heavy metal transport; hyperaccumulation; deficiency; metal homeostasis; evolution
Abstract :
[en] Transition metal transporters are of central importance in the plant metal homeostasis network which maintains internal metal concentrations within physiological limits. An overview is given of the functions of known transition metal transporters in the context of the unique chemical properties of their substrates. The modifications of the metal homeostasis network associated with the adaptation to an extreme metalliferous environment are illustrated in two Brassicaceae metal hyperaccumulator model plants based on cross-species transcriptomics studies. In a comparison between higher plants and unicellular algae, hypotheses are generated for evolutionary changes in metal transporter complements associated with the transition to multicellularity. (c) 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.
Merchant S., and Dreyfuss B.W. Posttranslational assembly of photosynthetic metalloproteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998) 25-51
Krämer, U. and Clemens, S. (2005) in: Molecular Biology of Metal Homeostasis and Detoxification, Topics in Current Genetics, Vol. 14, pp. 216-271 (Tamás, M. and Martinoia, E. Eds.).
Clemens S., Palmgren M.G., and Krämer U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7 (2002) 309-315
Hussain D., et al. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 (2004) 1327-1339
Lanquar V., et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24 (2005) 4041-4051
Abdel-Ghany S.E., Muller-Moule P., Niyogi K.K., Pilon M., and Shikanai T. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17 (2005) 1233-1251
Huang C., Barker S.J., Langridge P., Smith F.W., and Graham R.D. Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol. 124 (2000) 415-422
Sancenon V., Puig S., Mateu-Andres I., Dorcey E., Thiele D.J., and Penarrubia L. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J. Biol. Chem. 279 (2004) 15348-15355
Finney L.A., and O'Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300 (2003) 931-936
Lee M., Lee K., Lee J., Noh E.W., and Lee Y. AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol. 138 (2005) 827-836
Rogers E.E., and Guerinot M.L. FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14 (2002) 1787-1799
Green L.S., and Rogers E.E. FRD3 controls iron localization in Arabidopsis. Plant Physiol. 136 (2004) 2523-2531
Haydon M.J., and Cobbett C.S. A novel major facilitator superfamily protein at the tonoplast influences Zn tolerance and accumulation in Arabidopsis. Plant Physiol. 143 (2007) 1705-1719
Grotz N., and Guerinot M.L. Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochim. Biophys. Acta 1763 (2006) 595-608
Colangelo E.P., and Guerinot M.L. Put the metal to the petal: metal uptake and transport throughout plants. Curr. Opin. Plant Biol. 9 (2006) 322-330
Puig S., Andres-Colas N., Garcia-Molina A., and Penarrubia L. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ. 30 (2007) 271-290
Williams L.E., and Mills R.F. P(1B)-ATPases - an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 10 (2005) 491-502
Clemens S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88 (2006) 1707-1719
Krämer U. MTP1 mops up excess zinc in Arabidopsis cells. Trends Plant Sci. 10 (2005) 313-315
Pittman J.K. Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol. 167 (2005) 733-742
Hanikenne M., Krämer U., Demoulin V., and Baurain D. A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschyzon merolae. Plant Physiol. 137 (2005) 428-446
Cohen C.K., Garvin D.F., and Kochian L.V. Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 218 (2004) 784-792
Fraústo da Silva J.J.R., and Williams R.J.P. The Biological Chemistry of the Elements (2001), Clarendon Press, Oxford, UK
Changela A., Chen K., Xue Y., Holschen J., Outten C.E., O'Halloran T.V., and Mondragon A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301 (2003) 1383-1387
Outten C.E., and O'Halloran T.V. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292 (2001) 2488-2492
O'Halloran T.V., and Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275 (2000) 25057-25060
Puig S., et al. Higher plants possess two different types of ATX1-like copper chaperones. Biochem. Biophys. Res. Commun. 354 (2007) 385-390
Andres-Colas N., Sancenon V., Rodriguez-Navarro S., Mayo S., Thiele D.J., Ecker J.R., Puig S., and Penarrubia L. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J. 45 (2006) 225-236
Grotz N., Fox T., Connolly E., Park W., Guerinot M.L., and Eide D. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc. Natl. Acad. Sci. USA 95 (1998) 7220-7224
Schaaf G., Ludewig U., Erenoglu B.E., Mori S., Kitahara T., and von Wiren N. ZmYSl functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. 279 (2004) 9091-9096
Schaaf G., Schikora A., Haberle J., Vert G., Ludewig U., Briat J.F., Curie C., and von Wiren N. A putative function for the arabidopsis Fe-Phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol. 46 (2005) 762-774
Eren E., and Arguello J.M. Arabidopsis HMA2, a divalent heavy metal-transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol. 136 (2004) 3712-3723
Wintz H., Fox T., Wu Y.Y., Feng V., Chen W., Chang H.S., Zhu T., and Vulpe C. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278 (2003) 47644-47653
Korshunova Y.O., Eide D., Clark W.G., Guerinot M.L., and Pakrasi H.B. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40 (1999) 37-44
Arrivault S., Senger T., and Krämer U. 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 (2006) 861-879
Blaudez D., Kohler A., Martin F., Sanders D., and Chalot M. Poplar metal tolerance protein 1 (MTP1) confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15 (2003) 2911-2928
Kobae Y., Uemura T., Sato M.H., Ohnishi M., Mimura T., Nakagawa T., and Maeshima M. Zinc transporter of Arabidopsis thaliana AtMTPl is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 45 (2004) 1749-1758
Desbrosses-Fonrouge A.G., Voigt K., Schröder A., Arrivault S., Thomine S., and Krämer U. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett. 579 (2005) 4165-4174
Delhaize E., Kataoka T., Hebb D.M., White R.G., and Ryan P.R. Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15 (2003) 1131-1142
Gravot A., Lieutaud A., Verret F., Auroy P., Vavasseur A., and Richaud P. AtHMA3, a plant PIB-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett. 561 (2004) 22-28
Kim S.A., Punshon T., Lanzirotti A., Li L., Alonso J.M., Ecker J.R., Kaplan J., and Guerinot M.L. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314 (2006) 1295-1298
Thomine S., Lelievre F., Debarbieux E., Schroeder J.I., and Barbier-Brygoo H. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34 (2003) 685-695
Reeves R.D., and Baker A.J.M. In: Raskin I., and Ensley B.D. (Eds). Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment (2000), Wiley, Hoboken, NJ 193-230
Talke I.N., Hanikenne M., and Krämer U. 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 (2006) 148-167
Becher M., Talke I.N., Krall L., and Krämer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37 (2004) 251-268
van de Mortel J.E., et al. Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. 142 (2006) 1127-1147
Weber M., Harada E., Vess C., von Roepenack-Lahaye E., and Clemens S. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37 (2004) 269-281
Filatov V., Dowdle J., Smirnoff N., Ford-Lloyd B., Newbury H.J., and Macnair M.R. Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol. Ecol. 15 (2006) 3045-3059
Hammond J.P., et al. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol. 170 (2006) 239-260
Chiang H.C., Lo J.C., and Yeh K.C. Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ. Sci. Technol. 40 (2006) 6792-6798
Pence N.S., Larsen P.B., Ebbs S.D., Letham D.L., Lasat M.M., Garvin D.F., Eide D., and Kochian L.V. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 97 (2000) 4956-4960
Lasat M.M., Pence N.S., Garvin D.F., Ebbs S.D., and Kochian L.V. Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J. Exp. Bot. 51 (2000) 71-79
Assunção A.G.L., Da Costa Martins P., De Folter S., Vooijs R., Schat H., and Aarts M.G.M. Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 24 (2001) 217-226
Dräger D.B., Desbrosses-Fonrouge A.G., Krach C., Chardonnens A.N., Meyer R.C., Saumitou-Laprade P., and Krämer U. Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. 39 (2004) 425-439
Baker A.J.M., Reeves R.D., and Hajar A.S.M. Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brasicaceae). New Phytol. 127 (1994) 61-68
Papoyan A., and Kochian L.V. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 136 (2004) 3814-3823
Bernard C., Roosens N., Czernic P., Lebrun M., and Verbruggen N. A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett. 569 (2004) 140-148
Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., Vavasseur A., and Richaud P. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 576 (2004) 306-312
Mills R.F., Francini A., Ferreira da Rocha P.S., Baccarini P.J., Aylett M., Krijger G.C., and Williams L.E. 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 (2005) 783-791
Curie C., Alonso J.M., Le Jean M., Ecker J.R., and Briat J.F. Involvement of NRAMPl from Arabidopsis thaliana in iron transport. Biochem. J. 347 Pt 3 (2000) 749-755
Durrett, T.P., Gassmann, W. and Rogers, E.E. (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. doi:10.1104/pp.107.097162.
Lasat M.M., Baker A.J., and Kochian L.V. Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol. 118 (1998) 875-883
Callahan D.L., Baker A.J., Kolev S.D., and Wedd A.G. Metal ion ligands in hyperaccumulating plants. J. Biol. Inorg. Chem. 11 (2006) 2-12
Mari S., Gendre D., Pianelli K., Ouerdane L., Lobinski R., Briat J.F., Lebrun M., and Czernic P. Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J. Exp. Bot. 57 (2006) 4111-4122
Pianelli K., Mari S., Marques L., Lebrun M., and Czernic P. Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res. 14 (2005) 739-748
Gendre D., Czernic P., Conejero G., Pianelli K., Briat J.F., Lebrun M., and Mari S. TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J. 49 (2006) 1-15
McKie A.T., et al. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 5 (2000) 299-309
Schaaf G., Honsbein A., Meda A.R., Kirchner S., Wipf D., and von Wiren N. AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J. Biol. Chem. 281 (2006) 25532-25540
Waters B.M., Chu H.H., Didonato R.J., Roberts L.A., Eisley R.B., Lahner B., Salt D.E., and Walker E.L. 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 (2006) 1446-1458
Le Jean M., Schikora A., Mari S., Briat J.F., and Curie C. A loss-of-function mutation in AtYSLl reveals its role in iron and nicotianamine seed loading. Plant J. 44 (2005) 769-782
Trampczynska A., Bottcher C., and Clemens S. The transition metal chelator nicotianamine is synthesized by filamentous fungi. FEBS Lett. 580 (2006) 3173-3178
Kiranmayi P., and Mohan P.M. Metal transportome of Neurospora crassa. In Silico Biol. 6 (2006) 169-180
La Fontaine S., Quinn J.M., Nakamoto S.S., Page M.D., Gohre V., Moseley J.L., Kropat J., and Merchant S. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot. Cell 1 (2002) 736-757
Paz Y., Katz A., and Pick U. A multicopper ferroxidase involved in iron binding to transferrins in Dunaliella salina plasma membranes. J. Biol. Chem. 282 (2007) 8658-8666
Bloß T., Clemens S., and Nies D.H. Characterization of the ZATlp zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta 214 (2002) 783-791
Grossoehme N.E., Akilesh S., Guerinot M.L., and Wilcox D.E. Metal-binding thermodynamics of the histidine-rich sequence from the metal-transport protein IRT1 of Arabidopsis thaliana. Inorg. Chem. 45 (2006) 8500-8508
Baxter I., Tchieu J., Sussman M.R., Boutry M., Palmgren M.G., Gribskov M., Harper J.F., and Axelsen K.B. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol. 132 (2003) 618-628
Sondergaard T.E., Schulz A., and Palmgren M.G. Energization of transport processes in plants, roles of the plasma membrane H+-ATPase. Plant Physiol. 136 (2004) 2475-2482
