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Biochemical Journal logoLink to Biochemical Journal
. 2000 May 1;347(Pt 3):749–755.

Involvement of NRAMP1 from Arabidopsis thaliana in iron transport.

C Curie 1, J M Alonso 1, M Le Jean 1, J R Ecker 1, J F Briat 1
PMCID: PMC1221012  PMID: 10769179

Abstract

Nramp genes code for a widely distributed class of proteins involved in a variety of processes, ranging from the control of susceptibility to bacterial infection in mammalian cells and taste behaviour in Drosophila to manganese uptake in yeast. Some of the NRAMP proteins in mammals and in yeast are capable of transporting metal ions, including iron. In plants, iron transport was shown to require a reduction/Fe(II) transport system. In Arabidopsis thaliana this process involves the IRT1 and Fro2 genes. Here we report the sequence of five NRAMP proteins from A. thaliana. Sequence comparison suggests that there are two classes of NRAMP proteins in plants: A. thaliana (At) NRAMP1 and Oriza sativa (Os) NRAMP1 and 3 (two rice isologues) represent one class, and AtNRAMP2-5 and OsNRAMP2 the other. AtNramp1 and OsNramp1 are able to complement the fet3fet4 yeast mutant defective both in low- and high-affinity iron transports, whereas AtNramp2 and OsNramp2 fail to do so. In addition, AtNramp1 transcript, but not AtNramp2 transcript, accumulates in response to iron deficiency in roots but not in leaves. Finally, overexpression of AtNramp1 in transgenic A. thaliana plants leads to an increase in plant resistance to toxic iron concentration. Taken together, these results demonstrate that AtNramp1 participates in the control of iron homoeostasis in plants.

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Selected References

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  1. Alonso J. M., Hirayama T., Roman G., Nourizadeh S., Ecker J. R. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science. 1999 Jun 25;284(5423):2148–2152. doi: 10.1126/science.284.5423.2148. [DOI] [PubMed] [Google Scholar]
  2. Belouchi A., Cellier M., Kwan T., Saini H. S., Leroux G., Gros P. The macrophage-specific membrane protein Nramp controlling natural resistance to infections in mice has homologues expressed in the root system of plants. Plant Mol Biol. 1995 Dec;29(6):1181–1196. doi: 10.1007/BF00020461. [DOI] [PubMed] [Google Scholar]
  3. Belouchi A., Kwan T., Gros P. Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol Biol. 1997 Apr;33(6):1085–1092. doi: 10.1023/a:1005723304911. [DOI] [PubMed] [Google Scholar]
  4. Bode H. P., Dumschat M., Garotti S., Fuhrmann G. F. Iron sequestration by the yeast vacuole. A study with vacuolar mutants of Saccharomyces cerevisiae. Eur J Biochem. 1995 Mar 1;228(2):337–342. [PubMed] [Google Scholar]
  5. Brunelli J. P., Pall M. L. A series of yeast/Escherichia coli lambda expression vectors designed for directional cloning of cDNAs and cre/lox-mediated plasmid excision. Yeast. 1993 Dec;9(12):1309–1318. doi: 10.1002/yea.320091204. [DOI] [PubMed] [Google Scholar]
  6. Cellier M., Belouchi A., Gros P. Resistance to intracellular infections: comparative genomic analysis of Nramp. Trends Genet. 1996 Jun;12(6):201–204. doi: 10.1016/0168-9525(96)30042-5. [DOI] [PubMed] [Google Scholar]
  7. Chen X. Z., Peng J. B., Cohen A., Nelson H., Nelson N., Hediger M. A. Yeast SMF1 mediates H(+)-coupled iron uptake with concomitant uncoupled cation currents. J Biol Chem. 1999 Dec 3;274(49):35089–35094. doi: 10.1074/jbc.274.49.35089. [DOI] [PubMed] [Google Scholar]
  8. D'Souza J., Cheah P. Y., Gros P., Chia W., Rodrigues V. Functional complementation of the malvolio mutation in the taste pathway of Drosophila melanogaster by the human natural resistance-associated macrophage protein 1 (Nramp-1). J Exp Biol. 1999 Jul;202(Pt 14):1909–1915. doi: 10.1242/jeb.202.14.1909. [DOI] [PubMed] [Google Scholar]
  9. Eide D. J. The molecular biology of metal ion transport in Saccharomyces cerevisiae. Annu Rev Nutr. 1998;18:441–469. doi: 10.1146/annurev.nutr.18.1.441. [DOI] [PubMed] [Google Scholar]
  10. Eide D., Broderius M., Fett J., Guerinot M. L. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5624–5628. doi: 10.1073/pnas.93.11.5624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fleming M. D., Romano M. A., Su M. A., Garrick L. M., Garrick M. D., Andrews N. C. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1148–1153. doi: 10.1073/pnas.95.3.1148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fleming M. D., Trenor C. C., 3rd, Su M. A., Foernzler D., Beier D. R., Dietrich W. F., Andrews N. C. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet. 1997 Aug;16(4):383–386. doi: 10.1038/ng0897-383. [DOI] [PubMed] [Google Scholar]
  13. Fobis-Loisy I., Loridon K., Lobréaux S., Lebrun M., Briat J. F. Structure and differential expression of two maize ferritin genes in response to iron and abscisic acid. Eur J Biochem. 1995 Aug 1;231(3):609–619. doi: 10.1111/j.1432-1033.1995.tb20739.x. [DOI] [PubMed] [Google Scholar]
  14. Fox T. C., Shaff J. E., Grusak M. A., Norvell W. A., Chen Y., Chaney R. L., Kochian L. V. Direct Measurement of 59Fe-Labeled Fe2+ Influx in Roots of Pea Using a Chelator Buffer System to Control Free Fe2+ in Solution. Plant Physiol. 1996 May;111(1):93–100. doi: 10.1104/pp.111.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gunshin H., Mackenzie B., Berger U. V., Gunshin Y., Romero M. F., Boron W. F., Nussberger S., Gollan J. L., Hediger M. A. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 1997 Jul 31;388(6641):482–488. doi: 10.1038/41343. [DOI] [PubMed] [Google Scholar]
  16. Kieber J. J., Rothenberg M., Roman G., Feldmann K. A., Ecker J. R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 Feb 12;72(3):427–441. doi: 10.1016/0092-8674(93)90119-b. [DOI] [PubMed] [Google Scholar]
  17. Liu X. F., Culotta V. C. Mutational analysis of Saccharomyces cerevisiae Smf1p, a member of the Nramp family of metal transporters. J Mol Biol. 1999 Jun 18;289(4):885–891. doi: 10.1006/jmbi.1999.2815. [DOI] [PubMed] [Google Scholar]
  18. Liu X. F., Culotta V. C. Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene. J Biol Chem. 1999 Feb 19;274(8):4863–4868. doi: 10.1074/jbc.274.8.4863. [DOI] [PubMed] [Google Scholar]
  19. Liu X. F., Supek F., Nelson N., Culotta V. C. Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem. 1997 May 2;272(18):11763–11769. doi: 10.1074/jbc.272.18.11763. [DOI] [PubMed] [Google Scholar]
  20. Loulergue C., Lebrun M., Briat J. F. Expression cloning in Fe2+ transport defective yeast of a novel maize MYC transcription factor. Gene. 1998 Dec 28;225(1-2):47–57. doi: 10.1016/s0378-1119(98)00531-9. [DOI] [PubMed] [Google Scholar]
  21. Nelson N. Metal ion transporters and homeostasis. EMBO J. 1999 Aug 16;18(16):4361–4371. doi: 10.1093/emboj/18.16.4361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Orgad S., Nelson H., Segal D., Nelson N. Metal ions suppress the abnormal taste behavior of the Drosophila mutant malvolio. J Exp Biol. 1998 Jan;201(Pt 1):115–120. doi: 10.1242/jeb.201.1.115. [DOI] [PubMed] [Google Scholar]
  23. Pinner E., Gruenheid S., Raymond M., Gros P. Functional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family. J Biol Chem. 1997 Nov 14;272(46):28933–28938. doi: 10.1074/jbc.272.46.28933. [DOI] [PubMed] [Google Scholar]
  24. Radisky D. C., Babcock M. C., Kaplan J. The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J Biol Chem. 1999 Feb 19;274(8):4497–4499. doi: 10.1074/jbc.274.8.4497. [DOI] [PubMed] [Google Scholar]
  25. Raguzzi F., Lesuisse E., Crichton R. R. Iron storage in Saccharomyces cerevisiae. FEBS Lett. 1988 Apr 11;231(1):253–258. doi: 10.1016/0014-5793(88)80742-7. [DOI] [PubMed] [Google Scholar]
  26. Reuber T. L., Ausubel F. M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell. 1996 Feb;8(2):241–249. doi: 10.1105/tpc.8.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Robinson N. J., Procter C. M., Connolly E. L., Guerinot M. L. A ferric-chelate reductase for iron uptake from soils. Nature. 1999 Feb 25;397(6721):694–697. doi: 10.1038/17800. [DOI] [PubMed] [Google Scholar]
  28. Rodrigues V., Cheah P. Y., Ray K., Chia W. malvolio, the Drosophila homologue of mouse NRAMP-1 (Bcg), is expressed in macrophages and in the nervous system and is required for normal taste behaviour. EMBO J. 1995 Jul 3;14(13):3007–3020. doi: 10.1002/j.1460-2075.1995.tb07303.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Supek F., Supekova L., Nelson H., Nelson N. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc Natl Acad Sci U S A. 1996 May 14;93(10):5105–5110. doi: 10.1073/pnas.93.10.5105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Touraine B., Glass A. D. NO3- and ClO3- fluxes in the chl1-5 mutant of Arabidopsis thaliana. Does the CHL1-5 gene encode a low-affinity NO3- transporter? Plant Physiol. 1997 May;114(1):137–144. doi: 10.1104/pp.114.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Vidal S. M., Malo D., Vogan K., Skamene E., Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell. 1993 May 7;73(3):469–485. doi: 10.1016/0092-8674(93)90135-d. [DOI] [PubMed] [Google Scholar]
  32. Yi Y., Guerinot M. L. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J. 1996 Nov;10(5):835–844. doi: 10.1046/j.1365-313x.1996.10050835.x. [DOI] [PubMed] [Google Scholar]
  33. van der Zaal B. J., Neuteboom L. W., Pinas J. E., Chardonnens A. N., Schat H., Verkleij J. A., Hooykaas P. J. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 1999 Mar;119(3):1047–1055. doi: 10.1104/pp.119.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]

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