–1369

    Article  PubMed  CAS  Google Scholar 

  • Jung H. 2002. The sodium/substrate symporter family: structural and functional features. FEBS Lett. 529:73–77

    Article  PubMed  CAS  Google Scholar 

  • Kerr P.S., D.G. Bievins, B.J. Rapp, D.D. Randell 1983. Soybean leaf urease: comparison with seed urease. Physiol. Plant. 57:339–342

    Article  CAS  Google Scholar 

  • King S.L., D. Kozono, P. Agre 2004. From structure to disease: The evolving tale of aquaporin biology. Nat. Rev. Mol. Cell Biol. 5:687–698

    Article  PubMed  CAS  Google Scholar 

  • Klebl F., M. Wolf, N. Sauer 2003. A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana [delta]-TIP or [gamma]-TIP. FEBS Lett. 547:69–74

    Article  PubMed  CAS  Google Scholar 

  • Krogmeier M.J., G.W. McCarty, J.M. Bremner 1989. Phytotoxicity of foliar-applied urea. Proc. Natl. Acad. Sci. USA 86:8189–8191

    Article  PubMed  CAS  Google Scholar 

  • Lejay L., P. Tillard, M. Lepetit, F.D. Olive, S. Filleur, F. Daniel-Vedele, A. Gojon 1999. Molecular and functional regulation of two NO -3 uptake systems by N- and C-status of Arabidopsis plants. Plant J. 18:509–519

    Article  PubMed  CAS  Google Scholar 

  • Leung D.W., D.D.F. Loo, B.A. Hirayama, T. Zeuthen, E.M. Wright 2000. Urea transport by cotransporters. J. Physiol. 528:251–257

    Article  PubMed  CAS  Google Scholar 

  • Liu L.H., U. Ludewig, W.B. Frommer, N. von Wirén 2003a. AtDUR3 encodes a new type of high-affinity urea/H+ symporter in Arabidopsis. Plant Cell 15:790–800

    Article  CAS  Google Scholar 

  • Liu L.H., U. Ludewig, B. Gassert, W.B. Frommer, N. von Wirén 2003b. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 133:1220–1228

    Article  CAS  Google Scholar 

  • Ludevid D., H. Höfte, E. Himelblau, M.J. Chrispeels 1992. The expression pattern of the tonoplast intrinsic protein χ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 100:1627–1633

    Article  Google Scholar 

  • Ma S., T.M. Quist, A. Ulanov, R. Joly, H.J. Bohnert 2004. Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. Plant J. 40:845–859

    Article  PubMed  CAS  Google Scholar 

  • Marmagne A., M.A. Rouet, M. Ferro, N. Rolland, C. Alcon, J. Joyard, J. Garin, H. Barbier-Brygoo, G. Ephritikhine 2004. Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Mol. Cell Proteomics 3:675–691

    Article  PubMed  CAS  Google Scholar 

  • Marschner H. 1995. Mineral nutrition of higher plants. Second ed. Academic Press, London, UK

    Google Scholar 

  • Masclaux C., M.H. Valadier, N. Brugiere, J.F. Morot-Gaudry, B. Hirel 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

    Article  PubMed  CAS  Google Scholar 

  • Mitamura O., M. Kawashima, H. Maeda 2000a. Urea degradation by picophytoplankton in the euphotic zone of Lake Biwa. Limnology 1:19–26

    Article  CAS  Google Scholar 

  • Mitamura O., Y. Seike, K. Kondo, N. Ishida, M. Okumura 2000b. Urea decomposing activity of fractionated brackish phytoplankton in Lake Nakaumi. Limnology 1:75–80

    Article  CAS  Google Scholar 

  • Polacco J.C., M.A. Holland 1993. Roles of urease in plant cells. Int. Rev. Cytology - Survey Cell Biol. 145:65–103

    CAS  Google Scholar 

  • Quigley F., J.M. Rosenberg, Y. Shachar-Hill, H.J. Bohnert 2001. From genome to function: the Arabidopsis aquaporins. Genome Biol. 3:17

    Article  Google Scholar 

  • Reizer J., A. Reizer, J. Saier 1994. A functional superfamily of sodium/solute symporters. Biochim. Biophys. Acta – Rev. Biomembr. 1197:133–166

    CAS  Google Scholar 

  • Saier M.H., Jr. 2000. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:354–411

    Article  PubMed  CAS  Google Scholar 

  • Saito C., T. Ueda, H. Abe, Y. Wada, T. Kuroiwa, A. Hisada, M. Furuya, A. Nakano 2002. A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J. 29:245–255

    Article  PubMed  Google Scholar 

  • Schmid M., T.S. Davison, S.R. Henz, U.J. Pape, M. Demar, M. Vingron, B. Schölkopf, D. Weigel, J.U. Lohmann 2005. A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37:501–506

    Article  PubMed  CAS  Google Scholar 

  • Schwacke R., A. Schneider, E. van der Graaff, K. Fischer, E. Catoni, M. Desimone, W.B. Frommer, U.I. Flugge, R. Kunze 2003. ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26

    Article  PubMed  CAS  Google Scholar 

  • Stebbins N.E., J.C. Polacco 1995. Urease is not essential for ureide degradation in soybean. Plant Physiol. 109:169–175

    PubMed  CAS  Google Scholar 

  • Sui H., B.-G. Han, J.K. Lee, P. Walian, B.K. Jap 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878

    Article  PubMed  CAS  Google Scholar 

  • Sumrada R., M. Gorski, T. Cooper 1976. Urea transport-defective strains of Saccharomyces cerevisiae. J. Bacteriol. 125:1048–1056

    PubMed  CAS  Google Scholar 

  • Thomas D., P. Bron, G. Ranchy, L. Duchesne, A. Cavalier, J.-P. Rolland, C. Raguénès-Nicol, J.-F. Hubert, W. Haase, C. Delamarche 2005. Aquaglyceroporins, one channel for two molecules. Biochim. Biophys. Acta- Bioenergetics 1555:181–186

    Article  Google Scholar 

  • Tsukaguchi H., C. Shayakul, U.V. Berger, B. Mackenzie, S. Devidas, W.B. Guggino, A.N. van Hoek, M.A. Hediger 1998. Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 273:24737–24743

    Article  PubMed  CAS  Google Scholar 

  • Turk E., E.M. Wright 1997. Membrane topology motifs in the SGLT cotransporter family. J. Membr. Biol. 159:1–20

    Article  PubMed  CAS  Google Scholar 

  • Tyerman S., H. Bohnert, C. Maurel, E. Steudle, J. Smith 1999. Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J. Exp. Bot. 50:1055–1071

    Article  CAS  Google Scholar 

  • Valladares A., M.L. Montesinos, A. Herrero, E. Flores 2002. An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol. Microbiol. 43:703–715

    Article  PubMed  CAS  Google Scholar 

  • Wallace I.S., D.M. Roberts 2004. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol. 135:1059–1068

    Article  PubMed  CAS  Google Scholar 

  • Watson C.J., H. Miller, P. Poland, D.J. Kilpatrick, M.D.B. Allen, M.K. Garret, C.B. Christianson 1994. Soil properties and the ability of the urease inhibitor N-(N-Butyl)thiophosphoric triamide (NBTPT) to reduce ammonia volatilization from surface-applied urea. Soil Biol. Biochem. 26:1165–1171

    Article  CAS  Google Scholar 

  • Weig A., C. Deswarte, M.J. Chrispeels 1997. The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol. 114:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Wilson M.R., S.I. O´Donoghue, N.A. Walker 1988. The transport and metabolism of urea in Chara australis: III. Two specific transport systems. J. Exp. Bot. 39:763–774

    Article  CAS  Google Scholar 

  • Wilson M.R., N.A. Walker 1988. The transport and metabolism of urea in Chara australis: I. Passive diffusion, specific transport and metabolism of urea and methylurea. J. Exp. Bot. 39:739–751

    Article  CAS  Google Scholar 

  • Witte C.P., S.A. Tiller, M.A. Taylor, H.V. Davies 2002. Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of 15N after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiol. 128:1129–1136

    Article  PubMed  CAS  Google Scholar 

  • Xu X., L. Zhou, O. Van Cleemput, Z. Wang 2000. Fate of urea-15N in a soil-wheat system as influenced by urease inhibitor hydroquinone and nitrification inhibitor dicyandiamide. Plant Soil 220:261–270

    Article  CAS  Google Scholar 

  • You G., C.P. Smith, Y. Kanai, W.S. Lee, M. Stelzner, M.A. Hediger 1993. Cloning and characterization of the vasopressin-regulated urea transporter. Nature 365:844–847

    Article  PubMed  CAS  Google Scholar 

  • Zardoya R. 2005. Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414

    PubMed  CAS  Google Scholar 

  • Zonia L.E., N.E. Stebbins, J.C. Polacco 1995. Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol 107:1097–1103

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Pflanzenernährung (330), Universität Hohenheim, Fruwirthstrasse 20, 70599, Stuttgart, Germany

    S. Kojima, A. Bohner & N. von Wirén

Authors
  1. S. Kojima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Bohner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. von Wirén
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. von Wirén.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kojima, S., Bohner, A. & von Wirén, N. Molecular Mechanisms of Urea Transport in Plants. J Membrane Biol 212, 83–91 (2006). https://doi.org/10.1007/s00232-006-0868-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-006-0868-6

Keywords

Search

Navigation