Skip to main content
SpringerLink
Log in

Metal Transport

  • Chapter
  • First Online:
The Plant Plasma Membrane

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 19))

  • 2246 Accesses

Abstract

One-third of all proteins require metal cofactors for function, yet metals can be toxic and need to be tightly controlled. Metal homeostasis is basically the equilibrium between metal uptake and metal efflux, making metal transporters key players in controlling cellular metal content. Here, we review the major families of metal transporters that participate in transport of divalent metal cations, focusing on Fe, about which the most is known.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abboud S, Haile DJ (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem 275:19906–19912

    Article  CAS  PubMed  Google Scholar 

  • Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251

    Article  CAS  PubMed  Google Scholar 

  • Andres-Colas N, Sancenon V, Rodriguez-Navarro S, Mayo S, Thiele DJ, Ecker JR, Puig S, Penarrubia L (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236

    Article  CAS  PubMed  Google Scholar 

  • Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2009) OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol. doi:10.1007/s11103-009-9500-3

    PubMed  Google Scholar 

  • Argüello JM (2003) Identification of ion selectivity determinants in heavy metal transport P1B-tpe ATPases. J Membr Biol 195:93–108

    Article  PubMed  CAS  Google Scholar 

  • Arrivault S, Senger T, Kramer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879

    Article  CAS  PubMed  Google Scholar 

  • Atkinson PG, Blackwell JM, Barton CH (1997) Nramp1 locus encodes a 65 kDa interferon-gamma-inducible protein in murine macrophages. Biochem J 325:779–786

    CAS  PubMed  Google Scholar 

  • Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101

    Article  CAS  PubMed  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S, Su XC, Miras R, Bal N, Mintz E, Catty P, Shokes JE, Scott RA (2006) Structural basis for metal binding specificity: the N-terminal cadmium binding domain of the P1-type ATPase CadA. J Mol Biol 356:638–650

    Article  CAS  PubMed  Google Scholar 

  • Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628

    Article  CAS  PubMed  Google Scholar 

  • Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268

    Article  CAS  PubMed  Google Scholar 

  • Blaudez D, Kohler A, Martin F, Sanders D, Chalot M (2003) Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15:2911–2928

    Article  CAS  PubMed  Google Scholar 

  • Borjigin J, Payne AS, Deng J, Li X, Wang MM, Ovodenko B, Gitlin JD, Snyder SH (1999) A novel pineal night-specific ATPase encoded by the Wilson disease gene. J Neurosci 19:1018–1026

    CAS  PubMed  Google Scholar 

  • Bughio N, Yamaguchi H, Nishizawa N, Nakanishi H, Mori S (2002) Cloning an iron-regulated metal transporter from rice. J Exp Bot 53:1677–1682

    Article  CAS  PubMed  Google Scholar 

  • Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  PubMed  Google Scholar 

  • Cailliatte R, Lapeyre B, Briat J-F, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228

    Article  CAS  PubMed  Google Scholar 

  • Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P (1999) Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93:4406–4417

    CAS  PubMed  Google Scholar 

  • Changela A, Chen K, Xue Y, Holschen J, Outten CE, O’Halloran TV, Mondragon A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387

    Article  CAS  PubMed  Google Scholar 

  • Cobbett CS, Hussain D, Haydon MJ (2003) Structural and functional relationships between type 1B heavy metal-transporting P-type ATPases in Arabidopsis. New Phytol 159:315–321

    Article  CAS  Google Scholar 

  • Cohen A, Nelson H, Nelson N (2000) The family of SMF metal ion transporters in yeast cells. J Biol Chem 275:33388–33394

    Article  CAS  PubMed  Google Scholar 

  • Cohen CK, Garvin DF, Kochian LV (2004) Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 218:784–792

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Briat J-F (2003) Iron transport and signaling in plants. Annu Rev Plant Biol 54:183–206

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat J-F (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat J-F, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Cassin G, Counch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nictotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11

    Article  CAS  PubMed  Google Scholar 

  • Dancis A, Haile D, Yuan DS, Klausner RD (1994) The Saccharomyces cerevisiae copper transport protein (Ctr1p). J Biol Chem 41:25660–25667

    Google Scholar 

  • De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM (2009) Three-dimensional structure of the human copper transporter hCTR1. Proc Natl Acad Sci USA 106:4237–4242

    Article  PubMed  Google Scholar 

  • Delhaize E, Kataoka T, Hebb DM, White RG, Ryan PR (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15:1131–1142

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Gruber BD, Pittman JK, White G, Leung H, Miao Y, Jiang L, Ryan PR, Richardson AE (2007) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J 51:198–210

    Article  CAS  PubMed  Google Scholar 

  • Desbrosses-Fonrouge AG, Voigt K, Schroder A, Arrivault S, Thomine S, Kramer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579:4165–4174

    Article  CAS  PubMed  Google Scholar 

  • DiDonato RJ, Roberts L, Sanderson T, Eisley R, Walker E (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414

    Article  CAS  PubMed  Google Scholar 

  • Donovan A, Brownlie A, Zhou Y, Shepard J, Pratt SJ, Moynihan J, Paw BH, Drejer A, Barut B, Zapata A, Law TC, Brugnara C, Lux SE, Pinkus GS, Pinkus JL, Kingsley PD, Palis J, Fleming MD, Andrews NC, Zon LI (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403:776–781

    Article  CAS  PubMed  Google Scholar 

  • Dufner-Beattie J, Langmade SJ, Wang F, Eide D, Andrews GK (2003a) Structure, function, and regulation of a subfamily of mouse zinc transport genes. J Biol Chem 278:50142–50150

    Article  CAS  PubMed  Google Scholar 

  • Dufner-Beattie J, Wang F, Kuo Y-M, Gitschier J, Eide D, Andrews GK (2003b) The acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J Biol Chem 278:33474–33481

    Article  CAS  PubMed  Google Scholar 

  • Eckhardt U, Marques AM, Buckhout TJ (2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol Biol 45:437–448

    Article  CAS  PubMed  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628

    Article  CAS  PubMed  Google Scholar 

  • Ellis CD, Wang F, MacDiarmid CW, Clark S, Lyons TJ, Eide DJ (2004) Zinc and Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 3:323–335

    Google Scholar 

  • Ellis CD, Macdiarmid CW, Eide DJ (2005) Heteromeric protein complexes mediate zinc transport into the secretory pathway of eukaryotic cells. J Biol Chem 280:28811–28818

    Article  CAS  PubMed  Google Scholar 

  • Eng BH, Guerinot ML, Eide D, Saier MHJ (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166:1–7

    Article  CAS  PubMed  Google Scholar 

  • Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting PIIB-Type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723

    Article  CAS  PubMed  Google Scholar 

  • Finney LA, O’Halloran TV (2003) Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300:931–936

    Article  CAS  PubMed  Google Scholar 

  • Fleming MD, Trenor CC, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16:383–386

    CAS  PubMed  Google Scholar 

  • Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95:1148–1153

    Article  CAS  PubMed  Google Scholar 

  • Forbes JR, Cox DW (2000) Copper-dependent trafficking of Wilson disease mutant ATP7B proteins. Hum Mol Genet 9:1927–1935

    Article  CAS  PubMed  Google Scholar 

  • Forbes JR, Gros P (2003) Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 102:1884–1892

    Article  CAS  PubMed  Google Scholar 

  • Gadd GM, Laurence OS (1996) Demonstration of high-affinity Mn2+ uptake in Saccharomyces cerevisiae. Microbiology 142:1159–1167

    Article  CAS  PubMed  Google Scholar 

  • Gaither LA, Eide DJ (2000) Functional expression of the human hZIP2 zinc transporter. J Biol Chem 275:5560–5564

    Article  CAS  PubMed  Google Scholar 

  • Gaither LA, Eide DJ (2001) The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J Biol Chem 276:22258–22264

    Article  CAS  PubMed  Google Scholar 

  • Gitan RS, Eide DJ (2000) Zinc-regulated ubiquitin conjugation signals endocytosis of the yeast ZRT1 zinc transporter. Biochem J 346:329–336

    Article  CAS  PubMed  Google Scholar 

  • Gitan RS, Luo H, Rodgers J, Broderius M, Eide D (1998) Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J Biol Chem 273:28617–28624

    Article  CAS  PubMed  Google Scholar 

  • Goswami T, Bhattacharjee A, Babal P, Searle S, Moores E, Li M, Blackwell JM (2001) Natural-resistance-associated macrophage protein 1 is a H+/bivalent cation antiporter. Biochem J 354:511–519

    Article  CAS  PubMed  Google Scholar 

  • Gouaux E, Mackinnon R (2005) Principles of selective ion transport in channels and pumps. Science 310:1461–1465

    Article  CAS  PubMed  Google Scholar 

  • Govoni G, Gros P (1998) Macrophage NRAMP1 and its role in resistance to microbial infections. Inflamm Res 47:277–284

    Article  CAS  PubMed  Google Scholar 

  • Grass G, Wong MD, Rosen BP, Smith RL, Rensing C (2002) ZupT is a Zn(II) uptake system in E. coli. J Bacteriol 184:864–866

    Article  CAS  PubMed  Google Scholar 

  • Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611

    Article  CAS  PubMed  Google Scholar 

  • Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561:22–28

    Article  CAS  PubMed  Google Scholar 

  • Grotz N, Fox T, Connolly EL, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95:7220–7224

    Article  CAS  PubMed  Google Scholar 

  • Gruenheid S, Pinner E, Desjardins M, Gros P (1997) Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of phagosomes. J Exp Med 185:717–730

    Article  CAS  PubMed  Google Scholar 

  • Gruenheid S, Canonne-Hergaux F, Gauthier S, Hackam DJ, Grinstein S, Gros P (1999) The iron transport protein NRAMP2 is an integral membrane glycoprotein that co-localizes with transferrin in recycling endosomes. J Exp Med 189:831–841

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820

    CAS  PubMed  Google Scholar 

  • Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488

    Article  CAS  PubMed  Google Scholar 

  • Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Biol 54:2601–2613

    CAS  Google Scholar 

  • Hamburger D, Rezzonico E, Petétot JM-C, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  CAS  PubMed  Google Scholar 

  • Henriques R, Jásik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C (2002) Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol Biol 50:587–597

    Article  CAS  PubMed  Google Scholar 

  • Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393

    Article  CAS  PubMed  Google Scholar 

  • Hung JH, Suzuki M, Yamaguchi Y, Yuan DS, Klausner RD, Gitlin JD (1997) Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J Biol Chem 272:21461–21466

    Article  CAS  PubMed  Google Scholar 

  • Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339

    Article  CAS  PubMed  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2008) Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284:3470–3479

    Article  PubMed  CAS  Google Scholar 

  • Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–3214

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346

    Article  CAS  PubMed  Google Scholar 

  • Kampfenkel K, Kushnir S, Babiychuk E, Inzé D, Van Montagu M (1995) Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J Biol Chem 270:28479–28486

    Article  CAS  PubMed  Google Scholar 

  • Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis IRT1 metal transporter requires lysine residues. Plant Physiol 146:1964–1973

    Article  CAS  PubMed  Google Scholar 

  • Khush GS (2005) What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol 59:1–6

    Article  CAS  PubMed  Google Scholar 

  • Kim BE, Wang F, Dufner-Beattie J, Andrews GK, Eide DJ, Petris MJ (2004) Zn2+-stimulated endocytosis of the mZIP4 zinc transporter regulates its location at the plasma membrane. J Biol Chem 279:4523–4530

    Article  CAS  PubMed  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron acquisition-related genes in iron-deficient rice is coordinately induced by partially conserved iron-deficiency-responsive elements. J Exp Bot 56:1305–1316

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, Kimura K, Iuchi S, Kobayashi M, Taylor GJ, Koyama H (2008) Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. Plant Physiol 148:969–980

    Article  CAS  PubMed  Google Scholar 

  • Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424

    Article  CAS  PubMed  Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with broad specificity. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Kumanovics A, Poruk KE, Osborne KA, Ward DM, Kaplan J (2006) The YKE4 (YIL023C) encodes a bidirectional zinc transporter in the endoplasmic reticulum of S. cerevisiae. J Biol Chem 281:22566–22574

    Article  CAS  PubMed  Google Scholar 

  • Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schroder A, Kramer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    Article  CAS  PubMed  Google Scholar 

  • Lasswell J, Rogg LE, Nelson DC, Rongey C, Bartel B (2000) Cloning and characterization of IAR1, a gene required for auxin conjugate sensitivity in Arabidopsis. Plant Cell 12:2395–2408

    CAS  PubMed  Google Scholar 

  • Le Jean M, Schikora A, Mari S, Briat JF, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J 44:769–782

    Article  PubMed  CAS  Google Scholar 

  • Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulation in rice. Plant Cell Environ 32:408–416

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800

    Article  CAS  PubMed  Google Scholar 

  • Li L, Kaplan J (2001) The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J Biol Chem 276:5036–5043

    Article  CAS  PubMed  Google Scholar 

  • Li Z-S, Lu Y-P, R-G Z, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cervisiae: YCF1-catayzed transport of bis (glutathionato) cadmium. Proc Natl Acad Sci USA 94:42–47

    Article  CAS  PubMed  Google Scholar 

  • Lin Y-F, Liang H-M, Yang S-Y, Boch A, Clemens S, Chen C-C, Wu J-F, Huang J-L, Yeh K-C (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404

    Article  CAS  PubMed  Google Scholar 

  • Liu XF, Culotta VC (1999) Mutational analysis of Saccharomyces cerevisiae Smf1p, a member of the Nramp family of metal transporters. J Mol Biol 289:885–891

    Article  CAS  PubMed  Google Scholar 

  • Liu XF, Supek F, Nelson H, Culotta VC (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem 272:11763–11769

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Zhu Q, Zhang Z, Xu J, Yang J, Wong MH (2005) Variations in cadimum accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric 85:147–153

    Article  CAS  Google Scholar 

  • MacDiarmid CW, Gaither LA, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845–2855

    Article  CAS  PubMed  Google Scholar 

  • MacDiarmid CW, Milanick MA, Eide DJ (2003) Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J Biol Chem 278:15065–15072

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie B, Hediger MA (2004) SLC11 family of H+-coupled metal-ion transporters NRAMP1 and DMT1. Eur J Physiol 447:571–579

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, Boston

    Google Scholar 

  • McKie AT, Marciana P, Rolfs A, Brennan K, Wehr K, Barow D, Miret S, Bomford A, Peters TJ, Farzaneh F, Hediger MA, Hentze MW, Simpson RJ (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell 5:299–309

    Article  CAS  PubMed  Google Scholar 

  • Mercer JF, Barnes N, Stevenson J, Strausak D, Llanos RM (2003) Copper-induced trafficking of the cU-ATPases: a key mechanism for copper homeostasis. Biometals 16:175–184

    Article  CAS  PubMed  Google Scholar 

  • Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J 35:164–176

    Article  CAS  PubMed  Google Scholar 

  • Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791

    Article  CAS  PubMed  Google Scholar 

  • Moreau S, Tohomson RW, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific transporter in soybean. J Biol Chem 277:4738–4746

    Article  CAS  PubMed  Google Scholar 

  • Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904

    Article  CAS  PubMed  Google Scholar 

  • Mori S, Nishsizawa NK, Hayashi H, Chino M, Yoshimura E, Ishihara J (1991) Why are young rice plants highly susceptible to iron deficiency? Plant Soil 130:143–156

    Article  CAS  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419

    Article  PubMed  CAS  Google Scholar 

  • Nagasaka S, Takahashi M, Nakanishi-Itai R, Bashir K, Nakanishi H, Mori S, Nishizawa NK (2009) Time course analysis of gene expression over 24 hours in Fe-deficient barley roots. Plant Mol Biol 69:621–631

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances Cd uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:1–6

    Article  CAS  Google Scholar 

  • Nies DH (2007) How cells control zinc homeostasis. Science 317:1695–1696

    Article  CAS  PubMed  Google Scholar 

  • Nose Y, Kim BE, Thiele DJ (2006) Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metab 4:235–244

    Article  CAS  PubMed  Google Scholar 

  • Outten CE, O’Halloran TV (2001) Fentommolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492

    Article  CAS  PubMed  Google Scholar 

  • Payne AS, Gitlin JD (1998) Functional expression of the Menkes disease protein reveals common biochemical mechanisms among the copper-transporting P-type ATPases. J Biol Chem 273:3765–3770

    Article  CAS  PubMed  Google Scholar 

  • Pedas P, Ytting CK, Fuglsang AT, Jahm TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466

    Article  CAS  PubMed  Google Scholar 

  • Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJ, Blaudez D, Chalot M, Sanders D (2007) A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci USA 104:8532–8537

    Article  CAS  PubMed  Google Scholar 

  • Pena MM, Puig S, Thiele DJ (2000) Characterization of the Saccharomyces cerevisiae high affinity copper transporter Ctr3. J Biol Chem 275:33244–33251

    Article  CAS  PubMed  Google Scholar 

  • Pinner E, Gruenheid S, Raymond M, Gros P (1997) 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 272:28933–28938

    Article  CAS  PubMed  Google Scholar 

  • Portnoy ME, Liu XF, Culotta VC (2000) Saccharomyces cereivisiae expresses three functionally distinct homologues of the Nramp family of metal transporters. Mol Cell Biol 20:7893–7902

    Article  CAS  PubMed  Google Scholar 

  • Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O’Halloran TV (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284:805–808

    Article  CAS  PubMed  Google Scholar 

  • Ramesh SA, Shin R, Eide DJ, Schachtman DP (2003) Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol 133:126–134

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149

    Article  CAS  Google Scholar 

  • Reeves PG, Chaney RL (2004) Marginal nutritional status of zinc, iron, and calcium increases cadmium retention in the duodenum and other organs of rats fed rice-based diets. Environ Res 96:311–322

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Proctor CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998

    Article  CAS  PubMed  Google Scholar 

  • Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97:12356–12360

    Article  CAS  PubMed  Google Scholar 

  • Romheld V (1987) Different strategies for iron acquisition in higher plants. Physiol Plant 70:231–234

    Article  Google Scholar 

  • Rosenzweig AC (2002) Metallochaperones: bind and deliver. Chem Biol 9:673–677

    Article  CAS  PubMed  Google Scholar 

  • Rutherford JC, Cavet JS, Robinson NJ (1999) Cobalt-dependent transcriptional switching by a dual-effector MerR-like protein regulates a cobalt-exporting variant CPx-type ATPase. J Biol Chem 274:25827–25832

    Article  CAS  PubMed  Google Scholar 

  • Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587

    Article  CAS  PubMed  Google Scholar 

  • Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355

    Article  CAS  PubMed  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Schaaf G, Schikora A, Haberle J, Vert G, Ludewig U, Briat JF, Curie C, von Wiren N (2005) A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774

    Article  CAS  PubMed  Google Scholar 

  • Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wiren N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540

    Article  CAS  PubMed  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  CAS  PubMed  Google Scholar 

  • Segond D, Dellagi A, Lanquar V, Rigault M, Patrit O, Thomine S, Expert D (2009) NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J 58:195–207

    Article  CAS  PubMed  Google Scholar 

  • Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T, Müller-Moulé P, Munekaga Y, Niyogi KK, Pilon M (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346

    Article  CAS  PubMed  Google Scholar 

  • Simmons RW, Pongsakul P, Chaney RL, Saiyasitpanich D, Slinphoklap S, Nobuntou W (2003) The relative exclusion of zinc and iron from rice grain in relation to rice grain cadmium as compared to soybean: implications for human health. Plant Soil 257:163–170

    Article  CAS  Google Scholar 

  • Spiller S, Terry N (1980) Limiting factors in photosynthesis: II. Iron stress diminishes photochemical capacity by reducing the number of photosynthetic units. Plant Physiol 65:121–125

    Article  CAS  PubMed  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  PubMed  Google Scholar 

  • Takahashi MT, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicoianamine aminotransferase genes. Nat Biotechnol 19:466–469

    Article  CAS  PubMed  Google Scholar 

  • Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420:337–340

    Article  CAS  PubMed  Google Scholar 

  • Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102:12276–12281

    Article  CAS  PubMed  Google Scholar 

  • Talke IN, Hanikenne M, Kramer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167

    Article  CAS  PubMed  Google Scholar 

  • Taylor KM, Nicholson RI (2003) The LZT proteins; the LIV-1 subfamily of zinc transporters. Biochim Biophys Acta 1611:16–30

    Article  CAS  PubMed  Google Scholar 

  • Terry N (1980) Limiting factors in photosynthesis: I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol 65:114–120

    Article  CAS  PubMed  Google Scholar 

  • Terry N, Abadia J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646

    Article  CAS  Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci USA 97:4991–4996

    Article  CAS  PubMed  Google Scholar 

  • Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Bygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    Article  CAS  PubMed  Google Scholar 

  • Tsukahara T, Ezaki T, Moriguchi J, Furuki K, Shimbo S, Matsuda-Inoguchi N, Ikeda M (2003) Rice as the most influential source of cadmium intake among general Japanese population. Sci Total Environ 305:41–51

    Article  CAS  PubMed  Google Scholar 

  • Valentine RA, Jackson KA, Christie GR, Mathers JC, Taylor PM, Ford D (2007) ZnT5 variant B is a bidirectional zinc transporter and mediates zinc uptake in human intestinal Caco-2 cells. J Biol Chem 282:14389–14393

    Article  CAS  PubMed  Google Scholar 

  • Varotto C, Maiwald D, Pesaresi P, Jahns P, Francesco S, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589–599

    Article  CAS  PubMed  Google Scholar 

  • Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  CAS  PubMed  Google Scholar 

  • Verret F, Gravot A, Auroy P, Preveral S, Forestier C, Vavasseur A, Richaud P (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett 579:1515–1522

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and plant growth. Plant Cell 14:1223–1233

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Barberon M, Zelazny E, Seguela M, Briat J-F, Curie C (2009) Arabidopsis IRT2 cooperates with the high affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229:1171–1179

    Article  CAS  PubMed  Google Scholar 

  • von Wirén N, Mori S, Marschner H, Römheld V (1994) Iron inefficiency in maize mutant ys1 (Zea mays L. cv yellow-stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol 106:71–77

    Google Scholar 

  • Waldron KJ, Robinson NJ (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 6:25–35

    Article  CAS  Google Scholar 

  • Wang F, Kim BE, Petris MJ, Eide DJ (2004a) The mammalian ZIP5 protein is a zinc transporter that localizes to the basolateral surface of polarized cells. J Biol Chem 279:1433–1441

    Google Scholar 

  • Wang F, Dufner-Beattie J, Kim B-E, Petris MJ, Andrews G, Eide DJ (2004b) Zinc-stimulated endocytosis controls activity of the mouse ZIP1 and ZIP3 zinc uptake transporters. J Biol Chem 279:24631–24639

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Kim B-E, Dufner-Beattie J, Petris MJ, Andrews G, Eide DJ (2004c) Acrodermatitis enteropathica mutations affect transport activity, localization and zinc-responsive trafficking of the mouse ZIP4 zinc transporter. Hum Mol Genet 13:563–571

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Walker EL (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458

    Article  CAS  PubMed  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Mills RF (2005) P(1B)-ATPases – an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126

    Article  CAS  PubMed  Google Scholar 

  • Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653

    Article  CAS  PubMed  Google Scholar 

  • Woeste KE, Kieber JJ (2000) A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455

    CAS  PubMed  Google Scholar 

  • Wong CKE, Cobbett CS (2008) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78

    Article  CAS  Google Scholar 

  • Yuan DS, Stearman R, Dancis A, Dunn T, Beeler T, Klausner RD (1995) The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc Natl Acad Sci USA 92:2632–2636

    Article  CAS  PubMed  Google Scholar 

  • Yuan DS, Dancis A, Klausner RD (1997) Restriction of copper export in Saccharomyces cerevisiae to a late Golgi or post-Golgi compartment in the secretory pathway. J Biol Chem 272:25787–25793

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996a) The yeast ZRT1 gene encodes the zinc transporter of a high affinity uptake system induced by zinc limitation. Proc Natl Acad Sci USA 93:2454–2458

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996b) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271:23203–23210

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work in the Guerinot lab is supported by grants from NSF, DOE, NIGMS, and NIEHS. Aaron Atkinson was partially supported by a Graduate Assistance in Areas of National Need fellowship.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

    Aaron Atkinson & Mary Lou Guerinot

Authors
  1. Aaron Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mary Lou Guerinot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mary Lou Guerinot .

Editor information

Editors and Affiliations

  1. Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Angus S. Murphy

  2. Department of Horticulture, Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Burkhard Schulz

  3. Department of Horticulture, Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Wendy Peer

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Atkinson, A., Guerinot, M.L. (2011). Metal Transport. In: Murphy, A., Schulz, B., Peer, W. (eds) The Plant Plasma Membrane. Plant Cell Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13431-9_14

Download citation

Publish with us

Policies and ethics

Search

Navigation