Iron uptake, trafficking and homeostasis in plants

Planta

Volumn 216, Issue 4, 2003, Pages 541-551

  Hell, Rüdiger ^a   Stephan, Udo W ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Iron sulfur cluster; Malnutrition; Micronutrients; Phloem; Transport

Indexed keywords

CELLS; CHELATION; IRON COMPOUNDS; METABOLISM; PH EFFECTS; SOIL MECHANICS; TOXIC MATERIALS;

HOMEOSTASIS;

PLANTS (BOTANY);

IRON;

CHEMICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; PHYSIOLOGY; PLANT; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; IRON; MODELS, CHEMICAL; PLANT SHOOTS; PLANTS;

EID: 0038047698     PISSN: 00320935     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00425-002-0920-4     Document Type: Review

References (101)

1. Albury MS, Affourtit C, Crichton PG, Moore AL (2002) Structure of the plant alternative oxidase. Site-directed mutagenesis provides new information on the active site and membrane topology. J Biol Chem 277:1190-1194
2. Becker R, Fritz E, Manteuffel R (1995) Subcellular localization and characterization of excessive iron in the nicotianamine-less tomato mutant chloronerva. Plant Physiol 1995:269-275
3. Bienfait HF (1988) Proteins under the control of the gene for Fe efficiency in tomato. Plant Physiol 88:785-787
4. Bienfait HF, Scheffers MR (1992) Some properties of ferric citrate relevant to the iron nutrition of plants. Plant Soil 143:141-144
5. Bienfait HF, van den Briel W, Mesland-Mul NT (1985) Free space iron pools in roots. Generation and mobilization. Plant Physiol 78:596-600
6. Böhme H, Scholz G (1960) Versuche zur Normalisierung des Phänotyps der Mutante chloronerva von Lycopersicon esculenturn Mill.. Kulturpflanze 8:93-109
7. Briat JF (2002) Metal ion-activated oxidative stress and its control. In: Inzé D, Van Montagu M (eds) Oxidative stress in plants. Taylor & Francis, London, pp 171-190
8. Briat JF, Lobréaux S, Grignon N, Vansuyt G (1999) Regulation of plant ferritin synthesis: how and why. Cell Mol Life Sci 56:155-166
9. Bughio N, Takahashi M, Yoshimura E, Nishizawa N K, Mori S (1997) Light-dependent iron transport into isolated barley chloroplasts. Plant Cell Physiol 38:101-105
10. Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475-486
11. Cohen CK, Fox TC, Garvin D F, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy metal transport in plants. Plant Physiol 116:1063-1072
12. Connolly, EL, Fett, JP, Guerinot, ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347-1357
13. Curie C, Alonso J, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749-755
14. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripel encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346-349
15. Deák M, Horvath GV, Davletova S, Torok K, Sass L, Vass I, Barna B, Kiraly Z, Dudits D (1999) Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat Biotechnol 17:192-196
16. Douchkov D, Hell R, Stephan UW, Bäumlein H (2001) Increased iron efficiency in transgenic plants due to ectopic expression of nicotianamine synthase. In: Horst WJ, Schenk MK, Bürkert A, Claassen N, Flessa H, Frommer WB, Goldbach H, Olfs H, Römheld V, Sattelmacher B, Schmidhalter U, Schubert S, v Wirén N, Wittenmayer L (eds) Plant nutrition. Food security and sustainability of agro-ecosystems through basic and applied research. Kluwer, Dordrecht, pp 54-55
17. Eckhardt U, Mas Marques A, Buckhout TJ (2001) Two-iron regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol Biol 45:437-448
18. Edding JL, Brown AL (1967) Absorption and translocation of foliar-applied iron. Plant Physiol 42:15-19
19. 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
20. Fox TC, Guerinot ML (1998) Molecular biology of cation transport in plants. Annu Rev Plant Physiol Plant Mol Biol 49:669-696
21. + release into the xylem sap. Cell 94:647-655
22. Giritch A, Herbik A, Balzer HJ, Ganal M, Stephan UW, Bäumlein H (1997) A root-specific iron-regulated gene of tomato encodes a lysyl-tRNA-synthetase-like protein. Eur J Biochem 244:310-317
23. Giritch A, Ganal M, Stephan UW, Bäumlein H (1998) Structure, expression and chromosomal localisation of the metallothionein-like gene family of tomato. Plant Mol Biol 37:701-714
24. Goto F, Yoshihara T, Saiki H (1998) Iron accumulation in tobacco plants expressing soyabean ferritin gene. Transgenic Res 7:173-180
25. Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17:282-286
26. Gregorio GB (2002) Progress in breeding for trace minerals in staple crops. J Nutr 132:500-502
27. Grusak MA (1994) Iron transport to developing ovules of Pisum sativum: I. Seed import characteristics and phloem iron-loading capacity of source regions. Plant Physiol 104:649-655
28. Grusak MA, DellaPenna D (1999) Improving the nutrient composition of plants to enhance human nutrition and health. Annu Rev Plant Physiol Plant Mol Biol 50:133-161
29. Grusak MA, Pezeshgi S (1996) Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol 110:329-334
30. Guerinot ML (2001) Improving rice yields - ironing out the details. Nat Biotechnol 19:417-418
31. Helder RJ, Boerma J (1969) An electron-microscopical study of the plasmodesmata in the roots of young barley seedlings. Acta Bot Neerl 18:99-107
32. Herbik A, Giritch A, Horstmann C, Becker R, Balzer HJ, Bäumlein H, Stephan UW (1996) Iron and copper nutrition-dependent changes in protein expression in a tomato wild type and the nicotianamine-free mutant chloronerva. Plant Physiol 111:533-540
33. Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, Stephan UW, Bäumlein H (1999) Isolation, characterization and cDNA cloning of nicotianamine synthase from barley. A key enzyme for iron homeostasis in plants. Eur J Biochem 265:231-239
34. Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471-480
35. Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa N K, Mori S (2001) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J 25:159-167
36. King JC (2002a) Evaluating the impact of plant biofortification on human nutrition. J Nutr. 132:511-513
37. King JC (2002b) Biotechnology: a solution for improving nutrient bioavailability. Int J Vitam Nutr Res 72:7-12
38. Kobayashi T, Nakanishi H, Takahashi M, Kawasaki S, Nishizawa N K, Mori S (2001) In vivo evidence that Ids3 from Hordeum vulgate encodes a dioxygenase that converts 2′-deoxymugineic acid to mugineic acid in transgenic rice. Planta 212:864-871
39. Köhler B, Wegner LH, Osipov V, Raschke K (2002) Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X-QUAC, the main anion conductance in xylem-parenchyma cells of barley roots. Plant J 30:133-142
40. Kopriva S, Buchert T, Fritz G, Suter M, Benda R, Schünemann V, Koprivova A, Schürmann P, Trautwein AX, Kroneck PM, and Brunold C (2002) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation. J Biol Chem 277:21786-21791
41. 3+ reduction in intact sunflower leaves. Plant Physiol 23:1069-1079
42. Krüger C, Berkowitz O, Stephan UW, Hell R (2002) A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. J Biol Chem 277:25062-25069
43. Kushnir S, Babiychuk E, Storozhenko S, Davey M, Papenbrock J, De Rycke R R, Engler G, Stephan U, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89-100
44. Landsberg EC (1984) Regulation of iron-stress-response by whole-plant activity. J Plant Nutr 7:609-621
45. Larbi A, Morales F, López-Millán AF, Gogorcena Y, Abadía A, Moog PR, Abadía J (2001) Technical advance: reduction of Fe(III)-chelates by mesophyll leaf disks of sugar beet. Multi-component origin and effects of Fe deficiency. Plant Cell Physiol 42:94-105
46. Laulhère, J-P, Labouré, A-M, Briat, J-F (1990) Photoreduction and incorporation of iron into ferritins. Biochem J 269:79-84
47. Ling HQ, Koch G, Bäumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96:7098-7103
48. Ling HQ, Bauer P, Berecky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99:13938-13943
49. Liu DH, Adler K, Stephan U W (1998) Iron-containing particles accumulate in organelles and vacuoles of leaf and root cells in the nicotianamine-free tomato mutant chloronerva. Protoplasma 201:213-220
50. Longnecker N, Welch RM (1990) Accumulation of apoplastic iron in plant roots. A factor in the resistance of soybeans to iron-deficiency induced chlorosis. Plant Physiol 92:17-22
51. López-Millán AF, Morales F, Abadía A, Abadía J (2000) Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiol 124:873-884
52. Lucca P, Hurrell R, Potrykus I (2001) Approaches to improving the bioavailability and level of iron in rice seeds. J Sci Food Agric 81:828-834
53. Ma JF, Shinada T, Matsuda C, Nomoto K (1995) Biosynthesis of phytosiderophores, mugineic acids, associated with methionine cycling. J Biol Chem 270:16549-16554
54. Maas M, Van de Wetering DAM, Van Beusichem ML, Bienfait HF (1988) Characterization of phloem iron and its possible role in the regulation of Fe-efficiency reactions. Plant Physiol 87:167-171
55. Marentes E, Grusak MA (1998) Iron transport and storage within the seed coat and embryo of developing seeds of pea (Pisum sativum L). Seed Sci Res 8:367-375
56. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London
57. Mäser P, Thomine S, Schroeder JI, Ward J M, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper F, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646-1667
58. Mori S (1999) Iron acquisition by plants. Curr Opin Plant Biol 2:250-253
59. Mori S, Nakanishi H, Takahashi M, Higuchi K, Nishizawa N-K (2001) Genetic engineering of transgenic rice with barley strategy-II genes. In: Horst WJ, Schenk MK, Bürkert A, Claassen N, Flessa H, Frommer WB, Goldbach H, Olfs H, Römheld V, Sattelmacher B, Schmidhalter U, Schubert S, v Wirén N, Wittenmayer L (eds) Plant nutrition food security and sustainability of agro-ecosystems through basic and applied research. Kluwer, Dordrecht, pp 14-15
60. Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kikuchi S, Mori S, Nishizawa NK (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots. Plant J 30:83-94
61. Neilands JB, Konopka K, Schwyn B, Coy M, Francis T, Paw BH, Bagg A (1987) Comparative biochemistry of microbial iron assimilation. In: Winkelmann G, van der Helm D, Neilands JB (eds) Iron transport in microbes, plants and animals. VCH, Weinheim, pp 3-34
62. +-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817-845
63. Petit JM, van Wuytswinkel O, Briat JF, Lobréaux S (2001) Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem 276:5584-5590
64. 2+-chelator nicotianamine: J Exp Bot 48:759-767
65. Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Fe homeostasis in plant cells: does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration? Planta 213:967-976
66. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils: Nature 397:694-697
67. Rogers, EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787-1799
68. Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175-180
69. Samuelsen AI, Martin RC, Mok DWS, Mok MC (1998) Expression of the yeast FRE genes in transgenic tobacco. Plant Physiol 118:51-58
70. Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167-192
71. Savino G, Briat JF, Lobréaux S (1997) Inhibition of the iron-induced ZmFer1 maize ferritin gene expression by antioxidants and serine/threonine phosphatase inhibitors. J Biol Chem 272:33319-33326
72. Schikora A, Schmidt W (2001) Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiol 125:1679-1687
73. Schmidke I, Krüger C, Frömmichen R, Scholz G, and Stephan UW (1999) Phloem loading and transport characteristics of iron in interaction with plant-endogenous ligands in castor bean seedlings. Physiol Plant 106:82-89
74. Schmidt W (1999) Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141:1-26
75. Scholz G (1989) Effect of nicotianamine on iron re-mobilization in de-rooted tomato seedlings. Biometals 2:89-91
76. Scholz G, Becker R, Pich A, Stephan UW (1992) Nicotianamine - a common constituent of strategies I and II of iron acquisition in plants. J Plant Nutr 15:1649-1665
77. Schurr U (1999) Dynamics of nutrient transport from the root to the shoot. Prog Bot 60:234-253
78. Shingles R, North M, McCarty RE (2002) Ferrous ion transport across chloroplast inner envelope membranes. Plant Physiol 128:1022-1030
79. Stephan UW, Scholz G (1990) Nicotianamine concentrations in iron sufficient and iron deficient sunflower and barley roots J. Plant Physiol 136:631-634
80. Stephan UW, Scholz G (1993) Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol Plant 88:522-529
81. Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 9:84-90
82. Strasser O, Köhl K, Römheld V (1999) Overestimation of apoplastic Fe in roots of soil grown plants. Plant Soil 210:179-187
83. Takagi S (1976) Naturally occurring iron-chelating compounds in oat- and rice-root washings. Activity measurement and preliminary characterization. Soil Sci Plant Nutr 22:423-433
84. Takahashi M, Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa NK, Mori S (1999) Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiol 121:947-956
85. Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466-469
86. Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030-1043
87. 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
88. Tiffin LO (1966) Iron translocation: plant culture, exudate sampling, iron citrate analysis. Plant Physiol 45:280-283
89. Van der Schott C, Rinne P (1999) The symplasmic organization of the shoot apical meristem In: Van Bel AJE, Van Kesteren WJP (eds) Plasmodesmata - structure, function, role in cell communication. Springer, Berlin Heidelberg New York
90. Van Wuytswinkel O, Vansuyt G, Grignon N, Fourcroy P, Briat JF (1999) Iron homeostasis alteration in transgenic tobacco overexpressing ferritin. Plant J 17:93-97
91. Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589-599
92. Vert G, Briat JF, Curie C (2001) Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J 26:181-189
93. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223-1233
94. II. Implications for metal transport in plants. Plant Physiol 119:1107-1114
95. Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85-94
96. Welch RM (2002) Breeding strategies for biofortified staple plant foods to reduce micronutrient malnutrition globally. J Nutr 132:495-499
97. Yamaguchi H, Nakanishi H, Nishizawa N-K, Mori S (2000) Isolation and characterization of IDI2, a new Fe-deficiency-induced cDNA from barley roots, which encodes a protein related to the α subunit of eukaryotic initiation factor 2B (elF2Bα). J Exp Bot 51:3001-2007
98. Yamaguchi H, Nishizawa N-K, Nakanishi H, Mori S (2002) IDI7, a new iron-regulated ABC transporter from barley roots, localizes to the tonoplast. J Exp Bot 53:727-735
99. 59iron in iron-sufficient and -deficient bean plants. J Plant Nutr 18:2049-2058
100. Zimmermann MB, Hurrell RF (2002) Improving iron, zinc and vitamin A nutrition through plant biotechnology. Curr Opin Biotechnol 13:142-145
101. 2 activation in the biosynthesis of ethylene. J Am Chem Soc 124:4602-4609