Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Facing the challenges of Cu, Fe and Zn homeostasis in plants

Nature Chemical Biology volume 5, pages 333–340 (2009)Cite this article

Abstract

Plants have recently moved into the spotlight owing to the growing realization that the world needs solutions to energy and food production that are sustainable and environmentally sound. Iron, copper and zinc are essential for plant growth and development, yet the same properties that make these transition metals indispensable can also make them deadly in excess. Iron and copper are most often used for their redox properties, whereas zinc is primarily used for its ability to act as a Lewis acid. Here we review recent advances in the field of metal homeostasis and integrate the findings on uptake and transport of these three metals.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Intercellular metal transport in dicots.
Figure 2: Intercellular metal transport in monocots.
Figure 3: Intracellular metal transport.

Similar content being viewed by others

References

  1. Marschner, H. Mineral Nutrition of Higher Plants (Academic Press, Boston, 1995).

    Google Scholar 

  2. Balk, J. & Lobreaux, S. Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324–331 (2005).

    CAS  PubMed  Google Scholar 

  3. Lim, N.C., Freake, H.C. & Bruckner, C. Illuminating zinc in biological systems. Chem. Eur. J. 11, 38–49 (2005).

    Google Scholar 

  4. Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I. & Lux, A. Zinc in plants. New Phytol. 173, 677–702 (2007).

    CAS  PubMed  Google Scholar 

  5. Ciftci-Yilmaz, S. & Mittler, R. The zinc finger network of plants. Cell. Mol. Life Sci. 65, 1150–1160 (2008).

    CAS  PubMed  Google Scholar 

  6. Palmgren, M.G. et al. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13, 464–473 (2008).

    CAS  PubMed  Google Scholar 

  7. Guerinot, M.L. & Yi, Y. Iron: nutritious, noxious, and not readily available. Plant Physiol. 104, 815–820 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Palmgren, M.G. PLANT PLASMA MEMBRANE H+-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 817–845 (2001).

    CAS  PubMed  Google Scholar 

  9. Dinneny, J.R. et al. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942–945 (2008).

    CAS  PubMed  Google Scholar 

  10. Puig, S., Andres-Colas, N., Garcia-Molina, A. & Penarrubia, L. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ. 30, 271–290 (2007).

    CAS  PubMed  Google Scholar 

  11. Robinson, N.J., Procter, C.M., Connolly, E.L. & Guerinot, M.L. A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697 (1999).

    CAS  PubMed  Google Scholar 

  12. Connolly, E.L., Campbell, N.H., Grotz, N., Prichard, C.L. & Guerinot, M.L. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol. 133, 1102–1110 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Haydon, M.J. & Cobbett, C.S. Transporters of ligands for essential metal ions in plants. New Phytol. 174, 499–506 (2007).

    CAS  PubMed  Google Scholar 

  14. Nagasaka, S. et al. Time course analysis of gene expression over 24 hours in Fe-deficient barley roots. Plant Mol. Biol. 69, 621–631 (2009).

    CAS  PubMed  Google Scholar 

  15. Suzuki, M. et al. Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J. 48, 85–97 (2006).

    CAS  PubMed  Google Scholar 

  16. Suzuki, M. et al. Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol. Biol. 66, 609–617 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Kim, S.A. & Guerinot, M.L. Mining iron: iron uptake and transport in plants. FEBS Lett. 581, 2273–2280 (2007).

    CAS  PubMed  Google Scholar 

  18. 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. USA 93, 5624–5628 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Vert, G. et al. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and plant growth. Plant Cell 14, 1223–1233 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Varotto, C. et al. The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. 31, 589–599 (2002).

    CAS  PubMed  Google Scholar 

  21. Henriques, R. et al. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 50, 587–597 (2002).

    CAS  PubMed  Google Scholar 

  22. Connolly, E.L., Fett, J.P. & Guerinot, M.L. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14, 1347–1357 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Kerkeb, L. et al. Iron-induced turnover of the Arabidopsis IRT1 metal transporter requires lysine residues. Plant Physiol. 146, 1964–1973 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Ishimaru, Y. et al. Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 45, 335–346 (2006).

    CAS  PubMed  Google Scholar 

  25. Cheng, L. et al. Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol. 145, 1647–1657 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Korshunova, Y.O., Eide, D., Clark, W.G., Guerinot, M.L. & Pakrasi, H.B. The IRT1 protein from Arabidopsis thaliana is a metal transporter with broad specificity. Plant Mol. Biol. 40, 37–44 (1999).

    CAS  PubMed  Google Scholar 

  27. Sancenón, V. et al. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J. Biol. Chem. 279, 15348–15355 (2004).

    PubMed  Google Scholar 

  28. Wintz, H. et al. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278, 47644–47653 (2003).

    CAS  PubMed  Google Scholar 

  29. Curie, C. et al. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346–349 (2001).

    CAS  PubMed  Google Scholar 

  30. Schaaf, G. et al. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. 279, 9091–9096 (2004).

    CAS  PubMed  Google Scholar 

  31. Inoue, H. et al. 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 (2009).

    CAS  PubMed  Google Scholar 

  32. Curie, C. et al. Metal movement within the plant: contribution of nictotianamine and yellow stripe 1-like transporters. Ann. Bot. (Lond.) 103, 1–11 (2009).

    CAS  Google Scholar 

  33. Durrett, T.P., Gassmann, W. & Rogers, E.E. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 144, 197–205 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Green, L.S. & Rogers, E.E. FRD3 controls iron localization in Arabidopsis thaliana. Plant Physiol. 136, 2523–2531 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Yokosho, K., Yamaji, N., Ueno, D., Mitani, N. & Ma, J.F. OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol. 149, 297–305 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Hussain, D. et al. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16, 1327–1339 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Becher, M., Talke, I.N., Krall, L. & Kramer, 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, 251–268 (2004).

    CAS  PubMed  Google Scholar 

  38. Weber, M., Harada, E., Vess, C., Roepenack-Lahaye, E. & 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, 269–281 (2004).

    CAS  PubMed  Google Scholar 

  39. Hanikenne, M. et al. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391–395 (2008).

    CAS  PubMed  Google Scholar 

  40. Milner, M.J. & Kocian, L.V. Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann. Bot. (Lond.) 102, 3–13 (2008).

    CAS  Google Scholar 

  41. Kraemer, U. The dilemma of controlling heavy metal accumulation in plants. New Phytol. 181, 3–5 (2009).

    CAS  PubMed  Google Scholar 

  42. Krämer, U., Talke, I.N. & Hanikenne, M. Transition metal transport. FEBS Lett. 581, 2263–2272 (2007).

    PubMed  Google Scholar 

  43. Andrés-Colás, N. et al. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J. 45, 225–236 (2006).

    PubMed  Google Scholar 

  44. Kobayashi, Y. et al. 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 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  46. Waters, B.M. et al. 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 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  48. Schaaf, G. et al. A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol. 46, 762–774 (2005).

    CAS  PubMed  Google Scholar 

  49. Koike, S. et al. OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39, 415–424 (2004).

    CAS  PubMed  Google Scholar 

  50. Stacey, M.G. et al. The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol. 146, 589–601 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Alscher, R.G., Erturk, N. & Heath, L.S. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53, 1331–1341 (2002).

    CAS  PubMed  Google Scholar 

  52. Myouga, F. et al. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20, 3148–3162 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Cohu, C.M. & Pilon, M. Regulation of superoxide dismutase expression by copper availability. Physiol. Plant. 129, 747–755 (2007).

    CAS  Google Scholar 

  54. Yamasaki, H. et al. Regulation of copper homeostasis by micro-RNA in Arabidopsis. J. Biol. Chem. 282, 16369–16378 (2007).

    CAS  PubMed  Google Scholar 

  55. Abdel-Ghany, S.E. & Pilon, M. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J. Biol. Chem. 283, 15932–15945 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Yamasaki, H., Hayashi, M., Fukazawa, M., Kobayashi, Y. & Shikanai, T. SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21, 347–361 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Eriksson, M. et al. Genetic dissection of nutritional copper signaling in Chlamydomonas distinguishes regulatory and target genes. Genetics 168, 795–807 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Duy, D. et al. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19, 986–1006 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Teng, Y.S. et al. Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 18, 2247–2257 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Jeong, J. et al. Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc. Natl. Acad. Sci. USA 105, 10619–10624 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Heazlewood, J.L. et al. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241–256 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Mukherjee, I., Campbell, N.H., Ash, J.S. & Connolly, E.L. Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223, 1178–1190 (2006).

    CAS  PubMed  Google Scholar 

  63. Abdel-Ghany, S.E., Muller-Moule, P., Niyogi, K.K., Pilon, M. & Shikanai, T. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17, 1233–1251 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Seigneurin-Berny, D. et al. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J. Biol. Chem. 281, 2882–2892 (2006).

    CAS  PubMed  Google Scholar 

  66. Moreno, I. et al. AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J. Biol. Chem. 283, 9633–9641 (2008).

    CAS  PubMed  Google Scholar 

  67. Kushnir, S. et al. A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13, 89–100 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Chen, S., Sanchez-Fernandez, R., Lyver, E.R., Dancis, A. & Rea, P.A. Functional characterization of AtATM1, AtATM2 and AtATM3, a subfamily of Arabidopsis half-molecule ABC transporters implicated in iron homeostasis. J. Biol. Chem. 282, 21561–21571 (2007).

    CAS  PubMed  Google Scholar 

  69. Maxfield, A.B., Heaton, D.N. & Winge, D.R. Cox17 is functional when tethered to the mitochondrial inner membrane. J. Biol. Chem. 279, 5072–5080 (2004).

    CAS  PubMed  Google Scholar 

  70. Kim, S.A. et al. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295–1298 (2006).

    CAS  PubMed  Google Scholar 

  71. Lanquar, V. et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041–4051 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  73. Desbrosses-Fonrouge, A.G. et al. 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 (2005).

    CAS  PubMed  Google Scholar 

  74. Arrivault, S., Senger, T. & Kramer, 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, 861–879 (2006).

    CAS  PubMed  Google Scholar 

  75. Kobae, Y. et al. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 45, 1749–1758 (2004).

    CAS  PubMed  Google Scholar 

  76. Gustin, J.L. et al. MTP1-dependent Zn sequestration into shoot vacuoles suggest dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J. 57, 1116–1127 (2009).

    CAS  PubMed  Google Scholar 

  77. Whiteman, S.-A., Nühse, T.S., Ashford, D.A., Sanders, D. & Maathuis, F.J.M. A proteomic and phosphoproteomic analysis of Oryza sativa plasma membrane and vacuolar membrane. Plant J. 56, 146–156 (2008).

    CAS  PubMed  Google Scholar 

  78. Halliwell, B. & Gutteridge, J.M.C. Biologically relevant metal ion-dependent hydroxyl radical generation. FEBS Lett. 307, 108–112 (1992).

    CAS  PubMed  Google Scholar 

  79. Hintze, K.J. & Theil, E.C. Cellular regulation and molecular interactions of the ferritins. Cell. Mol. Life Sci. 63, 591–600 (2006).

    CAS  PubMed  Google Scholar 

  80. Ravet, K. et al. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J. 57, 400–412 (2009).

    CAS  PubMed  Google Scholar 

  81. Carrondo, M.A. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22, 1959–1968 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Busch, A., Rimbauld, B., Naumann, B., Rensch, S. & Hippler, M. Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo-oxidative stress in response to iron availability in Chlamydomonas reinhardtii. Plant J. 55, 201–211 (2008).

    CAS  PubMed  Google Scholar 

  83. Long, J.C., Sommer, F., Allen, M.D., Lu, S.F. & Merchant, S.S. FER1 and FER2 encoding two ferritin complexes in Chlamydomonas reinhardtii chloroplasts are regulated by iron. Genetics 179, 137–147 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Petit, J.M., Briat, J.-F. & Lobréaux, S. Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem. J. 359, 575–582 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Marchetti, A. et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457, 467–470 (2009).

    CAS  PubMed  Google Scholar 

  86. Shi, H., Bencze, K.Z., Stemmler, T.L. & Philpott, C.C. A cytosolic iron chaperone that delivers iron to ferritin. Science 320, 1207–1210 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Mira, H., Martínez-García, F. & Peñarrubia, L. Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. Plant J. 25, 521–528 (2001).

    CAS  PubMed  Google Scholar 

  88. Abdel-Ghany, S.E. et al. AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett. 579, 2307–2312 (2005).

    CAS  PubMed  Google Scholar 

  89. Attallah, C.V., Welchen, E., Pujol, C., Bonnard, G. & Gonzalez, D.H. Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol. Biol. 65, 343–355 (2007).

    CAS  PubMed  Google Scholar 

  90. Clemens, S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochim. 88, 1707–1719 (2006).

    CAS  Google Scholar 

  91. Guo, W.-J., Meetam, M. & Goldsbrough, P.B. Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol. 146, 1697–1706 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Salt, D.E., Baxter, I. & Lahner, B. Ionomics and the study of the plant ionome. Annu. Rev. Plant Biol. 59, 709–733 (2008).

    CAS  PubMed  Google Scholar 

  93. Ishimaru, Y. et al. Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc. Natl. Acad. Sci. USA 104, 7373–7378 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Punshon, T., Guerinot, M.L. & Lanzirotti, A. Using synchrotron x-ray fluorescence microprobes to study metal(loid) homeostasis in plants. Ann. Bot. (Lond.) 103, 665–672 (2009).

    CAS  Google Scholar 

  95. Domaille, D.W., Que, E.L. & Chang, C.J. Synthetic fluorescent sensors for studying the cell biology of metals. Nat. Chem. Biol. 4, 168–175 (2008).

    CAS  PubMed  Google Scholar 

  96. Sinclair, S.A., Sherson, S.M., Jarvis, R., Camakaris, J. & Cobbett, C.S. The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol. 174, 39–45 (2007).

    CAS  PubMed  Google Scholar 

  97. Walker, E.L. & Connolly, E.L. Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Curr. Opin. Plant Biol. 11, 530–535 (2008).

    CAS  PubMed  Google Scholar 

  98. Tottey, S. et al. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455, 1138–1142 (2008).

    CAS  PubMed  Google Scholar 

  99. Waldron, K.J. & Robinson, N.J. How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 6, 25–35 (2009).

    Google Scholar 

  100. Pais, I. & Jones, J.B. The Handbook of Trace Elements (St. Lucie Press, Boca Raton, Florida, USA, 1997).

    Google Scholar 

Download references

Acknowledgements

We thank members of the Guerinot laboratory for helpful discussions; we also thank the many laboratories, both cited and not cited in this review due to space limitations, who have contributed to this field of investigation. C.P. is supported by a training grant from the US National Institute of General Medical Sciences (T32GM008704). Work in our laboratory is supported by grants from the US National Science Foundation (IBN-0344305; IBN-0419695; DBI-0606193), the US National Institutes of Health (RO1 GM 078536), the US Department of Energy (DE-FG-2-06ER15809) and the US National Institute of Environmental Health Sciences (5 P42 ES007373).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire, USA

    Christine M Palmer & Mary Lou Guerinot

Authors
  1. Christine M Palmer
    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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palmer, C., Guerinot, M. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5, 333–340 (2009). https://doi.org/10.1038/nchembio.166

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchembio.166

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing