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

Nature Chemical Biology

Volumn 5, Issue 5, 2009, Pages 333-340

  Palmer, Christine M ^a   Guerinot, Mary Lou ^a  

^a Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; IRON; LEWIS ACID; ZINC; CHELATING AGENT;

CELL TRANSPORT; CELL VACUOLE; CONCENTRATION (PARAMETERS); ENERGY YIELD; FOOD INDUSTRY; HOMEOSTASIS; INTRACELLULAR TRANSPORT; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; PHYTOTOXICITY; PLANT DEVELOPMENT; PLANT GROWTH; PLANT ROOT; PLANT SEED; PLANT TISSUE; PRIORITY JOURNAL; REDUCTION; REVIEW; SOIL ACIDIFICATION; TRANSPORT KINETICS; CHEMISTRY; METABOLISM; PLANT; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CHELATING AGENTS; COPPER; HOMEOSTASIS; IRON; PLANTS; ZINC;

EID: 65149090846     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.166     Document Type: Review

References (99)

1. Marschner, H. Mineral Nutrition of Higher Plants (Academic Press, Boston, 1995).
2. Balk, J. & Lobreaux, S. Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324-331 (2005).
3. Lim, N.C., Freake, H.C. & Bruckner, C. Illuminating zinc in biological systems. Chem. Eur. J. 11, 38-49 (2005).
4. Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I. & Lux, A. Zinc in plants. New Phytol. 173, 677-702 (2007).
5. Ciftci-Yilmaz, S. & Mittler, R. The zinc finger network of plants. Cell. Mol. Life Sci. 65, 1150-1160(2008).
6. Palmgren, M.G. et al. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13, 464-473 (2008).
7. Guerinot, M.L. & Yi, Y. Iron: nutritious, noxious, and not readily available. Plant Physiol. 104, 815-820 (1994).
8. Palmgren, M.G. PLANT PLASMA MEMBRANE H+-ATPases: powerhouses for nutrient uptake. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 817-845 (2001).
9. Dinneny, J.R. et al. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942-945 (2008).
10. Puig, S., Andres-Colas, N., Garcia-Molina, A. & Penarrubia, L. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and bio-technological applications. Plant Cell Environ. 30, 271-290 (2007).
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).
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).
13. Haydon, M.J. & Cobbett, C.S. Transporters of ligands for essential metal ions in plants. New Phytol. 174, 499-506 (2007).
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).
15. Suzuki, M. et al. Biosynthesis and secretion of mugineic acid family phytosidero-phores in zinc-deficient barley. Plant J. 48, 85-97 (2006).
16. Suzuki, M. et al. Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol. Biol. 66, 609-617 (2008).
17. Kim, S.A. & Guerinot, M.L. Mining iron: iron uptake and transport in plants. FEBS Lett. 581, 2273-2280(2007).
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).
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).
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).
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).
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).
23. Kerkeb, L. et al. Iron-induced turnover of the Arabidopsis IRT1 metal transporter requires lysine residues. Plant Physiol. 146, 1964-1973 (2008).
24. 2+. Plant J. 45, 335-346 (2006).
25. Cheng, L. et al. Mutation in nicotianamine aminotransferase stimulated the Fe(11) acquisition system and led to iron accumulation in rice. Plant Physiol. 145, 1647-1657 (2007).
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).
27. Sancenón, V. et al. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J. Biol. Chem. 279, 15348-15355 (2004).
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).
29. Curie, C. et al. Maize yellow stripel encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346-349 (2001).
30. Schaaf, G. et al. ZmYS1 functions as a proton-coupled symporter for phytosi-derophore- and nicotianamine-chelated metals. J. Biol. Chem. 279, 9091-9096 (2004).
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).
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).
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).
34. Green, L.S. & Rogers, E.E. FRD3 controls iron localization in Arabidopsis thaliana. Plant Physiol. 136, 2523-2531 (2004).
35. Yokosho, K., Yamaji, N., Ueno, D., Mitani, N. & Ma, J.F. OsFRDLl is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol. 149, 297-305 (2009).
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).
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).
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 Zl P transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269-281 (2004).
39. Hanikenne, M. et al. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391-395 (2008).
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).
41. Kraemer, U. The dilemma of controlling heavy metal accumulation in plants. New Phytol. 181, 3-5(2009).
42. Krämer, U., Talke, I.N. & Hanikenne, M. Transition metal transport. FEBS Lett. 581, 2263-2272 (2007).
43. Andrés-Colás, N. et al. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metal lochaperones and functions in copper detoxification of roots. Plant J. 45, 225-236 (2006).
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).
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).
46. Waters, B.M. etal. 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).
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).
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).
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).
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).
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).
52. Myouga, F. et al. A heterocomplex of iron superoxide dismutases defends chloro-plast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20, 3148-3162 (2008).
53. Cohu, C.M. & Pilon, M. Regulation of superoxide dismutase expression by copper availability. Physiol. Plant. 129, 747-755 (2007).
54. Yamasaki, H. et al. Regulation of copper homeostasis by micro-RNA in Arabidopsis. J. Biol. Chem. 282, 16369-16378 (2007).
55. Abdel-Ghany, S.E. & Pilon, M. Micro RNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J. Biol. Chem. 283, 15932-15945 (2008).
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).
57. Eriksson, M. et al. Genetic dissection of nutritional copper signaling in Chlamydomonas distinguishes regulatory and target genes. Genetics 168, 795-807 (2004).
58. Duy, D. et al. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19, 986-1006 (2007).
59. Teng, Y.S. et al. Tic21 is an essential translocon component for protein transloca-tion across the chloroplast inner envelope membrane. Plant Cell 18, 2247-2257 (2006).
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).
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).
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).
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).
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).
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).
66. Moreno, I. et al. AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J. Biol. Chem. 283, 9633-9641 (2008).
67. Kushnir, S. et al. A mutation of the mitochondrial ABC transporter Stal leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13, 89-100 (2001).
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).
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).
70. Kim, S.A. et al. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295-1298(2006).
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).
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).
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).
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).
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).
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).
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).
78. Halliwell, B. & Gutteridge, J.M.C. Biologically relevant metal ion-dependent hydroxyl radical generation. FEBS Lett. 307, 108-112 (1992).
79. Hintze, K.J. & Theil, E.C. Cellular regulation and molecular interactions of the ferritins. Cell. Mol. Life Sci. 63, 591-600 (2006).
80. Ravet, K. et al. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J. 57, 400-412 (2009).
81. Carrondo, M.A. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22, 1959-1968 (2003).
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).
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).
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).
85. Marchetti, A. et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457, 467-470 (2009).
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).
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).
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).
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).
90. Clemens, S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochim. 88, 1707-1719 (2006).
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).
92. Salt, D.E., Baxter, I. & Lahner, B. lonomics and the study of the plant ionome. Annu. Rev. Plant Biol. 59, 709-733 (2008).
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).
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).
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).
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).
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).
98. Tottey, S. et al. Protein-folding location can regulate manganese-binding versus copper-or zinc-binding. Nature 455, 1138-1142 (2008).
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).