Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view

Plant, Cell and Environment

Volumn 31, Issue 1, 2008, Pages 123-143

  Ernst, Wilfried H O ^a   Krauss, Gerd Joachim ^b   Verkleij, Jos A C ^a   Wesenberg, Dirk ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Glucosinolates; Glutathione; Hypertolerance; Hypotolerance; Metallothionein; Phytochelatin; Zinc cadmium ratio

Indexed keywords

GLUCOSINOLATE; GLUTATHIONE; HEAVY METAL; METALLOTHIONEIN; SULFUR; VEGETABLE PROTEIN;

ANGIOSPERM; ECOLOGICAL APPROACH; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GENE EXPRESSION; HEAVY METAL; METABOLISM; SULFUR; TOLERANCE;

ANGIOSPERM; ARTICLE; CHEMISTRY; DRUG EFFECT; ECOSYSTEM; METABOLISM; SOIL POLLUTANT;

ANGIOSPERMS; ECOSYSTEM; GLUCOSINOLATES; GLUTATHIONE; METALLOTHIONEIN; METALS, HEAVY; PLANT PROTEINS; SOIL POLLUTANTS; SULFUR;

MAGNOLIOPHYTA;

EID: 36749090100     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2007.01746.x     Document Type: Article

References (285)

1. Adriaensen K., van der Lelie D., Van Laere A., Vangronsveld J. Colpaert J.V. (2004) A zinc-adapted fungus protects pines from zinc stress. New Phytologist 161, 549 555.
2. Ager F.J., Ynsa M.D., Domínguez-Solís J.R., López-Martín M.C., Gotor C. Romero L.C. (2003) Nuclear micro-probe analysis of Arabidopsis thaliana leaves. Nuclear Instruments and Methods in Physics Research B 210, 401 406.
3. Ahmad A., Khan I., Anjum N.A., Abrol Y.P. Iqbal M. (2005) Role of sulphate transporter systems in sulphur efficiency of mustard genotypes. Plant Science 169, 842 846.
4. Andersen M.K., Raulund-Rasmussen K., Strobel B.W. Hansen H.C.B. (2004) The effects of tree species and site on the solubility of Cd, Cu, Ni, Pb and Zn in soils. Water, Air, & Soil Pollution 154, 357 370.
5. Armengaud P., Breitling R. Amtmann A. (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiology 136, 2556 2576.
6. Arrivault S., Senger T. Krämer U. (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant Journal 46, 861 879.
7. Artetxe U., Garcia-Plazaola J.I., Hernandez A. Becerril J.M. (2002) Low light grown duckweed plants are more protected against the toxicity induced by Zn and Cd. Plant Physiology and Biochemistry 40, 859 863.
8. Assunção A.G.L., Ten Bookum W.M., Nelissen H.J.M., Vooijs R., Schat H. Ernst W.H.O. (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159, 411 419.
9. Assunção A.G.L., Ten Bookum W.M., Nelissen H.J.M., Vooijs R., Schat H. Ernst W.H.O. (2003b) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytologist 159, 383 390.
10. Ayalon O., Nishri A. Avnimelech Y. (1991) Distribution of soluble iron and zinc in leachates of municipal wastes. In Iron Nutrition and Interactions in Plants (eds Y. Chen Y. Hadar pp. 53 56. Kluwer Academic Publishers, Dordrecht, the Netherlands.
11. Baker A.J.M. Brooks R.R. (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1, 81 126.
12. Barceló J. Poschenrieder C. (1990) Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13, 1 37.
13. Beck A., Lendzian K., Oven M., Christmann A. Grill E. (2003) Phytochelatin synthase catalyzes key step in turnover of glutathione conjugates. Phytochemistry 62, 423 431.
14. Belimov A.A., Hontzeas N., Safronova V.I., Demchinskaya S.V., Piluza G., Bullitta S. Glick B.R. (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biology & Biochemistry 37, 241 250.
15. van Belleghem F., Cuypers A., Semane B., Smeets K., Vangronsveld J., Haen J. Valcke R. (2007) Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytologist 173, 495 508.
16. Bernard C., Roosens N., Czernic P., Lebrun M. Verbruggen N. (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Letters 569, 140 148.
17. Bert V., Macnair M.R., DeLaguerie P., Saumitou-Laprade P. Petit D. (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytologist 146, 225 233.
18. Bert V., Meerts P., Saumitou-Laprade P., Salis P., Gruber W. Verbruggen N. (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant and Soil 249, 9 18.
19. Bhattacharya P., Welch A.H., Stollenwerk K.G., McLaughlin M., Bundschuh J. Panaullah G. (2007) Arsenic in the environment: biology and chemistry. Science of the Total Environment 379, 109 120.
20. Bleeker P.M., Hakvoort H.W.J., Bliek M., Souer E. Schat H. (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant Journal 45, 917 929.
21. Blum R., Beck A., Korte A., Stengel A., Letzel T., Lendzian K. Grill E. (2007) Function of phytochelatin synthase in catabolism of glutathione- conjugates. Plant Journal 49, 740 749.
22. Bogs J., Bourbouloux A., Cagnac O., Wachter A., Rausch T. Delrot S. (2003) Functional characterization and expression analysis of a glutathione transporter, BjGT1, from Brassica juncea: evidence for regulation by heavy metal exposure. Plant, Cell & Environment 26, 1703 1711.
23. Boominathan R. Doran P.M. (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnology & Bioengineering 83, 158 167.
24. Bovet L., Eggmann T., Meylan-Bettex M., Polier J., Kammer P., Marin E., Feller U. Martinoia E. (2003) Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant, Cell & Environment 26, 371 378.
25. Bowen G.D., Skinner M.F. Bevege D.I. (1974) Zinc uptake by mycorrhizal and uninfected roots of Pinus radiata and Araucaria cunninghamii. Soil Biology & Biochemistry 6, 141 144.
26. Bradley R., Burt A.J. Read D.J. (1981) Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature 292, 335 337.
27. Bradshaw A.D. (1952) Populations of Agrostis tenuis resistant to lead and zinc poisoning. Nature 169, 1098.
28. Broadley M.R., White P.J., Hammond J.P., Zelko I. Lux A. (2007) Zinc in plants. New Phytologist 173, 677 702.
29. Brown M.T. Wilkins D.A. (1985) Zinc tolerance of mycorrhizal Betula. New Phytologist 99, 101 106.
30. Brune A., Urbach W. Dietz K.J. (1995) Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: a comparison of Cd-, Mo-, Ni- and Zn-stress. New Phytologist 129, 403 409.
31. Carol R.J. Dolan L. (2002) Building a hair. Tip growth in Arabidopsis thaliana root hairs. Philosophical Transactions: Biological Sciences 357, 815 821.
32. Cazalé A.C. Clemens S. (2001) Arabidopsis thaliana expresses a second functional phytochelatin synthase. FEBS Letters 507, 215 219.
33. Chaney R.L., Malik M., Li Y.M., Brown S.L., Brewer E.P., Angle J.S. Baker A.J.M. (1997) Phytoremediation of soil metals. Current Opinion in Biotechnology 8, 279 284.
34. Chang T., Liu X., Xu H., Meng K., Chen S. Zhu Z. (2004) A metallothionein-like gene htMT2 strongly expressed in internodes and nodes of Helianthus tuberosus and effects of metal ion treatment on its expression. Planta 218, 449 455.
35. Chardonnens A.N., Ten Bookum W.M., Kuijper L.D.J., Verkleij J.A.C Ernst W.H.O. (1998) Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. Physiologia Plantarum 104, 75 80.
36. Chen A., Komives E.A. Schroeder J.I. (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiology 141, 108 120.
37. Chen J., Zhou J. Goldsbrough P.B. (1997) Characterization of phytochelatin synthase from tomato. Physiologia Plantarum 101, 165 172.
38. Chen M., Ma L.Q. Harris W.G. (2002) Arsenic concentration in Florida surface soils. Soil Science Society of America Journai 66, 632 640.
39. Chiang H.C., Lo J.C. Yeh K.C. (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environmental Science & Technology 40, 6792 6798.
40. Clemens S. (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212, 475 486.
41. Clemens S. (2006a) Evolution and function of phytochelatin synthases. Journal of Plant Physiology 163, 319 332.
42. Clemens S. (2006b) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707 1719.
43. Clemens S., Simm C. Maier T. (2003) Heavy metal-binding proteins and peptides. In Polyamides and Complex Proteinaceous Materials II (eds S. Fahnestock A. Steinbüchel pp. 255 288. Wiley-VCH, Weinheim, Germany.
44. Cobbett C. (2003a) Heavy metals and plants - model systems and hyperaccumulators. New Phytologist 159, 289 293.
45. Cobbett C.S. (2003b) Metallothioneins and phytochelatins: molecular aspects. In Sulphur in Plants (ed. A. Ahmad pp. 177 188. Kluwer Academic Publishers, Dordrecht, the Netherlands.
46. Cobbett C.S., May M.J., Howden R. Rolls B. (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant Journal 16, 73 78.
47. Cohen C.K., Garvin D.F. Kochian L.V. (2004) Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 218, 784 792.
48. Coleman C.M., Boyd R.S. Eubanks M.D. (2005) Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. Journal of Chemical Ecology 31, 1669 1681.
49. Coolong T.W., Randle W.M., Toler H.D. Sams C.E. (2004) Zinc availability in hydroponic culture influences glucosinolate concentrations in Brassica rapa. HortScience 39, 84 86.
50. Cosio C., Martinoia E. Keller C. (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology 134, 716 725.
51. 3Gly assisted multivariate curve solution. Environmental Science & Technology 39, 778 786.
52. Davis M.A. Boyd R.S. (2000) Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae). New Phytologist 146, 211 217.
53. De Knecht J.A. (1994) Cadmium tolerance and phytochelatin production in Silene vulgaris. PhD thesis, Vrije Universiteit, Amsterdam, the Netherlands.
54. De Knecht J.A., Koevoets P.L.M., Verkleij J.A.C. Ernst W.H.O. (1992) Evidence against a role for phytochelatins in naturally selected increased cadmium tolerance in Silene vulgaris (Moench) Garcke. New Phytologist 122, 681 688.
55. De Knecht J.A., van Dillen M., Koevoets P., Schat H., Verkleij J. Ernst W.H.O. (1994) Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris (chain length distribution and sulfide incorporation). Plant Physiology 104, 255 261.
56. De Knecht J.A., van Baren N., Bookum T.W.M., Wong Fong Sang H.W., Koevoets P.L.M., Schat H. Verkleij J.A.C. (1995) Synthesis and degradation of phytochelatins in cadmium sensitive and cadmium-tolerant Silene vulgaris. Plant Science 106, 9 18.
57. De Vos C.H.R., Vooijs R., Schat H. Ernst W.H.O. (1989) Copper-induced damage to the permeability barrier in roots of Silene cucubalus. Journal of Plant Physiology 135, 165 169.
58. De Vos C.H.R., Vonk M.J., Vooijs R. Schat H. (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiology 98, 853 858.
59. De Vos C.H.R., Ten Bookum W.M., Vooijs R., Schat H. De Kok L.J. (1993) Effect of copper on fatty acid composition and peroxidation of lipids in the roots of copper tolerant and sensitive Silene cucubalus. Plant Physiology and Biochemistry 31, 151 158.
60. Domènech J., Mir G., Huguet G., Capdevila M., Molinas M. Atrian S. (2006) Plant metallothionein domains: functional insight into physiological metal binding and protein folding. Biochimie 88, 583 593.
61. Domínguez-Solís J.R., López-Martín M.C., Ager F.J., Ynsa M.D., Romero L.C. Gotor C. (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotechnology Journal 2, 469 476.
62. Ducruix C., Junot C., Fievet J.B., Villiers F., Ezan E. Bourguignon J. (2006) New insights into the regulation of phytochelatin biosynthesis in A. thaliana cells from metabolite profiling analyses. Biochemie 88, 1733 1742.
63. Ebbs S., Lau I., Ahner B. Kochian L. (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214, 635 640.
64. Eriksen J., Murphy M.D. Schnug E. (1998) The soil sulphur cycle. In Sulphur in Agroecosystems (ed. E. Schnug pp. 39 73. Kluwer Academic Publishers, Dordrecht, the Netherlands.
65. Ernst W. (1974) Schwermetallvegetation der Erde. Fischer Verlag, Stuttgart, Germany.
66. Ernst W.H.O. (1997) Life-history syndromes and the ecology of plants from high sulphur-habitats. In Sulphur Metabolism in Higher Plants. Molecular, Ecophysiological and Nutritional Aspects (eds W.J. Cram, L.J. De Kok, I. Stulen, C. Brunold H. Rennenberg pp. 131 146. Backhuys Publishers, Leiden, the Netherlands.
67. Ernst W.H.O. (1999) Biomarkers in plants. In Biomarkers: A Pragmatic Basis for Remediation of Severe Pollution in Eastern Europe (eds D.B. Peakall, C.H. Walker P. Migula pp. 135 151. Kluwer Academic Publishers, Dordrecht, the Netherlands.
68. Ernst W.H.O. (2000) Agricultural aspects of sulfur. In Environmental Technologies to Treat Sulfur Pollution (eds P. Lens L.H. Pol pp. 355 376. IWA Publishing, London, England.
69. Ernst W.H.O. (2005) Phytoextraction of mine wastes - options and impossibilities. Chemie der Erde-Geochemistry 65, 29 42.
70. Ernst W.H.O. (2006) Evolution of metal tolerance in higher plants. Forest Snow and Landscape Research 80, 251 274.
71. Ernst W.H.O. Nelissen H.J.M. (2000) Life-cycle phases of a zinc- and cadmium-resistant ecotype of Silene vulgaris in risk assessment of polymetallic mine soils. Environmental Pollution 107, 329 338.
72. Ernst W.H.O., Verkleij J.A.C. Schat H. (1992) Metal tolerance in plants. Acta Botanica Neerlandica 41, 229 248.
73. Ernst W.H.O., Nelissen H.J.M. Ten Bookum W.M. (2000) Combination toxicology of metal-enriched soils: physiological responses of a Zn- and Cd-resistant ecotype of Silene vulgaris on polymetallic soils. Environmental and Experimental Botany 43, 55 71.
74. Falk K.L., Tokuhisa J.G. Gershenzon J. (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biology 9, 573 581.
75. Finkemeier I., Kluge C., Metwally A., Georgi M., Grotjohann N. Dietz K.J. (2003) Alterations in Cd-induced gene expression under nitrogen deficiency in Hordeum vulgare. Plant, Cell & Environment 26, 821 833.
76. Foley R.C., Liang Z.M. Singh K.B. (1997) Analysis of type 1 metallothionein cDNAs in Vicia faba. Plant Molecular Biology 33, 583 591.
77. Freeman J.L., Persans M.W., Nieman K., Albrecht C., Peer W., Pickering I.J. Salt D.E. (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16, 2176 2191.
78. Gadapati W.R. Macfie S.M. (2006) Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Science 170, 471 480.
79. Gamborg O.L., Miller R.A. Ojima K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research 50, 151 158.
80. Garcia-Hernandez M., Murphy A. Taiz L. (1998) Metallothioneins 1 and 2 have distinct but overlapping expression patterns in Arabidopsis. Plant Physiology 118, 387 397.
81. Gasic K. Korban S.S. (2007) Expression of Arabidopsis phytochelatin synthase in Indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta 225, 1277 1285.
82. Gawel J.E. Hemond H.F. (2004) Biomonitoring for metal contamination near two Superfund sites in Woburn, Massachusetts, using phytochelatins. Environmental Pollution 131, 125 135.
83. Gawel J.E., Trick C.G. Morel F.M.M. (2001) Phytochelatins are bioindicators of atmospheric metal exposure via direct foliar uptake in trees near Sudbury, Ontario, Canada. Environmental Science & Technology 35, 2108 2113.
84. Gibson B.R. Mitchell D.T. (2006) Sensitivity of ericoid mycorrhizal fungi and mycorrhizal Calluna vulgaris to copper mine spoil from Avoca, County Wicklow. Proceedings of the Royal Irish Academy: Biology and Environment 106, 9 18.
85. Göhre V. Paszkowski U. (2006) Contribution of the arbuscular mycorrhizal symbionts to heavy metal phytoremediation. Planta 223, 1115 1122.
86. Gong J.M., Lee D.A. Schroeder J.I. (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 100, 10118 10123.
87. Gratao P.L., Polle A., Lea P. Azevedo R.A. (2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology 32, 481 494.
88. Gray N.F. (1996) Field assessment of acid mine drainage contamination in surface and ground water. Environmental Geology 27, 358 361.
89. Grill E., Winnacker E.L. Zenk M.H. (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230, 674 676.
90. Grill E., Gekeler W., Winnacker E.L. Zenk H.H. (1986) Homo-phytochelatins are heavy metal-binding peptides of homo-glutathione containing Fabales. FEBS Letters 205, 47 50.
91. Grill E., Winnacker E.L. Zenk M.H. (1988) Occurrence of heavy metal binding phytochelatins in plants growing in a mining refuse area. Experientia 44, 539 540.
92. Grill E., Loeffler S., Winnacker E.L. Zenk M.H. (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proceedings of the National Academy of Sciences of the United States of America 86, 6838 6842.
93. Grzam A., Tennstedt P., Clemens S., Hell R. Meyer A.J. (2006) Vacuolar sequestration of glutathione S-conjugates outcompetes a possible degradation of the glutathione moiety by phytochelatin synthase. FEBS Letters 580, 6384 6390.
94. Guo W.-J., Bundithya W. Goldsbrough P.B. (2003) Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytologist 159, 369 381.
95. Gupta S.C. Goldsbrough P.B. (1991) Phytochelatin accumulation and cadmium tolerance in selected tomato cell-lines. Plant Physiology 97, 306 312.
96. Gupta D.K., Tohoyama H., Joho M. Inouhe M. (2002) Possible roles of phytochelatins and glutathione metabolism in cadmium tolerance in chickpea roots. Journal of Plant Research 115, 429 437.
97. Haines B.J. (2002) Zincophilic root foraging in Thlaspi caerulescens. New Phytologist 155, 363 372.
98. Halkier B.A. Gershenzon J. (2006) Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57, 303 333.
99. Hall J.C. (2002) Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany 53, 1 11.
100. Hammond J.P., Bowen H.C., White J.P., Mills V., Pyke K.A., Baker A.J.M., Whiting S.N., May S.T. Broadley M.R. (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytologist 170, 239 260.
101. Haneklaus S., Bloem E. Schnug E. (2003) The global sulphur cycle and its links to plant environment. In Sulphur in Plants (eds Y.P. Abrol A. Ahmad pp. 1 28. Kluwer Academic Publishers, Dordrecht, the Netherlands.
102. Harada E., Yamaguchi Y., Koizumi N. Hiroshi S. (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. Journal of Plant Physiology 159, 445 448.
103. Harmens H., Den Hartog P.R., Ten Bookum W.M. Verkleij J.A.C. (1993) Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins. Plant Physiology 103, 1305 1309.
104. Hart J.J., Welch R.M., Norvell W.A. Kochian L.V. (2002) Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiologia Plantarum 116, 73 78.
105. Hart J.J., Welch R.M., Norvell W.A. Kochian L.V. (2006) Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytologist 172, 261 271.
106. Hartley-Whitaker J., Ainsworth G. Meharg A.A. (2001a) Copper- and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant, Cell & Environment 24, 713 722.
107. Hartley-Whitaker J., Ainsworth G., Vooijs R., Ten Bookum W.M., Schat H. Meharg A.A. (2001b) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiology 126, 299 306.
108. Hassinen V.H., Tervahauta A.L., Halimaa P., Plessl M., Peräniemi S., Schat H., Aarts M.G.M., Servomaa K. Kärenlampi S.O. (2007) Isolation of Zn-responsive genes from two accessions of the hyperaccumulator plant Thlaspi caerulescens. Planta 225, 977 989.
109. Hawkesford M.J. (2003) Transporter gene families in plants: the sulphate transporter gene family - redundancy or specialization? Physiologia Plantarum 117, 155 163.
110. Hawkesford M.J. De Kok L.J. (2006) Managing sulphur metabolism in plants. Plant, Cell & Environment 29, 382 395.
111. Heckathorn S.A., Mueller J.K., LaGuidice S., Zhu B., Barrett T., Blair B. Dong Y. (2004) Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. American Journal of Botany 91, 1312 1318.
112. Heise J., Krejci S., Miersch J., Krauss G.J. Humbeck K. (2007) Gene expression of metallothioneins in barley during senescence and heavy metal treatment. Crop Science 47, 1111 1118.
113. Heiss S., Schafer H.J., Haag-Kerwer A. Rausch T. (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Molecular Biology 39, 847 857.
114. Heiss S., Wachter A., Bogs J., Cobbett C. Rausch T. (2003) Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure. Journal of Experimental Botany 54, 1833 1839.
115. Hepper C. (1986) Growth of hyphae from Glomus spores in the presence of sulphur. New Phytologist 93, 537 542.
116. Herbette S., Taconnat L., Hugouvieux V., et al 2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88, 1751 1765.
117. Hernández-Allica J., Garbisu C., Becerril J.M., Barrutia O., Garcia-Plazaola J.I., Zhao F.J. McGrath S.P. (2006) Synthesis of low molecular weight thiols in response to Cd exposure in Thlaspi caerulescens. Plant, Cell & Environment 29, 1422 1429.
118. Hildebrandt U., Regvar M. Bothe H. (2006) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68, 139 146.
119. Hill K.A., Lion L.W. Ahner B.A. (2002) Reduced Cd accumulation in Zea mays: a protective role for phytosiderophore? Environmental Science & Technology 36, 5363 5368.
120. Hirata K., Tsuji N. Miyamoto K. (2005) Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. Journal of Bioscience and Bioengineering 100, 593 599.
121. Hoagland D.R. Arnon I. (1950) The water culture method for growing plants without soil. California Agriculture Experimental Station Berkeley Circular 347, 1 32.
122. van Hoof N.A., Koevoets P.L., Hakvoort H.W., Ten Bookum W.M., Schat H., Verkleij J.A. Ernst W.H.O. (2001a) Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper-tolerant Silene vulgaris. Physiologia Plantarum 113, 225 232.
123. van Hoof N.A.L., Hassinen V.H., Hakvoort H.W.J., Ballintijn K.F., Schat H., Verkleij J.A.C., Ernst W.H.O., Karenlampi S.O. Tervahauta A.I. (2001b) Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiology 126, 1519 1526.
124. Howarth J.R., Domínguez-Solís J.R., Gutiérrez- Alcalá G., Wray J.L., Romero L.C. Gotor C. (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Molecular Biology 51, 589 598.
125. Howden R. Cobbett C.S. (1992) Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiology 99, 100 107.
126. Howden R., Andersen C.R., Goldsbrough P.B. Cobbett C.S. (1995a) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiology 107, 1067 1073.
127. Howden R., Goldsbrough P.B., Andersen C.R. Cobbett C.S. (1995b) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiology 107, 1059 1066.
128. Inouhe M. (2005) Phytochelatins. Brasilian Journal of Plant Physiology 17, 65 78.
129. Inouhe M., Ninomiya S., Tohoyama H., Joho M. Murayama T. (1994) Different characteristics of roots in the cadmium-tolerance and Cd-binding complex formation between mono- and dicotyledonous plants. Journal of Plant Research 107, 201 207.
130. Inouhe M., Ito R., Ito S., Sasada N., Tohoyama H. Joho M. (2000) Azuki bean cells are hypersensitive to cadmium and do not synthesize phytochelatins. Plant Physiology 123, 1029 1036.
131. Isaure M.P., Fayard B., Sarret G., Pairis S. Bourguignon J. (2006) Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochimica Acta Part B: Atomic Spectroscopy 81, 1242 1252.
132. Jemal F., Didierjean L., Ghrir R., Ghorbal M.H. Burkard G. (1998) Characterization of cadmium binding peptides from pepper (Capsicum annuum). Plant Science 137, 143 154.
133. Jones M.D. Hutchinson T.C. (1988) Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. 2. Uptake of nickel, calcium, magnesium phosphorus and iron. New Phytologist 108, 461 470.
134. Kerkeb L. Krämer U. (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiology 131, 716 724.
135. Klapheck S., Fliegner W. Zimmer I. (1994) Hydroxymethyl-phytochelatins [(γ-glutamylcysteine)n-serine] are metal-induced peptides of the Poaceae. Plant Physiology 104, 1325 1332.
136. Klapheck S., Schlunz S. Bergmann L. (1995) Synthesis of phytochelatins and homo-phytochelatins in Pisum sativum L. Plant Physiology 107, 515 521.
137. Kneer R. Zenk M.H. (1997) The formation of Cd-phytochelatin complexes in plant cell cultures. Phytochemistry 44, 69 74.
138. Knop W. (1865) Quantitative Untersuchungen über die Ernährungsprocesse der Pflanzen. Das Landwirtschaftliche Versuchswesen und die Tätigkeit der landwirtschaftlichen Versuchsstationen Preussens (einschließlich der Tierseuchen- und Pflanzenschutzstellen) im Auftrag des Herrn Ministers für Landwirtschaft, Domänen und Forsten 7, 93 107.
139. Kohler A., Blaudez D., Chalot M. Martin F. (2004) Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytologist 164, 83 93.
140. Kovalchuk I., Titov V., Hohn B. Kovalchuk O. (2005) Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutation Research, Fundamental and Molecular Mechanisms of Mutagenesis 570, 149 161.
141. Krämer U. Clemens S. (2006) Functions and homeostasis of zinc, copper, and nickel in plants. In Metal Homeostasis and Detoxification. From Microbes to Man (eds M.J. Tamás E. Martinoia pp. 215 271. Springer, Berlin, Germany.
142. Krämer U., Pickering I.J., Prince R.C., Raskin I. Salt D.E. (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiology 122, 1343 1354.
143. Krupa Z., Öquist G. Huner N.P.A. (1993) The effects of cadmium on photosynthesis of Phaseolus vulgaris- a fluorescence analysis. Physiologia Plantarum 88, 626 630.
144. Lahner B., Gong J., Mahmoudian M., et al 2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nature Biotechnology 21, 1215 1221.
145. Landberg T. Greger M. (2002) Differences in oxidative stress in heavy metal resistant and sensitive clones of Salix viminalis. Journal of Plant Physiology 159, 69 75.
146. 2+ and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana. Journal of Experimental Botany 53, 447 453.
147. Lee D.A., Chen A. Schroeder J.I. (2003) ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant Journal 35, 637 646.
148. Lee J., Shim D., Song W.Y., Hwang I. Lee Y. (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Molecular Biology 54, 805 815.
149. Lee S.M. Kang B.S. (2005) Phytochelatin is not a primary factor in determining copper tolerance. Journal of Plant Biology 48, 32 38.
150. Lee S. Korban S.S. (2002) Transcriptional regulation of Arabidopsis thaliana phytochelatin synthase (AtPCS1) by cadmium during early stages of plant development. Planta 215, 689 693.
151. Lee S., Moon J.S., Domier L.L. Korban S.S. (2002) Molecular characterization of phytochelatin synthase expression in transgenic Arabidopsis. Plant Physiology and Biochemistry 40, 727 733.
152. Lee S., Moon J.S., Ko T.-S., Petros D., Goldsbrough P.B. Korban S.S. (2003a) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiology 131, 656 663.
153. Lee S., Petros D., Moon J.S., Ko T.-S., Goldsbrough P.B. Korban S.S. (2003b) Higher levels of ectopic expression of Arabidopsis phytochelatin synthase do not lead to increased cadmium tolerance and accumulation. Plant Physiology and Biochemistry 41, 903 910.
154. Lee T.M., Lai H.Y. Chen Z.S. (2004) Chemical amendments effect on the cadmium bioavailability of contaminated soils in Taiwan. Chemosphere 57, 1459 1471.
155. Li J., Guo J., Xu W. Ma M. (2006a) Enhanced cadmium accumulation in transgenic tobacco expressing the phytochelatin synthase gene of Cynodon dactylon L. Journal of Integrative Plant Biology 48, 928 937.
156. Li Y.J., Dhankher O.P., Carreira L., Lee D., Chen A., Schroeder J.I., Balish R.S. Meagher R.B. (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant & Cell Physiology 45, 1787 1797.
157. Li Y.J., Dankher O.P., Carreira L., Smith A.P. Meagher R.B. (2006b) The shoot-specific expression of gamma-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiology 141, 288 298.
158. Lindblom S.D., Abdel-Ghany S., Hanson B.R., Hwang S.B., Terry N. Pilon-Smits E.A.H. (2006) Constitutive expression of a high-affinity sulfate transporter in Indian mustard affects metal tolerance and accumulation. Journal of Environmental Quality 35, 726 733.
159. Loeffler S., Hochberger A., Grill E., Winnacker E.-L. Zenk M.H. (1989) Termination of the phytochelatin synthase reaction through sequestration of heavy metals by the reaction product. FEBS Letters 258, 42 46.
160. Lombi E., Tearall K.L., Howarth J.R., Zhao F.-J., Hawkesford M.J. McGrath S.P. (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiology 128, 1359 1367.
161. Loscos J., Naya L., Ramos J., Clemente M.R., Matamoros M.A. Becana M. (2006) A reassessment of substrate specificity and activation of phytochelatin synthases from model plants by physiologically relevant metals. Plant Physiology 140, 1213 1221.
162. Ma M., Lau P.-S., Jia Y.-T., Tsang W.-K., Lam S.K.S., Tam N.F.Y Wong Y.-S. (2003) The isolation and characterization of type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra cv. Merlin. Plant Science 164, 51 60.
163. McClendon J.H. (1999) The origin of life. Earth Science Reviews 47, 71 93.
164. McGrath S.P., Knight B., Killham K., Preston S. Paton G.I. (1999) Assessment of the toxicity of metals in soils amended with sewage sludge using a chemical speciation technique and a lux-based biosensor. Environmental Toxicology and Chemistry 18, 659 663.
165. McKenna I.M., Chaney R.L. Williams F.M. (1993) The effects of cadmium and zinc interactions on the accumulation and tissue distribution of zinc and cadmium in lettuce and spinach. Environmental Pollution 79, 113 120.
166. McMahon P.J. Anderson J.W. (1998) Preferential allocation of sulphur into γ-glutamylcysteinyl peptides in wheat plants grown at low sulphur nutrition in the presence of cadmium. Physiologia Plantarum 104, 440 448.
167. Macnair M.R., Bert V., Huitson S.B., Saumitou-Laprade P. Petit D. (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proceedings of the Royal Society of London B: Biological Sciences 266, 2175 2179.
168. Maksymiec W. Krupa Z. (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environmental and Experimental Botany 57, 187 194.
169. Mansouri-Bauly H., Kruse J., Sýkorová Z., Scheerer U. Kopriva S. (2006) Sulfur uptake in the ectomycorrhizal fungus Laccaria bicolor S238 N. Mycorrhiza 16, 4210 4427.
170. Mari S. Lebrun M. (2006) Metal immobilization: where and how? In Molecular Biology of Metal Homeostasis and Detoxification. From Microbe to Man (eds M.J. Tamas E. Martinoia pp. 274 298. Springer, Berlin, Germany.
171. Marschner H. (1995) Mineral Nutrition of Higher Plants, 2nd edn, Academic Press, London, England.
172. Maruyama-Nakashita A., Nakamura Y., Yamaya T. Takahashi H. (2004) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. Journal of Experimental Botany 55, 1843 1849.
173. Mathys W. (1975) Enzymes of heavy metal-resistant and non-resistant populations of Silene cucubalus and their interaction with some heavy metals in vitro and in vivo. Physiologia Plantarum 33, 161 165.
174. May M.J., Vernoux T., Sanchez-Fernandez R., Van Montagu M. Inze D. (1998) Evidence for posttranscriptional activation of γ-glutamylcysteine synthetase during plant stress responses. Proceedings of the National Academy of Sciences of the United States of America 95, 12049 12054.
175. Meda A.R., Scheuermann E.B., Prechsl U.E., Erenoglu B., Schaaf G., Hayen H., Weber G. von Wirén N. (2007) Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiology 143, 1761 1773.
176. Meerts P. Isacker N.V. (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecology 133, 221 231.
177. Meharg A.A. Hartley-Whitaker J. (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytologist 154, 29 43.
178. Mendoza-Cózatl D.G. Moreno-Sánchez R. (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modelling for plants. Journal of Theoretical Biology 238, 919 936.
179. Mendoza-Cózatl D., Loza-Tavera H., Hernández-Navarro A. Moreno-Sánchez R. (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiology Reviews 29, 653 671.
180. Mengoni A., Gonnelli C., Hakvoort H.W.J., Galardi F., Bazzicalupo M., Gabbrielli R. Schat H. (2003) Evolution of copper-tolerance and increased expression of a 2b-type metallothionein gene in Silene paradoxa L. populations. Plant and Soil 257, 451 457.
181. Mesjasz-Przybylowicz J., Grodzinska K., Przybylowicz W.J., Godzik B. Szarek-Lukaszewska G. (1999) Micro-PIXE studies of elemental distribution in seeds of Silene vulgaris from a zinc-dump in Olkusz, southern Poland. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 158, 306 331.
182. Mir G., Domènech J., Huguet G., Guo W.J., Goldsbrough P., Atrian S. Molinas M. (2004) A plant type 2 metallothionein (MT) from cork tissue responds to oxidative stress. Journal of Experimental Botany 55, 2483 2493.
183. Murashige T. Skoog F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473 497.
184. Murphy A. Taiz L. (1995) Comparison of metallothionein gene expression and nonprotein thiols in ten Arabidopsis ecotypes (correlation with copper tolerance). Plant Physiology 109, 945 954.
185. Murphy A. Taiz L. (1997) Correlation between potassium efflux and copper sensitivity in 10 Arabidopsis ecotypes. New Phytologist 136, 211 222.
186. + from Arabidopsis seedlings is mediated by ion channels and coupled citrate efflux. Plant Physiology 121, 1375 1382.
187. 2+ transporters OsIRT1 and OsIRT2 in rice. Soil Science & Plant Nutrition 52, 464 469.
188. Nikiforova V., Freitag J., Kempa S., Adamik M., Hesse H. Hoefgen R. (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant Journal 33, 633 650.
189. Nocito F.F., Lancilli C., Crema B., Fourcroy P., Davidian J.C. Sacchi G.A. (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiology 141, 1138 1148.
190. Noctor G. (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant, Cell & Environment 29, 409 425.
191. Noret N., Meerts P., Tolra R., Poschenrieder C., Barceló J. Escarré J. (2005) Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytologist 165, 763 772.
192. Noret N., Meerts P., Vanhaelen M., Dos Santos A. Escarré J. (2007) Do metal-rich plants deter herbivores? A field test of the defence hypothesis. Oecologia 152, 92 100.
193. Nussbaum S., Schmutz D. Brunold C. (1988) Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. Plant Physiology 88, 1407 1410.
194. Oven M., Grill E., Golan-Goldhirsh A., Kutchan T.M. Zenk M.H. (2002) Increase of free cysteine and citric acid in plant cells exposed to cobalt ions. Phytochemistry 60, 467 474.
195. Pajuelo E., Corrasco J.A., Romero L.C., Chamber M.A. Gotor C. (2007) Evaluation of the metal phytoextraction potential of crop legumes. Regulation of the expression of O-acetylserine (thiol)lyase under metal stress. Plant Biology 9, 672 681.
196. 2+ status effects on root and shoot heavy metal accumulation in Thlaspi caerulescens. New Phytologist 175, 51 58.
197. Peer W.A., Baxter I.R., Richards E.L., Freeman J.L. Murphy A.S. (2006) Phytoremediation and hyperaccumulator plants. In Molecular Biology of Metal Homeostasis and Detoxification. From Microbe to Man (eds M.J. Tamas E. Martinoia pp. 299 340. Springer, Berlin, Germany.
198. Pence N.S., Larsen P.B., Ebbs S.D., Letham D.L.D., Lasat M.M., Garvin D.F., Eide D. Kochian L.V. (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America 97, 4956 4960.
199. Pereira G.J.G., Molina S.M.G., Lea P.J. Azevedo R.A. (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant and Soil 239, 123 132.
200. Perfus-Barbeoch L., Leonhardt N., Vavasseur A. Forestier C. (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant Journal 32, 539 548.
201. Peroza E.A. Freisinger E. (2007) Metal ion binding properties of Triticum aestivum E(c)-1 metallothionein: evidence supporting two separate metal thiolate clusters. Journal of Biological Inorganic Chemistry 12, 377 391.
202. Peterson A.G. Oliver D.J. (2006) Leaf-targeted phytochelatin synthase in Arabidopsis thaliana. Plant Physiology and Biochemistry 44, 885 892.
203. Picault N., Cazalé A.C., Beyly A., Cuine S., Carrier P., Luu D.T., Forestier C. Peltier G. (2006) Chloroplast targeting of phytochelatin synthase in Arabidopsis: effects on heavy metal tolerance and accumulation. Biochimie 88, 1743 1750.
204. Piechalak A., Tomaszewska B., Baralkiewicz D. Malecka A. (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60, 153 162.
205. Podar D., Ramsey M.H. Hutchings M.J. (2004) Effect of cadmium, zinc and substrate heterogeneity on yield, shoot metal concentration and metal uptake by Brassica juncea: implications for human health risk assessment and phytoremediation. New Phytologist 163, 313 324.
206. 2+ tolerance and accumulation but not translocation to the shoot. Planta 223, 180 190.
207. Prat S. (1934) Heredibility of copper resistance (in German). Berichte der Deutschen Botanischen Gesellschaft 52, 65 67.
208. Psaras G.K., Constantinidis T., Cotsopoulos B. Manetas Y. (2000) Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Annals of Botany 86, 73 78.
209. Raab A., Feldmann J. Meharg A.A. (2004) The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiology 134, 1113 1122.
210. Ramos J., Clemente M.R., Naya L., Loscos J., Pérez-Rontomé C., Sato S., Tabata S. Becana M. (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiology 143, 1110 1118.
211. Rauser W.E. (1987) Changes in glutathione content of maize seedlings exposed to cadmium. Plant Science 51, 171 179.
212. Rauser W.E. (1999) Structure and function of metal chelators produced by plants. Cell Biochemistry and Biophysics 31, 19 48.
213. Rauser W.E. (2003) Phytochelatin-based complexes bind various amounts of cadmium in maize seedlings depending on the time of exposure, the concentration of cadmium and the tissue. New Phytologist 158, 269 278.
214. Rauser W.E. Meuwly P. (1995) Retention of cadmium in roots of maize seedlings. Plant Physiology 109, 195 202.
215. Rennenberg H. (2001) Glutathione - an ancient metabolite with modern tasks. In Significance of Glutathione to Plant Adaptation to the Environment (eds D. Grill, M. Tausz L.J. De Kok pp. 1 11. Kluwer Academic Publishers, Dordrecht, the Netherlands.
216. Rennenberg H., Schmitz K. Bergmann L. (1979) Long-distance transport of sulfur in Nicotiana tabacum. Planta 147, 57 62.
217. Rice C.M., Ahcroft W.A., Batten D.J., et al 1995) A Devonian auriferous hot-spring system, Rhynie, Scotland. Journal of the Geological Society 152, 229 250.
218. Rivera-Becerril F., Van Tuinen D., Gianinazzi S., Gianinazzi-Pearson V., Martin-Laurent F., Metwally A. Dietz K.-J. (2005) Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16, 51 60.
219. Rogers E.E., Eide D.J. Guerinot M.L. (2000) Altered selectivity in an Arabidopsis metal transporter. Proceedings of the National Academy of Sciences of the United States of America 97, 12356 12360.
220. Roosens N.H., Bernard C., Leplae R. Verbruggen N. (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Letters 577, 9 16.
221. Roosens N.H., Bernard C., Leplae R. Verbruggen N. (2005a) Adaptative evolution of metallothionein 3 in the Cd/Zn hyperaccumulator Thlaspi caerulescens. Zeitschrift für Naturforschung C - A Journal of Biosciences 60, 224 228.
222. Roosens N.H., Bernard C., Verbruggen N. Leplae R. (2005b) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222, 716 729.
223. 2+. Journal of Experimental Botany 57, 4003 4013.
224. Rother M., Krauss G.J., Grass G. Wesenberg D. (2006) Sulphate assimilation under Cd stress in Physcomitrella patens- combined transcript, enzyme and metabolite profiling. Plant, Cell & Environment 29, 1801 1811.
225. Salt D.E. Rauser W.E. (1995) MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology 107, 1293 1301.
226. Sanità di Toppi L., Prasad M.N.V. Ottonello S. (2002) Metal chelating peptides and proteins in plants. In Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants (eds M. Prasad K. Strzalka pp. 59 93. Kluwer Academic Publishers, Dordrecht, the Netherlands.
227. Sarry J.-E., Kuhn L., Ducruix C., et al 2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6, 2180 2198.
228. Satofuka H., Fukui T., Takagi M., Atomi H. Imanaka T. (2001) Metal-binding properties of phytochelatin-related peptides. Journal of Inorganic Biochemistry 86, 595 602.
229. 2+ differentially affects transcript amounts for γ-glutamylcysteine synthetase (γ-ECS) and metallothionein (MT2). FEBS Letters 404, 216 220.
230. Schat H. Kalff M.M.A. (1992) Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed strain? Plant Physiology 99, 1475 1480.
231. Schat H., Vooijs R. Kuiper E. (1996) Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50, 1888 1895.
232. Schat H., Llugany M., Vooijs R., Hartley-Whitaker J. Bleeker P.M. (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. Journal of Experimental Botany 53, 2381 2392.
233. Schiavon M., Zhang L., Abdel-Ghany S.E., Pilon M., Malagoli M. Pilon-Smits E.A.H. (2007) Variation in copper tolerance in Arabidopsis thaliana accessions Columbia, Landsberg erecta and Wassilewskija. Physiologia Plantarum 129, 342 350.
234. Schmöger M.E.V., Oven M. Grill E. (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiology 122, 793 801.
235. Semane B., Cuypers A., Smeets K., van Belleghem F., Horemans N., Schat H. Vangronsveld J. (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiologia Plantarum 129, 519 528.
236. Sharma S.S., Schat H., Vooijs R. Van Heerwaarden L.M. (1999) Combination toxicology of copper, zinc, and cadmium in binary mixtures: concentration- dependent antagonistic, nonadditive, and synergistic effects on root growth in Silene vulgaris. Environmental Toxicology and Chemistry 18, 348 355.
237. Sharples J.M., Meharg A.A., Chambers S.M. Cairney J.W.G. (2001) Arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytologist 151, 265 270.
238. Sneller F.E.C., van Heerwaarden L.M., Kraaijeveld-Smit F.J.L., Ten Bookum W.M., Koevoets P.L.M., Schat H. Verkleij J.A.C. (1999) Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. New Phytologist 144, 223 232.
239. Soliman M.H. (1976) pH-dependent heterosis of heavy metal-tolerant and non-tolerant hybrid of the monkey flower Minulus guttatus. Nature 262, 49 51.
240. Speiser D.M., Abrahamson S.L., Banuelos G. Ow D.W. (1992) Brassica juncea produces a phytochelatin-cadmium-sulfide complex. Plant Physiology 99, 817 821.
241. Stuyfzand P.J. (1993) Hydrochemistry and hydrology of the coastal dune area of the Western Netherlands. PhD thesis, Vrije Universiteit, Amsterdam, the Netherlands.
242. Sun X.M., Lu B., Huang S.Q., Mehta S.K., Xu L.L. Yang Z.M. (2007) Coordinated expression of sulfate transporters and its relation with sulfur metabolites in Brassica napus exposed to cadmium. Botanical Studies 48, 43 54.
243. Suzuki N. (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnology Journal 22, 19 25.
244. Thomine S., Wang R., Ward J.N., Crawford N.M. Schroeder J.I. (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proceedings of the National Academy of Sciences of the United States of America 97, 4991 4996.
245. van Tichelen K.K., Colpaert J.V. Vangronsveld J. (2001) Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytologist 150, 203 213.
246. Tolrà R.P., Poschenrieder C., Alonso R., Barceló D. Barceló J. (2001) Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytologist 151, 621 626.
247. Tolrà R., Pongrac P., Poschenrieder C., Vogel-Mikus K., Regvar M. Barceló J. (2006) Distinctive effects of cadmium on glucosinolate profiles in Cd hyperaccumulator Thlaspi praecox and non-hyperaccumulator Thlaspi arvense. Plant and Soil 288, 333 341.
248. Tonsor S.J., Alonso-Blanco C. Koornneef M. (2005) Gene function beyond the single trait: natural variation, gene effects, and evolutionary ecology in Arabidopsis thaliana. Plant, Cell & Environment 28, 2 20.
249. Tukendorf A. Rauser W.E. (1990) Changes in glutathione and phytochelatins in roots of maize seedlings exposed to cadmium. Plant Science 70, 155 166.
250. Tukendorf A., Skórzynska-Polit E. Baszynski T. (1997) Homophytochelatin accumulation in Cd-treated runner bean plants is related to their growth stage. Plant Science 129, 21 28.
251. Tuomainen M.H., Nunan N.M., Lehesranta S.J., Tervahauta A.I., Hassinen V.H., Schat H., Auriola S., McNicol J.W. Kärenlampi S.O. (2006) Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accession. Proteomics 6, 3696 3706.
252. Vatamaniuk O.K., Mari S., Lang A., Chalasani S., Demkiv L.O. Rea P.A. (2004) Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with gamma-glutamylcysteine during catalysis: stoichiometric and site-directed mutagenic analysis of Arabidopsis thaliana PCS1-catalyzed phytochelatin synthesis. Journal of Biological Chemistry 279, 22449 22460.
253. Vazquez M.D., Poschenrieder C. Barceló J. (1992) Ultrastructural effects and localization of low cadmium concentration in bean roots. New Phytologist 120, 215 220.
254. Vázquez S., Goldsbrough P. Carpena R.O. (2006) Assessing the relative contributions of phytochelatins and the cell wall to cadmium resistance in white lupin. Physiologia Plantarum 128, 487 495.
255. Verkleij J.A.C., Sneller F.E.C Schat H. (2003) Metallothioneins and phytochelatins: ecophysiological aspects. In Sulphur in Plants (eds Y.P. Abrol A. Ahmad pp. 163 176. Kluwer Academic Publishers, Dordrecht, the Netherlands.
256. van Vliet C., Andersen C.R. Cobbett C.S. (1995) Copper-sensitive mutant of Arabidopsis thaliana. Plant Physiology 109, 871 881.
257. Vögeli-Lange R. Wagner G.J. (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiology 92, 1086 1093.
258. Walton K.C. Johnson D.B. (1992) Microbiological and chemical characteristics of an acidic stream draining a disused copper mine. Environmental Pollution 76, 169 175.
259. Wangeline A.L., Burkhead J.L., Hale K.L., Lindblom S.D., Terry N., Pilon M. Pilon-Smits E.A.H. (2004) Overexpression of ATP sulfurylase in Indian mustard: effects on tolerance and accumulation of twelve metals. Journal of Environmental Quality 33, 54 60.
260. Weber M., Harada E., Vess C., van Roepenack-Lahaye E. Clemens S. (2004) 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 Journal 37, 269 281.
261. 2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant, Cell & Environment 29, 950 963.
262. Weckx J.E.J. Clijsters H.M.M. (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiologia Plantarum 96, 506 512.
263. Whiting S.N., Leake J.R., McGrath S.P. Baker A.J.M. (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytologist 145, 199 210.
264. Whiting S.N., De Souza M.P. Terry N. (2001) Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environmental Science & Technology 35, 3144 3150.
265. Wilkins D.A. (1957) Technique for the measurement of lead tolerance in plants. Nature 180, 37 38.
266. Willems G., Dräger D.B., Courbot M., Godé C., Verbruggen N. Saumitou-Laprade P. (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176, 659 674.
267. Wirtz M. Hell R. (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. Journal of Plant Physiology 163, 273 286.
268. 2+ is regulated by LCT1. Environmental Pollution 147, 584 592.
269. Wójcik M. Tukiendorf A. (2003) Response of wild type of Arabidopsis thaliana to copper stress. Biologia Plantarum 46, 79 84.
270. Wójcik M. Tukiendorf A. (2005) Cadmium uptake, localization and detoxification in Zea mays. Biologia Plantarum 49, 237 245.
271. Wójcik M., Vangronsveld J. Tukiendorf A. (2005a) Cadmium tolerance in Thlaspi caerulescens. I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environmental and Experimental Botany 53, 151 161.
272. Wójcik M., Vangronsveld J., D'Haen J. Tukiendorf A. (2005b) Cadmium tolerance in Thlaspi caerulescens. II. Localization of cadmium in Thlaspi caerulescens. Environmental and Experimental Botany 53, 163 171.
273. Xiang C. Oliver D.J. (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10, 1539 1550.
274. Xiang C., Werner B.L., Christensen E.L.M. Oliver D.J. (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiology 126, 564 574.
275. Yan S.L., Tsay C.C. Chen Y.R. (2000) Isolation and characterization of phytochelatin synthase in rice seedlings. Proceedings of the National Science Council of the Republic China Part B 24, 202 207.
276. Yoshimoto N., Takahashi H., Smith F.W., Yamaya T. Saito K. (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. The Plant Journal 29, 465 473.
277. Zhang H.Y., Xu W.Z., Guo J.B., He Z.Y. Ma M. (2005) Coordinated responses of phytochelatins and metallothioneins to heavy metals in garlic seedlings. Plant Science 169, 1059 1065.
278. Zhao F.J., Hamon R.E., Lombi E., McLaughlin M.J. McGrath S.P. (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 53, 535 543.
279. Zhao F.J., Wang J.R., Barker J.H.A., Schat H., Bleeker P.M. McGrath S.P. (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytologist 159, 403 410.
280. Zhao F.J., Jiang R.F., Dunham S.J. McGrath S.P. (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytologist 172, 646 654.
281. Zhigang A., Cuijie L., Yuangang Z., Yejie D., Wachter A., Gromes R. Rausch T. (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. Journal of Experimental Botany 57, 3575 3582.
282. Zhou J. Goldsbrough P.B. (1995) Structure, organization and expression of the metallothionein gene family in Arabidopsis. Molecular and General Genetics 248, 318 328.
283. Zhu Y.L., Pilon-Smits E.A.H., Jouanin L. Terry N. (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiology 119, 73 80.
284. Zhu Y.L., Pilon-Smits E.A.H., Tarun A.S., Weber S.U., Jouanin L. Terry N. (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiology 121, 1169 1177.
285. Zimeri A.M., Dhankher O.P., McCaig B. Meagher R.B. (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Molecular Biology 58, 839 855.