Heavy metals competing with iron under conditions involving phytoremediation

Iron Nutrition in Plants and Rhizospheric Microorganisms

Volumn , Issue , 2006, Pages 129-151

  Fodor, Ferenc ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

chelates; heavy metals; hyperaccumulation; iron; phytoremediation

Indexed keywords

EID: 79960485463     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/1-4020-4743-6_6     Document Type: Chapter

References (122)

1. Alcántara, E., Romera, F. J., Cañete, M. and de la Guardia, M. D. (1994) Effects of heavy metals on both induction and function of root Fe(III) reductase in Fe-deficient cucumber (Cucumis sativus L) plants, J. Exp. Bot. 45, 1893-1898.
2. Allison, J. D., Brown, D. S. and Novo-Gradak, K. J. (1991) A Geochemical Assessment Model for Environmental Systems v. 3.0. Environmental Research Laboratory United States Environmental Protection Agenci Washington D. C., USA.
3. Alloway, B. J. (1995) Heavy Metals in Soils. 2nd edition, Blackie and Son, Glasgow and London, U.K., pp. 134-155.
4. Anderegg, G. and Ripperger, H. (1989) The normalizing function for the tomato mutant chloronerva. Correlation between metal complex formation and biological activity of nicotianamine analogues, J. Chem. Soc. Chem. Commun. 10, 647-650.
5. Awad, F. and Römheld, V. (2000) Mobilization of heavy metals from contaminated calcareous soils by plant born, microbial and synthetic chelators and their uptake by wheat plants, J. Plant Nutr. 23, 1847-1855.
6. Baker, A. J. M. (1981) Accumulators and excluders -Strategies in the response of plants to heavy metals, J. Plant Nutr. 3, 643-654.
7. Baker, A. J. M. and Brooks, R. R. (1989) Terrestrial higher plants which hyperaccumulate metallic elements-A review of their distribution, ecology and phytochemistry, Biorecovery 1, 81-126.
8. Baker, A. J. M., McGrath, S. P., Reeves, R. D. and Smith, J. A. C. (2000) Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils, In N. Terry, G. Banuelos and J. Vangrosveld (eds.)), Phytoremediation of Contaminated Soil and Water, Lewis Publisher, Boca Raton, FL, USA, pp. 85-107.
9. Barak, P. and Helmke, P. A. (1993) The chemistry of zinc, In A. D. Robson (ed.)), Zinc in Soils and Plants, Kluwer Academic Publishers, New York, pp. 1-13.
10. Becker, R., Grün, M. and Scholz, G. (1992) Nicotianamine and the distribution of iron into the apoplasm and symplasm of tomato (Lycopersicon esculentum Mill.), Planta 187, 48-52.
11. Bell, P. F., Chaney, R. L and Angle, J. S. (1991a) Free metal activity and total metal concentrations as indices of micronutrient availability to barley [Hordeum vulgare (L.) Klages], Plant Soil 130, 51-62.
12. Bell, P. F., James, B. R. and Chaney, R. J. (1991b) Heavy metal extractability in long-term sewage sludge and metal salt-Amended soils, J. Environ. Qual. 20, 481-486.
13. Bienfait, H. F., van den Briel, W. and Mesland-Mul, N. T. (1985) Free space iron pools in roots. Generation and mobilization, Plant Physiol. 78, 596-600.
14. Blakeley, S. D., Robaglia, Ch., Brzezinski, R. and Thirion, J. P. (1986) Induction of low molecular weight cadmium-binding compound in soybean roots, J. Exp. Bot. 37, 956-964.
15. Blaylock, M. J., Salt, D. E., Dushenkov, S., Zakharova, O., Gussman, C., Kapulnik, Y., Ensley, B. D. and Raskin, I. (1997) Enhanced accumulation of Pb in Indian mustard by soil-Applied chelating agents, Environ. Sci. Technol. 31, 860-865.
16. Bolan, N. S., Adriano, D. C., Duraisamy, P., Mani, A. and Arulmozishelvan, K. (2003) Immobilization and phytoavailability of cadmium in variable charge soils I Effect of phosphate addition, Plant Soil 250, 83-94.
17. Brooks, R. R., Lee, J., Reeves, R. D. and Jaffré, T. (1977) Detection of nickeliferous rocks by analysis of herbarium species of indicator plants, J. Geochem. Explor. 7, 49-57.
18. Brooks, R. R. (1998) Plants That Hyperaccumulate Heavy Metals. CAB International, Wallingford, U. K.
19. Bughio, N., Yamaguchi, H., Nishizawa, N. K., Nakanishi, H. and Mori, S. (2002) Cloning an iron-regulated metal transporter from rice, J. Exp. Bot. 53, 1677-1682.
20. Chang, Y.-C., Zouari, M., Gogorcena, Y., Lucena, J. J. and Abadía, J. (2003) Effects of cadmium and lead on ferric chelate reductase activities in sugar beet roots, Plant Physiol. Biochem. 41, 999-1005.
21. Chaney, R. L., Brown, J. C. and Tiffin, L O. (1972) Obligatory reduction of ferric chelates in iron uptake by soybeans, Plant Physiol. 50, 208-213.
22. Chaney, R. L (1983) Plant uptake of inorganic waste constituents, In J. F. Parr, P. B. Marsh and J. S. Kla (eds.)), Land Treatment of Hazardous Wastes, Noyes Data Corp, Park Ridge, NJ, USA, pp. 50-76.
23. Chen, Y., Shi, J., Tian, G., Zheng, S. and Lin, Q. (2004) Fe deficiency induces Cu uptake and accumulation in Commelina communis, Plant Sci. 166, 1371-1377.
24. Cieslinski, G., Van Rees, K. C. J., Szmigielska, A. M. and Huang, P. M. (1997) Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions, J. Plant Nutr. 20, 753-764.
25. Cohen, C. K., Fox, T. C., Garvin, D. F. and Kochian, L V. (1998) The role of iron deficiency stress responses in stimulating heavy metal transport in plants, Plant Physiol. 116, 1063-1072.
26. Conolly, E. L., Fett, J. P. and Guerinot, M. L (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation, Plant Cell 14, 1347-1357.
27. Cooper, E. M., Sims, J. T., Cunningham, S. D., Huang, J. W. and Berti, W. R. (1999) Chelateassisted phytoextraction of lead from contaminated soils, J. Environ. Qual. 28, 1709-1719.
28. Crowley, D. E., Reid, C. P. P. and Szaniszlo, P. J. (1987) Microbial siderophores as iron sources for plants, In R. Winkelman, D. Van der Helm and J. B. Neilands (eds.)), Iron Transport in Microbes, Plants and Animals, VCH Publishers, New York, pp. 365-386.
29. Curie, C., Alonso, J., Le Jean, M., Ecker, J. R. and Briat, J.-F. (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport, Biochem. J. 347, 749-755.
30. Curie, C., Panaviene, Z., Loulerque, C., Dellaporta, S. T., 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.
31. Dix, D. R., Bridgham, J. T., Broderius, M. A., Byersdorfer, C. A. and Eide, D. J. (1994) The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae, J. Biol. Chem. 269, 26092-26099.
32. Eckhardt, U., Mas Marques, A. and Buckhout, T. J. (2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants, Plant Mol. Biol. 45, 437-448.
33. Eide, D. J. (1998) The molecular biology of metal ion transport in Saccharomyces cerevisiae, Annu. Rev. Nutr. 18, 441-469.
34. Eide, D., Broderius, M., Feit, J. and Guerinot, M. L (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast, P. Natl. Acad. Sci. USA 93, 5624-5628.
35. Epstein, A. L., Gussman, C. D., Blaylock, M. J., Yermiyahu, U., Huang, J. W., Kapulnik, Y. and Orser, C. S. (1999) EDTA and Pb-EDTA accumulation in Brassica junicea grown in Pb-Amended soil, Plant Soil 208, 87-94.
36. Ernst, W. H. O., Assunção, A. G. L., Verkleij, J. A. C. and Schat, H. (2002) How important is apoplastic zinc loading in Thlaspi caerulescens?, New Phytol. 155, 1-7.
37. Fodor, F., Sárvári, E., Láng, F., Szigeti, Z. and Cseh, E. (1996) Effects of Pb and Cd on cucumber depending on the Fe-complex in the culture solution, J. Plant Physiol. 148, 434-439.
38. Field, L S., Luk, E. and Culotta, V. C. (2002) Copper chaperones: personal escorts for metal ions, J. Bioenerg. Biomemb. 34, 373-379.
39. García-Marco, S., Yunta, F., de la Hinojosa, M I M., Martí, G. and Lucena, J. J. (2003) Evaluation of commercial Fe(III)-chelates using different methods, J. Plant Nutr. 26, 2009-2021.
40. Hassett, R., Dix, D. R., Eide, D. J. and Kosman, D. J. (2000) The Fe(II) permease Fet4p functions as a low affinity copper transporter and supports normal copper trafficking in Saccharomyces cerevisiae, Biochem J. 351, 477-484.
41. Hell, R. and Stephan, U. W. (2003) Iron uptake, trafficking and homeostasis in plants, Planta 216, 541-551.
42. Herbik, A., Bölling, C. and Buckhout, T. J. (2002) The involvement of a multicopper oxidase in iron uptake by the green algae Chlamydomonas reinhardtii, Plant Physiol. 130, 2039-2048.
43. Herbik, A., Giritch, A., Horstmann, C., Becker, R., Balzer, H. J., Bäumlein, H. and Stephan, U. W. (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.
44. Hider, R. C. (1984) Siderophore mediated absorption of iron, Struct. Bond. 58, 25-87.
45. Hider, R. C., Yoshimura, E., Khodr, H. and von Wirén, N. (2004) Competition or complementation: the iron-chelating abilities of nicotianamine and phytosiderophores, New Phytol. 164, 204-208.
46. Hill-Cottingham, D. G. and Lloyd-Jones, C. P. (1961) Absorption and breakdown of ironethylenediamine tetraacetic acid by tomato plants, Nature 189, 312.
47. Hill-Cottingham, D. G. and Lloyd-Jones, C. P. (1965) The behavior of iron chelating agents with plants, J. Exp. Bot. 16, 233-242.
48. Hoopes, J. T. and Dean, J. F. D. (2004) Ferroxidase activity in a laccase-like multcopper oxidase from Liriodendron tulipifera, Plant Physiol. Biochem. 42, 27-33.
49. Huang, J. W. W., Chen, J. J., Berti, W. R. and Cunningham, S. D. (1997) Phytorediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction, Environ. Sci. Technol. 31, 800-805.
50. Huang, J. W. and Cunningham, S. D. (1996) Lead phytoextraction: species variation in lead uptake and translocation, New Phytol. 134, 75-84.
51. Jeffreys, R. A. and Wallace, A. (1968) Detection of iron ethylenediamine di(ohydroxyphenylacetate) in plant tissue, Agron. J. 60, 613-616.
52. Kabata-Pendias, A. (2001) Trace Elements in Soils and Plants. 3rd edition, CRC Press, Boca Raton, FL, USA, pp. 413.
53. Kerkeb, L and Krämer, U. (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea, Plant Physiol. 131, 716-724.
54. Küpper, H., Lombi, E., Zhao, F. J. and McGrath, S. P. (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri, Planta 212, 75-84.
55. Küpper, H., Zhao, F. J. and McGrath, S. P. (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens, Plant Physiol. 119, 305-311.
56. Landsberg, E.-C. (1995) Transfer cell formation in sugar beet roots induced by latent Fe deficiency, In J. Abadía (ed.)), Iron Nutrition in Soils and Plants, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 67-75.
57. Lane, B., Kajoika, R. and Kennedy, R. (1987) The wheat-germ Ec protein is a zinc-containing metallothionein, Biochem. Cell Biol. 65, 1001-1005.
58. Larbi, A., Morales, F., Abadía, A., Gogorcena, Y., Lucena, J. J. and Abadía, J. (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition, Funct. Plant Biol. 29, 1453-1464.
59. Liao, M. T., Hedley, M. J., Wooley, D. J., Brooks, R. R. and Nichols, M. A. (2000) Copper uptake and translocation in chicory (Cichorium intybus L cv. Grasslands Puna) and tomato (Lycopersicon esculentum Mill. Cv. Rondy) plants grown in NFT system: II. The role of nicotianamine and histidine in xylem sap copper transport, Plant Soil 223, 243-252.
60. Liu, X. F., Supek, F., Nelson, N. and Culotta, V. C. (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene, J. Biol. Chem. 272, 11763-11769.
61. Lombi, E., Tearall, K. L., Howarth, J. R., Zhao, F.-J., Hawkesford, M. J. and McGrath, S. P. (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens, Plant Physiol. 128, 1359-1367.
62. López-Millán, A.-F., Morales, F., Abadía, A. and 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.
63. Lucena, C., Montilla, I., Romera, F. J. and Alcántara, E. (2003) Effects of several metals on both Fe(III)-and Cu(II)-reduction by roots of Fe-deficient cucumber plants, J. Plant Nutr. 26, 2069-2079.
64. Luo, Y. M. and Christie P. (1998) Bioavailability of copper and zinc in soils treated with alkaline stabilized sewage sludges, J. Environ. Qual. 27, 335-342.
65. Marschner, H., Römheld, V. and Kissel, M. (1986) Different strategies in higher plants in mobilization and uptake of iron, J. Plant Nutr. 9, 695-713.
66. Marschner, H. (1995) Mineral Nutrition of Higher Plants, Academic Press, London, U.K.
67. Maser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., Talke, I. N., Amtmann, A., Maathuis, F. J. M. and Sanders, D. (2001) Phylogenetic relationships within cation transporter families of Arabidopsis, Plant Physiol. 126, 1646-1667.
68. McBride, M. B. (1989) Reactions controlling heavy metal solubility in soils. Adv. Soil Sci. 10, 1-57.
69. McGrath, S. P., Zhao, F. J. and Lombi, E. (2002) Phytoremediation of metals, metalloids and radionuclides, Adv. Agron. 75, 1-56.
70. Merry, R. H., Tiller, K. G. and Alston, A. M. (1986) The effects of soil contamination with copper, lead and arsenic on the growth and composition of plants: effects of source of contamination, soil pH and waterlogging, Plant Soil 95, 255-270.
71. Murakami, T., Ise, K., Hayakawa, M., Kamei, S. and Takagi, S. (1989) Stabilities of metal complexes of mugineic acid and their specific affinities for iron (III), Chem. Lett. 2137-2140.
72. Murphy, A., Zhou, J., Goldsbrough, P. B. and Taiz, L (1997) Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana, Plant Physiol. 113, 1293-1301.
73. Naidu, R., Oliver, D. and McConnell, S. (2003) Heavy metal phytotoxicity in soils, In A. Langley, M. Gilbey and B. Kennedy (eds.)), Proceedings of the Fifth National Workshop on the Assessment of Site Contamination, Adelaide, Australia, pp. 235-240.
74. Nikolic, M. and Römheld, V. (2002) Does high bicarbonate supply to roots change availability of iron in the leaf apoplast?, Plant Soil 241, 67-74.
75. Nikolic, M., Römheld, V. and Merkt, N. (2000) Efect of bicarbonate on uptake and translocation of 59Fe in two grapevine rootstocks differing in their resistance to Fe deficiency chlorosis, Vitis 39, 145-149.
76. Nikolic, M. and Römheld, V. (2003) Nitrate does not result in iron inactivation in the apoplast of sunflower leaves, Plant Physiol. 132, 1303-1314.
77. Pandey, N. and Sharma, C. P. (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage, Plant Science 163, 753-758.
78. Parker, D. R., Norwell, W. A. and Chaney, R. L (1995) Geochem-PC: a chemical speciation program for IBM and compatible personal computers, In R. H. Loeppert, A. P. Schwab and S. Goldberg (eds.)), Chemical Equilibrium and Reaction Models (Special Publication No. 42.), Soil Science Society of America, Madison, WI, USA, pp. 253-269.
79. Pence, N. S., Larsen, P. B., Ebbs, S. D., Letham, D. L D., Lasat, M. M., Garvin, D. F., Eide, D. and Kochian, L V. (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens, P. Natl. Acad. Sci. USA 97, 4956-4960.
80. Perfus-Barbeoch, L., Leonhardt, N., Vavasseur, A. and Forestier, C. (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status, Plant J. 32, 539-548.
81. Pich, A., Scholz, G. and Stephan, U. W. (1994) Iron-dependent changes of heavy metals, nicotianamine and citrate in different plant organs and in the xylem exudates of two tomato genotypes. Nicotianamine as possible copper translocator, Plant Soil 165, 189-196.
82. Rauser, W. E. (1995) Phytochelatins and related peptides, Plant Physiol. 109, 1141-1149.
83. Rengel, Z., Römheld, V. and Marschner, H. (1998) Uptake of zinc and iron by wheat genotypes differing in tolerance to zinc deficiency, J. Plant Physiol. 152, 433-438.
84. Robinson, N. J., Procter, C. M., Conolly, E. L and Guerinot, M. L (1999) A ferric-chelate reductase for iron uptake from soils, Nature 397, 694-697.
85. Römheld, V. (1991) The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: An ecological approach, Plant Soil 130, 127-134.
86. Salt, D. E., Prince, R. C., Pickering, I. J. and Raskin, I. (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard, Plant Physiol. 109, 1427-1433.
87. Salt, D. E., Smith, R. D. and Raskin, I. (1998) Phytoremediation, Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643-668.
88. Sancenon, V., Puig, S., Mira, H., Thiele, D. J. and Peñarrubia, L (2003) Identification of a copper transporter family in Arabidopsis thaliana, Plant Mol. Biol. 51, 577-587.
89. Sanitá di Toppi, L and Gabrielli, R. (1999) Response to cadmium in higher plants, Env. Exp. Bot. 41, 105-130.
90. Satroutdinov, A. D., Dedyukhina, E. G., Chistyakova, T. I., Witschel, M., Minkevich, I. G., Eroshin, V. K. and Egli, T. (2000) Degradation of metal-EDTA complexes by resting cells of the bacterial strain DSM 9103, Environ. Sci. Technol. 34, 1715-1720.
91. Schmidt, W. (2003) Iron homeostasis in plants: sensing and signalling pathways, J. Plant Nutr. 26, 2211-2230.
92. Senden, M. H. M. N., Verburg, A. J. G. M., van der Meer, T. G. and Wolterbeek, H. Th. (1995) Citric acid in tomato plant roots and its effect on cadmium uptake and distribution, Plant Soil 171, 333-39.
93. Sharma, S. S., Kaul, S., Metwally, A., Goyal, K. C., Finkemeyer, I. and Dietz, K.-J. (2004) Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status, Plant Science 166, 1287-1295.
94. Siedlecka, A. and Krupa, Z. (1996) Interaction between cadmium and iron and its effects on photosynthetic capacity of primary leaves of Phaseolus vulgaris, Plant Physiol. Biochem. 34, 833-841.
95. Siedlecka, A. and Krupa, Z. (1999) Cd/Fe interaction in higher plants -its consequences for the photosynthetic apparatus, Photosynthetica 36, 321-331.
96. Singh, O. V., Labana, S., Pandey, G., Budhiraja, R. and Jain, R. K. (2003) Phytoremediation: an overview of metallic ion decontamination from soil, Appl. Microbiol. Biotechnol. 61, 405-412.
97. Smith, R. M. and Martell, A. E. (1989) Critical Stability Constants, Vols. 1-6, Plenum Press, New York.
98. Srivastava, A. and Appenroth, K. J. (1995) Interaction of EDTA and iron on the accumulation of Cd2+ in duckweeds (Lemnaceae), J. Plant Physiol. 146, 173-176.
99. Strasser, O., Köhl, K. and Römheld, V. (1999) Overestimation of apoplastic Fe in roots of soil grown plants, Plant Soil 210, 179-187.
100. Tatár, E., Mihucz, V. G., Varga, A., Záray, Gy. and Fodor, F. (1998) Determination of organic acids in xylem sap of cucumber: effect of lead contamination, Microchem. J. 58, 306-314.
101. Thomine, S., Leliévre, F., Debarbieux, E., Schroeder, J I and Barbier-Brygoo, H. (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency, Plant J. 34, 685-695.
102. Thomine, S., Wang, R., Ward, J. M., Crawford, N. M. and Schroeder, J I (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes, P. Natl. Acad. Sci. USA 97, 4991-4996.
103. Tiffin, L O. (1966) Iron translocation: plant culture, exudates sampling, iron citrate analysis, Plant Physiol. 45, 280-283.
104. Vacchina, V., Mari, S., Czernic, P., Marques, L., Pianelli, K., Schaumlöffel, D., Lebrun, M. and Lobinski, R. (2003) Speciation of nickel in a hyperaccumulating plant by highperformance liquid chromatography- inductively coupled plasma mass spectrometry and electrospray MS/MS assisted by cloning using yeast complementation, Anal. Chem. 75, 2740-2745.
105. Varga, A., Martinez, R. M. G., Záray, Gy. and Fodor, F. (1999) Investigation of effects of cadmium, lead, nickel and vanadium contamination on the uptake and transport processes in cucumber plants by TXRF spectrometry, Spectrochim. Acta B. 54, 1455-1462.
106. Varga, A., Záray, Gy., Fodor, F. and Cseh, E. (1997) Study of interaction of iron and lead during their uptake process in wheat roots by total-reflection X-ray fluorescence spectrometry, Spectrochim. Acta B 52, 1027-1032.
107. Varga, A., Záray, Gy. and Fodor, F. (2000) Investigation of element distributions between the symplasm and apoplasm of cucumber plants by TXRF spectrometry, Microchem. J. 67, 257-264.
108. Varga, A., Záray, Gy. and Fodor, F. (2002) Determination of element distribution between the symplasm and apoplasm of cucumber plant parts by total reflection X-ray fluorescence spectrometry, J. Inorg. Biochem. 89, 149-154.
109. Vassil, A. D., Kapulnik, Y., Raskin, I. and and Salt, D. E. (1998) The role of EDTA in lead transport and accumulation by indian mustard, Plant Physiol. 117, 447-453.
110. Vázquez, M. D., Barceló, J., Poschenrieder, C., Mádico, J., Hatton, P., Baker, A. J. M. and Cope, G. H. (1992) Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metalophyte that can hyperaccumulate both metals, J. Plant Physiol. 140, 350-355.
111. Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M. L., Briat, J.-F. and Curie, C. (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth, Plant Cell 14, 1223-1233.
112. Von Wirén, N., Marschner, H. and Römheld, V. (1996) Roots of iron-efficient maize also absorb phytosyderophore-chelated zinc, J. Plant Physiol. 111, 1119-1125.
113. Von Wirén, N., Klair, S., Bansal, S., Briat, J.-F., Khodr, H., Shioiri, T., Leigh, R. A. and Hider, R. C. (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants, Plant Physiol. 119, 1107-1114.
114. Wallace, A., Wallace, G. A. and Cha, J. W. (1992) Some modifications in trace metal toxicities and deficiencies in plants resulting from interactions with other elements and chelating agents -the special case of iron, J. Plant Nutr. 15, 1589-1598.
115. White, P. J. (2001) The pathways of calcium movement to the xylem, J. Exp. Bot. 52, 891-899.
116. White, P. J., Whiting, S. N., Baker, A. J. M. and Broadley, M. R. (2002) Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens?, New Phytol. 153, 199-211.
117. Whiting, S. N., Broadley, M. R. and White, P. J. (2003) Applying a solute transfer model to phytoextraction: Zinc acquisition by Thlaspi caerulescens, Plant Soil 249, 45-56.
118. Yang, X., Baligar, V. C., Martens, D. C. and Clark, R. B. (1996) Plant tolerance to nickel toxicity: II Nickel effects on influx and transport of mineral nutrients in four plant species, J. Plant Nutr. 19, 265-279.
119. Yang, Y., Jung, J., Song, W., Suh, H. and Lee, Y. (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance, Plant Physiol. 124, 1019-1026.
120. 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.
121. Zhao, F.-J., Hamon, R. E., Lombi, E., McLaughlin, M. J. and McGrath, S. P. (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens, J. Exp. Bot. 53, 535-543.
122. Zhao, F.-J., Lombi, E., Breedon, T. and McGrath, S. P. (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri, Plant Cell Environ. 23, 507-514.