Iron in seeds - Loading pathways and subcellular localization

Frontiers in Plant Science

Volumn 4, Issue JAN, 2014, Pages

  Grillet, Louis ^a   Mari, Stéphane ^b   Schmidt, Wolfgang ^a  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b Institut National pour la Recherche Agronomique   (France)

Author keywords

Biofortification; Fe in seeds; Fe storage; Fe transport; Grain filling

Indexed keywords

EID: 84900842616     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00535     Document Type: Review

References (99)

1. Bashir, K., Ishimaru, Y., and Nishizawa, N. (2010). Iron uptake and loading into rice grains. Rice 3, 122-130. doi: 10.1007/s12284-010-9042-y
2. Bashir, K., Ishimaru, Y., Shimo, H., Kakei, Y., Senoura, T., Takahashi, R., et al. (2011). Rice phenolics efflux transporter 2 (PEZ2) plays an important role in solubilizing apoplasmic iron. Soil Sci. Plant Nutr. 57, 803-812. doi: 10.1080/00380768.2011.637305
3. Bienfait, H., and Scheffers, M. (1992). Some properties of ferric citrate relevant to the iron nutrition of plants. Plant Soil 143, 141-144. doi: 10.1007/BF00009139
4. Blair, M. W., Knewtson, S. J. B., Astudillo, C., Li, C. M., Fernandez, A. C., and Grusak, M. A. (2010). Variation and inheritance of iron reductase activity in the roots of common bean (Phaseolus vulgaris L.) and association with seed iron accumulation QTL. BMC Plant Biol. 10:215. doi: 10.1186/1471-2229-10-215
5. Brown, J. C., and Chaney, R. L. (1971). Effect of iron on transport of citrate into xylem of soybeans and tomatoes. Plant Physiol. 47, 836-840. doi: 10.1104/pp.47.6.836
6. Conklin, P. L., Saracco, S. A., Norris, S. R., and Last, R. L. (2000). Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154, 847-856.
7. Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Jean, M., et al. (2009). Metal movement within the plant: contribution of nicotianamine and YELLOW STRIPE 1-LIKE transporters. Ann. Bot. 103, 1-11. doi: 10.1093/aob/mcn207
8. Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S. L., Briat, J. F., and Walker, E. L. (2001). Maize YELLOW STRIPE1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346-349. doi: 10.1038/35053080
9. Davila-Hicks, P., Theil, E. C., and Lönnerdal, B. (2004). Iron in ferritin or in salts (ferrous sulfate) is equally bioavailable in nonanemic women. Am. J. Clin. Nutr. 80, 936-940.
10. 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. 144, 197-205. doi: 10.1104/pp.107.097162
11. Eide, D., Broderius, M., Fett, J., and Guerinot, M. L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. U.S.A. 93, 5624-5628. doi: 10.1073/pnas.93.11.5624
12. Fernandez-Calvino, L., Faulkner, C., Walshaw, J., Saalbach, G., Bayer, E., Benitez-Alfonso, Y., et al. (2011). Arabidopsis plasmodesmal proteome. PLoS ONE 6:e18880. doi: 10.1371/journal.pone.0018880
13. Fourcroy, P., Siso-Terraza, P., Sudre, D., Saviron, M., Reyt, G., Gaymard, F., et al. (2013). Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol. 201, 155-167. doi: 10.1111/nph.12471
14. Foyer, C. H., and Lelandais, M. (1996). A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. J. Plant Physiol. 148, 391-398. doi: 10.1016/S0176-1617(96)80271-9
15. García, M., Romera, F., Stacey, M., Stacey, G., Villar, E., Alcántara, E., et al. (2013). Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants. Planta 237, 65-75. doi: 10.1007/s00425-012-1757-0
16. Gendre, D., Czernic, P., Conejero, G., Pianelli, K., Briat, J. F., Lebrun, M., et al. (2007). TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J. 49, 1-15. doi: 10.1111/j.1365-313X.2006.02937.x
17. Goto, F., Yoshihara, T., Shigemoto, N., Toki, S., and Takaiwa, F. (1999). Iron fortification of rice seed by the soybean ferritin gene. Nature Biotechnol. 17, 282-286. doi: 10.1038/7029
18. Grillet, L., Ouerdane, L., Hoang, M. T. T., Isaure, M. P., Lobinski, R., Curie, C., et al. (2013). Ascorbate efflux as a new strategy for iron reduction and transport in plants. J. Biol. Chem. doi: 10.1074/jbc.M113.514828
19. Grinstead, R. R. (1960). The oxidation of ascorbic acid by hydrogen peroxide-Catalysis by ethylenediaminetetraacetato-iron(III). J. Am. Chem. Soc. 82, 3464-3471. doi: 10.1021/ja01498a057
20. Grusak, M. A., and 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.
21. Hallberg, L., Brune, M., and Rossander, L. (1989). Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. Am. J. Clin. Nutr. 49, 140-144.
22. Hindt, M. N., and Guerinot, M. L. (2012). Getting a sense for signals: regulation of the plant iron deficiency response. Biochim. Biophys. Acta 1823, 1521-1530. doi: 10.1016/j.bbamcr.2012.03.010
23. Hocking, P. J., and Pate, J. S. (1977). Mobilization of minerals to developing seeds of legumes. Ann. Bot. 41, 1259-1278.
24. Inoue, H., Kobayashi, T., Nozoye, T., Takahashi, M., Kakei, Y., Suzuki, K., et al. (2009). 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. doi: 10.1074/jbc.M806042200
25. Ishimaru, Y., Kakei, Y., Shimo, H., Bashir, K., Sato, Y., Sato, Y., et al. (2011). A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J. Biol. Chem. 286, 24649-24655. doi: 10.1074/jbc.M111.221168
26. Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., et al. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62, 379-390. doi: 10.1111/j.1365-313X.2010.04158.x
27. Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., et al. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 45, 335-346. doi: 10.1111/j.1365-313X.2005.02624.x
28. Iwai, T., Takahashi, M., Oda, K., Terada, Y., and Yoshida, K. T. (2012). Dynamic changes in the distribution of minerals in relation to phytic acid accumulation during rice seed development. Plant Physiol. 160, 2007-2014. doi: 10.1104/pp.112.206573
29. Jeong, J., Cohu, C., Kerkeb, L., Pilon, M., Connolly, E. L., and Guerinot, M. L. (2008). Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc. Natl. Acad. Sci. U.S.A. 105, 10619-10624. doi: 10.1073/pnas.0708367105
30. Jeong, J., and Connolly, E. L. (2009). Iron uptake mechanisms in plants: functions of the FRO family of ferric reductases. Plant Sci. 176, 709-714. doi: 10.1016/j.plantsci.2009.02.011
31. Johnson, A. T., Kyriacou, B., Callahan, D. L., Carruthers, L., Stangoulis, J., Lombi, E., et al. (2011). Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron-and zinc-biofortification of rice endosperm. PLoS ONE 6:e24476. doi:10.1371/journal.pone.0024476
32. Kehr, J., and Rep, M. (2007). Protein extraction from xylem and phloem sap. Methods Mol. Biol. 355, 27-35.
33. Kim, S. A., Punshon, T., Lanzirotti, A., Li, L. T., Alonso, J. M., Ecker, J. R., et al. (2006). Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295-1298. doi: 10.1126/science.1132563
34. Klatte, M., Schuler, M., Wirtz, M., Fink-Straube, C., Hell, R., and Bauer, P. (2009). The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol. 150, 257-271. doi: 10.1104/pp.109.136374
35. Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., et al. (2004). OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39, 415-424. doi: 10.1111/j.1365-313X.2004.02146.x
36. Krüger, C., Berkowitz, O., Stephan, U. W., and 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. doi: 10.1074/jbc.M201896200
37. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W. B., and Patrick, J. W. (2003). Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 26, 37-56. doi: 10.1046/j.1365-3040.2003.00847.x
38. Lane, D. J. R., and Lawen, A. (2008). Non-transferrin iron reduction and uptake are regulated by transmembrane ascorbate cycling in K562 cells. J. Biol. Chem. 283, 12701-12708. doi: 10.1074/jbc.M800713200
39. Lanquar, V., Lelievre, F., Bolte, S., Hames, C., Alcon, C., Neumann, D., et al. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041-4051. doi: 10.1038/sj.emboj.7600864
40. Le Jean, M., Schikora, A., Mari, S., Briat, J. F., and Curie, C. (2005). A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J. 44, 769-782. doi: 10.1111/j.1365-313X.2005.02569.x
41. Lee, S., Jeon, U. S., Lee, S. J., Kim, Y. K., Persson, D. P., Husted, S., et al. (2009). Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Natl. Acad. Sci. U.S.A. 106, 22014-22019. doi: 10.1073/pnas.0910950106
42. Lee, S., Kim, Y.-S., Jeon, U., Kim, Y.-K., Schjoerring, J., and An, G. (2012). Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Mol. Cells 33, 269-275. doi: 10.1007/s10059-012-2231-3
43. Lin, Y. F., Liang, H. M., Yang, S. Y., Boch, A., Clemens, S., Chen, C. C., et al. (2009). Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol. 182, 392-404. doi: 10.1111/j.1469-8137.2009.02766.x
44. Ling, H. Q., Koch, G., Baumlein, H., and Ganal, M. W. (1999). Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc. Natl. Acad. Sci. U.S.A. 96, 7098-7103. doi: 10.1073/pnas.96.12.7098
45. Lobréaux, S., and Briat, J. F. (1991). Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem. J. 274, 601-606.
46. Lott, J., Goodchild, D., and Craig, S. (1984). Studies of mineral reserves in pea (Pisum sativum) cotyledons using low-water-content procedures. Funct. Plant Biol. 11, 459-469.
47. Lubkowitz, M. A., Hauser, L., Breslav, M., Naider, F., and Becker, J. M. (1997). An oligopeptide transport gene from Candida albicans. Microbiology 143, 387-396. doi: 10.1099/00221287-143-2-387
48. Lubkowitz, M. A., Barnes, D., Breslav, M., Burchfield, A., Naider, F., and Becker, J. M. (1998). Schizosaccharomyces pombe isp4 encodes a transporter representing a novel family of oligopeptide transporters. Mol. Microbiol. 28, 729-741. doi: 10.1046/j.1365-2958.1998.00827.x
49. Masuda, H., Usuda, K., Kobayashi, T., Ishimaru, Y., Kakei, Y., Takahashi, M., et al. (2009). Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2, 155-166. doi: 10.1007/s12284-009-9031-1
50. Masuda, H., Ishimaru, Y., Sann Aung, M., Kobayashi, T., Kakei, Y., Takahashi, M., et al. (2012). Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci. Rep. 2:543. doi: 10.1038/srep00543
51. Morrissey, J., Baxter, I. R., Lee, J., Li, L. T., Lahner, B., Grotz, N., et al. (2009). The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21, 3326-3338. doi: 10.1105/tpc.109.069401
52. Mukherjee, I., Campbell, N. H., Ash, J. S., and Connolly, E. L. (2006). Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223, 1178-1190. doi: 10.1007/s00425-005-0165-0
53. Murray-Kolb, L. E., Welch, R., Theil, E. C., and Beard, J. L. (2003). Women with low iron stores absorb iron from soybeans. Am. J. Clin. Nutr. 77, 180-184.
54. Nishiyama, R., Kato, M., Nagata, S., Yanagisawa, S., and Yoneyama, T. (2011). Identification of Zn-nicotianamine and Fe-2'-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.). Plant Cell Physiol. 53, 381-390. doi: 10.1093/pcp/pBR188
55. Noma, M., Noguchi, M., and Tamaki, E. (1971). New amino acid, nicotianamine, from tobacco leaves. Tetrahedron Lett. 12, 2017-2020. doi: 10.1016/S0040-4039(01)96769-3
56. Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Uozumi, N., et al. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286, 5446-5454. doi: 10.1074/jbc.M110.180026
57. Palmer, C. M., and Guerinot, M. L. (2009). Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat. Chem. Biol. 5, 333-340. doi: 10.1038/nchembio.166
58. Patrick, J. W., and Offler, C. E. (2001). Compartmentation of transport and transfer events in developing seeds. J. Exp. Bot. 52, 551-564. doi: 10.1093/jexbot/52.356.551
59. Persson, D. P., Hansen, T. H., Laursen, K. H., Schjoerring, J. K., and Husted, S. (2009). Simultaneous iron, zinc, sulfur and phosphorus speciation analysis of barley grain tissues using SEC-ICP-MS and IP-ICP-MS. Metallomics 1, 418-426. doi: 10.1039/b905688b
60. Procházka, Ž., and Scholz, G. (1984). Nicotianamine, the 'normalizing factor' for the auxotroph tomato mutant Chloronerva; a representative of a new class of plant effectors. Experientia 40, 794-801. doi: 10.1007/BF01951961
61. Rautenkranz, A. A. F., Li, L. J., Machler, F., Martinoia, E., and Oertli, J. J. (1994). Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare cv Gerbel) leaves. Plant Physiol. 106, 187-193.
62. Rellan-Alvarez, R., Abadia, J., and Alvarez-Fernandez, A. (2008). Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. a study by electrospray ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom 22, 1553-1562. doi: 10.1002/rcm.3523
63. Rellan-Alvarez, R., Giner-Martinez-Sierra, J., Orduna, J., Orera, I., Rodriguez-Castrillon, J. A., Garcia-Alonso, J. I., et al. (2010). Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol. 51, 91-102. doi: 10.1093/pcp/pcp170
64. Robinson, N. J., Procter, C. M., Connolly, E. L., and Guerinot, M. L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature 397, 694-697. doi: 10.1038/17800
65. Rodriguez-Celma, J., Lin, W. D., Fu, G. M., Abadia, J., Lopez-Millan, A. F., and Schmidt, W. (2013). Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol. 162, 1473-1485. doi: 10.1104/pp.113.220426
66. Rogers, E. E., Wu, X., Stacey, G., and Nguyen, H. T. (2009). Two MATE proteins play a role in iron efficiency in soybean. J. Plant Physiol. 166, 1453-1459. doi: 10.1016/j.jplph.2009.02.009
67. Römheld, V., and Marschner, H. (1983). Mechanism of iron uptake by peanut plants-I. Fe(III) reduction, chelate splitting, and release of phenolics. Plant Physiol. 71, 949-954.
68. Roschzttardtz, H., Conéjéro, G., Curie, C., and Mari, S. (2009). Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol. 151, 1-10. doi: 10.1104/pp.109.144444
69. Roschzttardtz, H., Conèjèro, G., Divol, F., Alcon, C., Verdeil, J.-L., Curie, C., et al. (2013). New insights into Fe localization in plant tissues. Front. Plant Sci. 4, 350. doi: 10.3389/fpls.2013.00350
70. Roschzttardtz, H., Grillet, L., Isaure, M. P., Conejero, G., Ortega, R., Curie, C., et al. (2011a). Plant cell nucleolus as a hot spot for iron. J. Biol. Chem. 286, 27863-27866. doi: 10.1074/jbc.C111.269720
71. Roschzttardtz, H., Séguéla-Arnaud, M., Briat, J.-F., Vert, G., and Curie, C. (2011b). The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23, 2725-2737. doi: 10.1105/tpc.111.088088
72. Santi, S., and Schmidt, W. (2009). Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol. 183, 1072-1084. doi: 10.1111/j.1469-8137.2009.02908.x
73. Sayers, M. H., Lynch, S. R., Jacobs, P., Charlton, R. W., Bothwell, T. H., Walker, R. B., et al. (1973). The Effects of ascorbic acid supplementation on the absorption of iron in maize, wheat and soya. Br. J. Haematol. 24, 209-218. doi: 10.1111/j.1365-2141.1973.tb05741.x
74. Schaaf, G., Ludewig, U., Erenoglu, B. E., Mori, S., Kitahara, T., and Von Wiren, N. (2004). ZmYS1 functions as a proton-coupled symporter for phytosiderophore-and nicotianamine-chelated metals. J. Biol. Chem. 279, 9091-9096. doi: 10.1074/jbc.M311799200
75. Schnell Ramos, M., Khodja, H., Mary, V., and Thomine, S. (2013). Using μPIXE for quantitative mapping of metal concentration in Arabidopsis thaliana seeds. Front. Plant Sci. 4:168. doi: 10.3389/fpls.2013.00168
76. Schuler, M., Rellàn-Alvarez, R., Fink-Straube, C., Abadia, J., and Bauer, P. (2012). Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24, 2380-2400. doi: 10.1105/tpc.112.099077
77. Shanmugam, V., Lo, J. C., Wu, C. L., Wang, S. L., Lai, C. C., Connolly, E. L., et al. (2011). Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana-The role in zinc tolerance. New Phytol. 190, 125-137. doi: 10.1111/j.1469-8137.2010.03606.x
78. Sperotto, R. A., Ricachenevsky, F. K., Waldow, V. D. A., and Fett, J. P. (2012). Iron biofortification in rice: it's a long way to the top. Plant Sci. 190, 24-39. doi: 10.1016/j.plantsci.2012.03.004
79. Stacey, M. G., Koh, S., Becker, J., and Stacey, G. (2002). AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. Plant Cell 14, 2799-2811. doi: 10.1105/tpc.005629
80. Stacey, M. G., Patel, A., Mcclain, W. E., Mathieu, M., Remley, M., Rogers, E. E., et al. (2008). The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol. 146, 589-601. doi: 10.1104/pp.107.108183
81. Stadler, R., Lauterbach, C., and Sauer, N. (2005). Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701-712. doi: 10.1104/pp.105.065607
82. Stoltzfus, R. J. (2003). Iron deficiency: global prevalence and consequences. Food Nutr. Bull. 24, 99-103.
83. Stomph, J. T., Jiang, W., and Struik, P. C. (2009). Zinc biofortification of cereals: rice differs from wheat and barley. Trends Plant Sci. 14, 123-124. doi: 10.1016/j.tplants.2009.01.001
84. Takahashi, M., Nozoye, T., Kitajima, N., Fukuda, N., Hokura, A., Terada, Y., et al. (2009). In vivo analysis of metal distribution and expression of metal transporters in rice seed during germination process by microarray and X-ray fluorescence imaging of Fe, Zn, Mn, and Cu. Plant Soil 325, 39-51. doi: 10.1007/s11104-009-0045-7
85. Thomine, S., and Vert, G. (2013). Iron transport in plants: better be safe than sorry. Curr. Opin. Plant Biol. 16, 322-327. doi: 10.1016/j.pbi.2013.01.003
86. Urzica, E. I., Casero, D., Yamasaki, H., Hsieh, S. I., Adler, L. N., Karpowicz, S. J., et al. (2012). Systems and trans-system level analysis identifies conserved iron deficiency responses in the plant lineage. Plant Cell 24, 3921-3948. doi: 10.1105/tpc.112.102491
87. Van Dongen, J. T., Ammerlaan, A. M. H., Wouterlood, M., Van Aelst, A. C., and Borstlap, A. C. (2003). Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann. Bot. 91, 729-737. doi: 10.1093/aob/mcg066
88. Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M. L., Briat, J. F., et al. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223-1233. doi: 10.1105/tpc.001388
89. von Wiren, N., Klair, S., Bansal, S., Briat, J. F., Khodr, H., Shioiri, T., et al. (1999). Nicotianamine chelates both Fe-III and Fe-II. Implications for metal transport in plants. Plant Physiol. 119, 1107-1114. doi: 10.1104/pp.119.3.1107
90. Wada, T., and Lott, J. N. A. (1997). Light and electron microscopic and energy dispersive X-ray microanalysis studies of globoids in protein bodies of embryo tissues and the aleurone layer of rice (Oryza sativa L.) grains. Can. J. Bot. 75, 1137-1147. doi: 10.1139/b97-125
91. Waters, B. M., Chu, H. H., Didonato, R. J., Roberts, L. A., Eisley, R. B., Lahner, B., et al. (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. doi: 10.1104/pp.106.082586
92. Waters, B. M., and Grusak, M. A. (2008). Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol. 177, 389-405.
93. Wintz, H., Fox, T., Wu, Y. Y., Feng, V., Chen, W. Q., Chang, H. S., et al. (2003). Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278, 47644-47653. doi: 10.1074/jbc.M309338200
94. Wirth, J., Poletti, S., Aeschlimann, B., Yakandawala, N., Drosse, B., Osorio, S., et al. (2009). Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7, 631-644. doi: 10.1111/j.1467-7652.2009.00430.x
95. Wu, H. L., Li, L. H., Du, J., Yuan, Y. X., Cheng, X. D., and Ling, H. Q. (2005). Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol. 46, 1505-1514. doi: 10.1093/pcp/pci163
96. Yokosho, K., Yamaji, N., Ueno, D., Mitani, N., and Ma, J. F. (2009). OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol. 149, 297-305. doi: 10.1104/pp.108.128132
97. Zaharieva, T. B., and Abadía, J. (2003). Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221, 269-275.
98. Zheng, L. Q., Cheng, Z. Q., Ai, C. X., Jiang, X. H., Bei, X. S., Zheng, Y., et al. (2010). Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5:e10190. doi:10.1371/journal.pone.0010190
99. Zimmermann, M. B., and Hurrell, R. F. (2007). Nutritional iron deficiency. Lancet 370, 511-520. doi: 10.1016/S0140-6736(07)61235-5