Plant and Soil

, Volume 284, Issue 1–2, pp 101–108 | Cite as

Expression, localization, and regulation of the iron transporter LeIRT1 in tomato roots

  • A. Schikora
  • O. Thimm
  • B. Linke
  • T. J. Buckhout
  • M. Müller
  • W. Schmidt
Research Article


Iron deficiency induces an array of developmental, metabolic and physiological responses that aid in improved acquisition of iron. As part of these responses, some root epidermal cells of so-called strategy I species develop conspicuous ingrowths at the outer tangential walls typical of transfer cells. These cells, characterized by a high area/volume ratio and numerous mitochondria, are thought to support the uptake of iron from the rhizosphere into the root symplasm by preferentially harboring proteins involved in iron acquisition. In the present study, we have analyzed the expression of the iron-regulated transporters LeIRT1 and LeIRT2 at the transcriptional level and show that LeIRT1 but not LeIRT2 is up-regulated in both roots and shoots in tomato (Lycopersicon esculentum Mill.) upon iron deficiency. Split-root studies reveal that expression of LeIRT1 is higher in roots that have been grown in the presence of iron then in roots grown in the absence of iron. In contrast, the frequency of transfer cells is higher in iron-deficient split roots. Protein abundance of LeIRT1 followed the same pattern; although, the difference in LeIRT1 between the split-root halves is less pronounced than those of the transcripts. Immunocytochemical analysis showed that LeIRT1 protein is polarized to membranes of distal tangential walls of epidermal cells. Protein density is not markedly higher in transfer cells compared to normal rhizodermal cells, suggesting a non-specific support of iron uptake by transfer cells via an increase in the surface/volume ratio. The results further indicate separate regulatory pathways for developmental and physiological responses to iron deficiency.


Immunochemistry Iron uptake Real-time PCR Split-roots Transfer 


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  1. Bereczky, Z, Wang, HY, Schubert, V, Ganal, M, Bauer, P 2003Differential regulation of nramp and irt metal transporter genes in wild type and iron uptake mutants of tomatoJ Biol Chem2782469724704PubMedCrossRefGoogle Scholar
  2. Brüggemann, W, Maas-Kantel, K, Moog,  1993Iron uptake by leaf mesophyll cells: the role of the plasma membrane-bound ferric-chelate reductasePlanta190151155CrossRefGoogle Scholar
  3. Cohen, CK, Garvin, DF, Kochian, LV 2004Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soilPlanta218784792PubMedCrossRefGoogle Scholar
  4. Colangelo, EP, Guerinot, ML 2004The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency responsePlant Cell1634003412PubMedCrossRefGoogle Scholar
  5. Connolly, EL, Fett, JP, Guerinot, ML 2002Expression of the IRT1 Metal Transporter is controlled by Metals at the Level of Transcript and Protein AccumulationPlant Cell1413471357PubMedCrossRefGoogle Scholar
  6. Curie, C, Briat, JF 2003Iron transport and signaling in plantsAnnu Rev Plant Biol54183206PubMedCrossRefGoogle Scholar
  7. Curie, C, Alonso, JM, Le Jean, M, Ecker, JR, Briat, JF 2000Involvement of NRAMP1 from Arabidopsisthaliana in iron transportBiochem J374955CrossRefGoogle Scholar
  8. Eckhardt, U, Mas Marques, A, Buckhout, TJ 2001Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutantsPlant Mol Biol45437448PubMedCrossRefGoogle Scholar
  9. Eide, D, Broderius, M, Feit, J, Guerinot, ML 1996A novel iron-regulated metal transporter from plants identified by functional expression in yeastProc Natl Acad Sci USA9356245628PubMedCrossRefGoogle Scholar
  10. Henriques, R, Jásik, J, Klein, M, Martinoia, E, Feller, U, Schell, J, Pais, MS, Koncz, C 2002Knock out mutant of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defectsPlant Mol Biol50587597PubMedCrossRefGoogle Scholar
  11. Jakoby, M, Wang, HY, Reidt, W, Weisshaar, B, Bauer, P 2004FRU (BLHH029) is required for induction of iron mobilization genes in Arabidopsis thalianaFEBS Lett577528534PubMedCrossRefGoogle Scholar
  12. Lanquar, V, Lelièvre, F, Bolte, S, Hamès, C, Alcon, C, Neumann, D, Vansuyt, G, Curie, C, Schröder, A, Krämer, U, Barbier-BBrygoo, H, Thomine, S 2005Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low ironEMBO J2440414051PubMedCrossRefGoogle Scholar
  13. Li, L, Cheng, X, Ling, HQ 2004Isolation and characterization of Fe(III)-chelate reductase gene LeFRO1 in tomatoPlant Mol Biol54125136PubMedCrossRefGoogle Scholar
  14. Ling, HQ, Bauer, P, Bereczky, Z, Keller, BM 2002The tomato fer gene encoding a bHLH protein controls iron-uptake responses in rootsProc Natl Acad Sci USA991393813943PubMedCrossRefGoogle Scholar
  15. Offler, CE, McCurdy, DW, Patrick, JW, Talbot, MJ 2003Transfer cells: cells specialized for a special purposeAnnu Rev Plant Biol54431454PubMedCrossRefGoogle Scholar
  16. Robinson, NJ, Procter, CM, Conolly, EL, Guerinot, ML 1999A ferric-chelate reductase for iron uptake from soilsNature397694697PubMedCrossRefGoogle Scholar
  17. Römheld, V, Marschner, H 1986Evidence for a specific uptake system for iron phytosiderophores in roots of grassesPlant Physiol80175180PubMedCrossRefGoogle Scholar
  18. Schikora, A, Schmidt, W 2001Iron stress-induced epidermal cell fate is regulated independently from physiological acclimations to low iron availabilityPlant Physiol12516791687PubMedCrossRefGoogle Scholar
  19. Schikora, A, Schmidt, W 2002Formation of transfer cells and H+-ATPase expression in tomato roots under P and Fe deficiencyPlanta215304311PubMedCrossRefGoogle Scholar
  20. Schmidt, W 2003Iron solutions: acquisition strategies and signaling pathwaysTrends Plant Sci8188193PubMedCrossRefGoogle Scholar
  21. Schmidt, W, Bartels, M 1996Formation of root epidermal transfer cells in PlantagoPlant Physiol110217225PubMedGoogle Scholar
  22. Schmidt, W, Michalke, W, Schikora, A 2003Proton pumping by tomato roots. Effect of Fe deficiency and hormones on the activity and distribution of plasma membrane H+-ATPase in rhizodermal cellsPlant Cell Environ26361370CrossRefGoogle Scholar
  23. Thimm, O, Essigmann, B, Kloska, S, Altmann, T, Buckhout, TJ 2001Response of Arabidopsis to iron deficiency stress as revealed by microarray analysisPlant Physiol12710301043PubMedCrossRefGoogle Scholar
  24. Thomine, S, Lelièvre, F, Debarbieux, E, Schroeder, JI, Barbier-Brygoo, H 2003AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiencyPlant J34685695PubMedCrossRefGoogle Scholar
  25. Thomine, S, Wang, R, Ward, JM, Crawford, NM, Schroeder, JI 2000Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genesProc Natl Acad Sci USA9749914996PubMedCrossRefGoogle Scholar
  26. Vert, G, Briat, JF, Curie, C 2001Arabidopsis IRT2 gene encodes a root-periphery iron transporterPlant J26181189PubMedCrossRefGoogle Scholar
  27. Vert, G, Briat, JF, Curie, C 2003Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signalsPlant Physiol132796804PubMedCrossRefGoogle Scholar
  28. Vert, G, Grotz, N, Dedaldechamp, F, Gaymard, F, Guerinot, ML, Briat, JF, Curie, C 2002IRT1, an Arabidopsis transporter essential for iron uptake from the soil and plant growthPlant Cell1412231233PubMedCrossRefGoogle Scholar
  29. Varotto, C, Maiwald, D, Pesaresi, P, Jahns, P, Salamini, F, Leister, D 2002The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thalianaPlant J31589599PubMedCrossRefGoogle Scholar
  30. Wang, YH, Garvin, DF, Kochian, LV 2002Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signalsPlant Physiol13013611370PubMedCrossRefGoogle Scholar
  31. Waters, BW, Blevins, DG, Eide, DJ 2002Characterization of FRO1, a pea ferric-chelate reductase involved in iron acquisitionPlant Physiol1298594PubMedCrossRefGoogle Scholar
  32. Wu, H, Li, L, Du, J, Yuan, Y, Cheng, X, Ling, H-Q 2005Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thalianaPlant Cell Physiol4615051514PubMedCrossRefGoogle Scholar
  33. Yuan, YX, Zhang, J, Wang, DW, Ling, HQ 2005AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plantsCell Res15613621PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • A. Schikora
    • 1
  • O. Thimm
    • 2
  • B. Linke
    • 3
  • T. J. Buckhout
    • 3
  • M. Müller
    • 3
  • W. Schmidt
    • 4
  1. 1.Biochimie et Physiologie Moléculaire des PlantesINRAMontpellier Cedex 01France
  2. 2.Metanomics GmbHBerlinGermany
  3. 3.Institute of BiologyHumboldt-University BerlinBerlinGermany
  4. 4.Institute of Plant and Microbial BiologyAcademia SinicaNankang, TaipeiRepublic of China

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