Functions and toxicity of nickel in plants: Recent advances and future prospects

Clean - Soil, Air, Water

Volumn 37, Issue 4-5, 2009, Pages 304-313

  Chen, Cuiyun ^a   Huang, Dejun ^a   Liu, Jianquan ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Accumulation; Heavy metals; Nickel; Plants; Pollution; Toxicity

Indexed keywords

ECOTOXICOLOGY; HEAVY METAL; HYPERACCUMULATION; NICKEL; PLANT; POLLUTION EFFECT; TOXICITY;

EID: 69549111728     PISSN: 18630650     EISSN: None     Source Type: Journal    
DOI: 10.1002/clen.200800199     Document Type: Review

References (207)

1. F. H. Nielson, in Trace Elements in Human and Animal Nutrition (Ed: W. Mertz), Academic Press, San Diego, CA 1987, pp. 245-273.
2. F. W. Sunderman, A. Oskarsson, in Metals and Their Compounds in the Environment (Ed: E. Merian), VCH, Weinheim 1991, pp. 1101-1126.
3. W. D. McIlveen, J. J. Negusanti, Nickel in the terrestrial environment, Sci. Total Environ. 1994, 148, 109-138.
4. S. P. McGrath, in Heavy Metals in Soils (Ed: B. J. Alloway), 2nd ed., Blackie Academic and Professional, London 1995, pp. 152-174.
5. B. J. Alloway, in Heavy Metal in Soils (Ed: B. J. Alloway), 2nd ed., Blackie Academic and Professional, London 1995, pp. 25-34.
6. D. E. Salt et al., in Phytoremediation of Contaminated Soil and Water (Eds: N. Terry, G. Banuelos), Lewis Publishers, Boca Raton, FL, 2000, pp. 189-200.
7. D. F. Easton et al., in Nickel and Human Health: Current Perspectives (Eds: E. Nieboer, J. O. Nriagu,), John Wiley & Sons, New York 1992, pp. 603-619.
8. B. A. Zarcinas, C. F. Ishak, M. J. McLaughlin, G. Cozens, Heavy metals in soils and crops in Southeast Asia. 1. Peninsular Malaysia, Environ. Geochem. Health 2004, 26, 343-357.
9. B. A. Zarcinas, P. Pongsakul, M. J. McLaughlin, G. Cozens, Heavy metals in soils and crops in Southeast Asia. 2. Thailand, Environ. Geochem. Health 2004, 26, 359-371.
10. M. S. A. Ahmad, M. Hussain, R. Saddiq, A. K. Alvi, Mungbean: A nickel indicator, accumulator or excluder?, Bull. Environ. Contam. Toxicol. 2007, 78, 319-324.
11. J. Zhao, G. Shi, Q. Yuan, Polyamines content and physiological and biochemical responses to ladder concentration of nickel stress in Hydrocharis dubia (Bl.) Backer leaves, BioMetals 2008, 21, 665-674.
12. A. Anderson, in Nickel and Human Health: Current Perspectives (Eds: E. Nieboer, J. O. Nriagu), John Wiley & Sons, New York 1992, pp. 621-627.
13. M. V. Kozlow, Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter: Natural selection or phenotypic acclimation?, Chemosphere 2005, 59, 189-197.
14. A. Papadopoulos et al., Determination and evaluation of cadmium, copper, nickel, and zinc in agricultural soils of western Macedonia, Greece, Environ. Manage. 2007, 40, 719-726.
15. B. A. Roberts, in The Vegetation of Ultramafic (Serpentine) Soils (Eds: A. J. M. Baker, J. Proctor, R. D. Reeves), Intercept Ltd., Andover, UK, 1992, pp. 53-66.
16. U. Kukier et al., The effect of pH on metal accumulation in two Alyssum species, J. Environ. Qual. 2004, 33, 2090-2102.
17. I. Déportes, J. L. Benoit-Guyod, D. Zmirou, Hazard to man and the environment posed by the use of urban waste compost: A review, Sci. Total Environ. 1995, 172, 197-222.
18. V. Barcan, E. Kovnatsky, Soil surface geochemical anomaly around the copper-nickel metallurgical smelter, Water Air Soil Pollut. 1998, 103, 197-218.
19. N. S. Karam et al., Metal concentrations, growth, and yield of potato produced from in vitro plantlets or microtubers and grown in municipal solid-waste amended substrates, J. Plant Nutr. 1998, 21, 725-739.
20. M. Astrom, A. Bjorklund, Hydrogeochemistry of a stream draining sulfide bearing postglacial sediments in Finland, Water Air Soil Pollut. 1996, 89, 233-246.
21. J. J. G. Zwolsman, A. J. van Bokhoven, Impact of summer droughts on water quality of the Rhine River-a preview of climate change, Water Sci. Technol. 2007, 56, 45-55.
22. Y. Guo, H. Marschner, Uptake, distribution, and binding of cadmium and nickel in different plant species, J. Plant Nutr. 1995, 18, 2691-2706.
23. D. E. Salt et al., Phytoremediation: A novel strategy for the removal of toxic metals from the environment using plants, BioTechnology 1995, 13, 468-474.
24. D. L. Eskew, R. M. Welch, W. A. Norvell, Nickel, an essential micronutrient for legumes and possibly all higher plants, Science 1983, 222, 621-623.
25. P. H. Brown, R. M. Welch, E. E. Cary, Nickel: A micronutrient essential for higher plants, Plant Physiol. 1987, 85, 801-803.
26. S. W. Ragsdale, Nickel biochemistry, Curr. Opin. Chem. Biol. 1998, 2, 208-215.
27. T. M. Nieminen, L. Ukonmaanaho, N. Rausch, W. Shotyk, Biogeochemistry of nickel and its release into the environment, Met. Ions Life Sci. 2007, 2, 1-30.
28. K. V. Madhava Rao, T. V. Sresty, Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses, Plant Sci. 2000, 157, 113-128.
29. J. Molas, Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni (II) complexes, Environ. Exp. Bot. 2002, 47, 115-126.
30. E. Gajewska, M. Sklodowska, M. Slaba, J. Mazur, Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots, Biol. Plant 2006, 50, 653-659.
31. B. Duarte, M. Delgado, I. Ca-ador, The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides, Chemosphere 2007, 69, 836-840.
32. U. Ermler et al., Active sites of transition -metal enzymes with a focus on nickel, Curr. Opin. Struct. Biol. 1998, 8, 749-758.
33. H. Küpper, P. M. H. Kroneck, in Metal Ions in Life Sciences (Eds: A. Sigel, H. Sigel, R. K. O. Sigel), Vol. 2, John Wiley & Sons, Chichester, UK, 2007, pp. 31-62.
34. S. B. Mulrooney, R. P. Hausinger, Nickel uptake and utilization by microorganisms, FEMS Microbiol. Rev. 2003, 27, 239-261.
35. T. Maier, A. Jacobi, M. Sauter, A. Bock, The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide protein, J. Bacteriol. 1993, 175, 630-635.
36. J. M. Collard et al., Plasmids for heavy metal resistance in Alcaligenes eutrophus CH34: Mechanisms and applications, FEMS Microbiol. Rev. 1994, 14, 405-414.
37. I. V. Seregin, A. D. Kozhevnikova, Physiological role of nickel and its toxic effects on higher plants, Russ. J. Plant Physiol. 2006, 53, 257-277.
38. T. V. Dan, S. Krishnaraj, P. K. Saxena, Cadmium and nickel uptake and accumulation in scented Geranium (Pelargonielm sp.'Frensham'), Water Air Soil Pollut. 2002, 137, 355-364.
39. K. Vogel-Mikus, D. Drobne, M. Regvar, Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia, Environ. Pollut. 2005, 133, 233-242.
40. D. A. Cataldo, T. R. Garland, R. E. Wildung, Nickel in plants: I. uptake kinetics using intact soybean seedlings, Plant Physiol. 1978, 62, 563-565.
41. 2+ by excised barley roots, Physiol. Plant. 1987, 71, 49-54.
42. L. V. Kochian, in Micronutrients in Agriculture (Eds: J. J. Mortvedt), Soil Science Society of America Madison, WI, 1991, pp. 251-270.
43. A. R. Oller, M. Costa, G. Oberd-rster, Carcinogenicity assessment of selected nickel compounds, Toxicol. Appl. Pharmacol. 1997, 143, 152-166.
44. L. Wolfram, B. Friedrich, T. Eitinger, The Alcaligenes eutrophus protein HoxN mediates nickel transport in Escherichia coli, J. Bacteriol. 1995, 177, 1840-1843.
45. T. Eitinger, M. A. Mandrand-Berthelot, Nickel transport systems in microorganisms, Arch. Microbiol. 2000, 173, 1-9.
46. T. Schor-Fumbarov, P. B. Goldsbrough, Z. Adam, E. Tel-Or, Characterization and expression of a metallothionein gene in the aquatic fern Azolla filiculoides under heavy metal stress, Planta 2005, 223, 69-76.
47. R. P. Hausinger, Metallocenter assembly in nickel-containing enzymes, J. Biol. Inorg. Chem. 1997, 2, 279-286.
48. J. W. Olson, C. Fu, R. J. Maier, The HypB protein from Bradyrhizobium japonicum can store nickel and is required for the nickel-dependent transcriptional regulation of hydrogenase, Mol. Microbiol. 1997, 24, 119-128.
49. R. K. Watt, P. W. Ludden, The identification, purification, and characterization of CooJ. A nickel-binding protein that is co-regulated with the Ni-containing CO dehydrogenase from Rhodospirillum rubrum, J. Biol. Chem. 1998, 273, 10019-10025.
50. S. G. Aschmann, R. J. Zasoski, Nickel and rubidium uptake by whole oat plants in solution culture, Physiol. Plant. 1987, 71, 191-196.
51. V. Antoniadis, J. S. Robinson, B. J. Alloway, Effects of short-term pH fluctuations on cadmium, nickel, lead, and zinc availability to ryegrass in a sewage sludge-amended field, Chemosphere 2008, 71, 759-764.
52. I. M. McKenna, R. L. Chaney, F. M. Williams, The effects of cadmium and zinc interactions on the accumulation and tissue distribution of zinc and cadmium in lettuce and spinach, Environ. Pollut. 1993, 79, 113-120.
53. Y. Luo, D. L. Rimmer, Zinc-copper interaction affecting plant growth on a metal -contaminated soil, Environ. Pollut. 1995, 88, 79-83.
54. D. Podar, M. H. Ramsey, M. J. Hutchings, 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 Phytol. 2004, 163, 313-324.
55. D. J. Burke, J. S. Weis, P. Weis, Release of metals by the leaves of the salt marsh grasses Spartina alterniflora and Phragmites australis, Estuar. Coast. Shelf Sci. 2000, 51, 153-159.
56. L. Jean et al., Effect of citric acid and EDTA on chromium and nickel uptake and translocation by Datura innoxia, Environ. Pollut. 2008, 153, 555-563.
57. G. C. Panda, S. K. Das, T. S. Bandopadhyay, A. K. Guha, Adsorption of nickel on husk of Lathyrus sativus: Behavior and binding mechanism, Colloids Surf., B 2007, 57, 135-142.
58. B. H. Robinson, R. R. Brooks, B. E. Clothier, Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: Potential use for phytomining and phytoremediation, Ann. Bot. 1999, 84, 689-694.
59. 2+ by excised barley roots, Physiol. Plant. 1987, 71, 49-54.
60. S. P. McGrath et al., Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri, Environ. Pollut. 2006, 141, 115-125.
61. J. Yanai, F. J. Zhao, S. P. McGrath, T. Kosaki, Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens, Environ. Pollut. 2006, 139, 167-175.
62. J. R. Peralta-Videa et al., Effect of mixed cadmium, copper, nickel and zinc at different pHs upon alfalfa growth and heavy metal uptake, Environ. Pollut. 2002, 119, 291-301.
63. Z. Kr-pa, A. Siedleka, W. Maksymiec, T. Baszynski, In vivo response of photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity, J. Plant Physiol. 1993, 142, 664-668.
64. P. M. Neumann, A. Chamel, Comparative phloem mobility of nickel in nonsenescent plants, Plant Physiol. 1986, 81, 689-691.
65. R. M. Welch, Micronutrient nutrition of plants, Crit. Rev. Plant Sci. 1995, 14, 49-82.
66. J. Fismes, G. Echevarria, E. Leclerc-Cessac, J.L. Morel, Uptake and transport of radioactive nickel and cadmium into three vegetables after wet aerial contamination, J. Environ. Qual. 2005, 34, 1497-1507.
67. V. Page, L. Weisskopf, U. Feller, Heavy metals in white lupin: Uptake, root-to-shoot transfer and redistribution within the plant, New Phytol. 2006, 171, 329-341.
68. W. E. Rauser, Structure and function of metal chelators produced by plants-the case for organic acids, amino acids, phytin, and metallothioneins, Cell Biochem. Biophys. 1999, 31, 19-48.
69. V. Vacchina et al., Speciation of nickel in a hyperaccumulating plant by high performance liquid chromatography-inductively coupled plasma mass spectrometry and electrospray MS/MS assisted by cloning using yeast complementation, Anal. Chem. 2003, 75, 2740-2745.
70. S. Kim, et al., Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants, Plant Cell Physiol. 2005, 46, 1809-1818.
71. J. F. Ma, D. Ueno, F. J. Zhao, S. P. McGrath, Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens, Planta 2005, 220, 731-736.
72. K. Pianelli et al., Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana, Transgenic. Res. 2005, 14, 739-748.
73. M. J. Haydon, C. S. Cobbett, Transporters of ligands for essential metal ions in plants, New Phytol. 2007, 174, 499-506.
74. G. J. Colpas, R. P. Hausinger, In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE, J. Biol. Chem. 2000, 275, 10731-10737.
75. U. Krämer et al., Free histidine as a metal chelator in plants that accumulate nickel, Nature 1996, 379, 635-638.
76. U. Krämer et al., Subcellular localization and speciation of nickel in hyperaccumulator and nonaccumulator Thlaspi species, Plant Physiol. 2000, 122, 1343-1353.
77. L. Kerkeb, U. Kr-mer, The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea, Plant Physiol. 2003, 131, 716-724.
78. D. Douchkov et al., Ectopic expression of nicotianamine synthase genes results in improved iron accumulation and increased nickel tolerance in transgenic tobacco, Plant Cell Environ. 2005, 28, 365-374.
79. M. Joho, M. Inouhe, H. Tohoyama, T. Murayama, A possible role of histidine in a nickel resistant mechanism in Saccharomyces cerevisiae, FEMS Microbiol. Lett. 1990, 66, 333-338.
80. O. DevThvre, J. Garbaye, B. Botton, Release of complexing organic acids by rhizosphere fungi as a factor in Norway spruce yellowing in acidic soils, Mycol. Res. 1996, 100, 1367-1374.
81. U. Ahonen-Jonnarth, P. A. W. Van Hees, U. S. Lundstrom, R. D. Finlay, Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations, New Phytol. 2000, 146, 557-567.
82. M. A. Fomina, I. J. Alexander, J. V. Colpaert, G. M. Gadd, Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi, Soil Biol. Biochem. 2005, 37, 851-866.
83. M.H. Lee et al., Purification and characterization of Klebsiella aerogenes UreE protein: A nickel-binding protein that functions in urease metallocenter assembly, Protein Sci. 1993, 2, 1042-1052.
84. C. Fu, J. W. Olsen, R. J. Maier, HypB protein of Bradyrhizobium japonicum is a metal-binding GTPase capable of binding 18 divalent nickel ions per dimmer, Proc. Natl. Acad. Sci. 1995, 92, 2333-2337.
85. R. L. Kerby, P. W. Ludden, G. P. Roberts, In vivo nickel insertion into the carbon monoxide dehydrogenase of Rhodospirillum rubrum: molecular and physiological characterization of cooCTJ, J. Bacteriol. 1997, 179, 2259-2266.
86. D. Gendre et al., TcYSL3, a member of the YSL gene family from the hyperaccumulator Thlaspi caerulescens, encodes a nicotianamine -Ni/ Fe transporter, Plant J. 2007, 49, 1-15.
87. H. Marschner, Mineral Nutrition of Higher Plants, 2nd ed., Academic Press, London 1995, pp 889.
88. V. Page, U. Feller, Selective transport of zinc, manganese, nickel, cobalt and cadmium in the root system and transfer to the leaves in young wheat plants, Ann. Bot. 2005, 96, 425-434.
89. O. Riesen, U. Feller, Redistribution of nickel, cobalt, manganese, zinc and cadmium via the phloem in young and in maturing wheat, J. Plant Nutr. 2005, 28, 421-430.
90. H. Küpper et al., Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense, J. Exp. Bot. 2001, 52, 2291-2300.
91. S. Sagner, R. Kneer, G. Wanner, J. P. Cosson, B. Deus-Neumann, M. H. Zenk, Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminate, Phytochemistry, 1998, 47, 339-347.
92. L. Pancaro et al., Further contribution on the relationship between nickel and malic and malonic acids in Alyssum, Giornale Botanico Italiano 1978, 112, 141-146.
93. R. R. Brooks, S. Shaw, A. A. Marfil, The chemical form and physiological function of nickel in some Iberian Alyssum species, Physiol. Plant. 1981, 51, 167-170.
94. M. H. Timperley, R. R. Brooks, P. J. Peterson, The distribution of nickel, copper, zinc, and iron in tree leaves, J. Exp. Bot. 1973, 24, 889-895.
95. D. L. Eskew, R. M. Welch, W. A. Norvell, Nickel in higher plants: Further evidence for an essential role, Plant Physiol. 1984, 76, 671-693.
96. M. W. Persans, K. Nieman, D. E. Salt. Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense, Proc. Natl. Acad. Sci. 2001, 98, 9995-10000.
97. M. Becher, I. N. Talke, L. Krall, U. Kramer, Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri, Plant J. 2004, 37, 251-268.
98. M. Weber et al., 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 J. 2004, 37, 269-281.
99. K. Wycisk, E. J. Kim, J. I. Schroeder, U. Kr-mer, Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana, FEBS Lett. 2004, 578, 128-134.
100. M. Courbot et al., Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus, Appl. Environ. Microb. 2004, 70, 7413-7417.
101. M. Bellion et al., Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum, New Phytol. 2007, 174, 151-158.
102. J.L. Freeman et al., Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators, Plant Cell 2004, 16, 2176-2191.
103. B. Ali, S. Hayat, Q. Fariduddin, A. Ahmad, 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea, Chemosphere 2008, 72, 1387-1392.
104. I. S. Sheoran, H. R. Singal, R. Singh, Effects of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeon pea (Cajanus cajan L.), Photosynth. Res. 1990, 23, 345-351.
105. M. Xylander, W. Braune, Influence of nickel on the green alga Haematococcus lacustris Rostafinski in phases of its life cycle, J. Plant Physiol. 1994, 144, 86-93.
106. A. Kabata-Pendias, H. Pendias, Trace Elements in Soils and Plants, 3 rd ed., CRC Press Inc., Boca Raton, FL, 2001, pp. 413.
107. A. G. L. Assunção et al., Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types, New Phytol. 2003, 159, 411-419.
108. E. G. Bollard, in Encyclopedia of Plant Physiology, New Series, 15B (Eds.: A. L_uchli, R. L. Bieleski), Springer-Verlag, Berlin 1983, pp. 695-755.
109. C. J. Asher, Micronutrients in Agriculture, 2 nd ed., Soil Science Society of America, Madison, WI, 1991, pp. 703-723.
110. A. J. Pollard, K. D. Powell, F. A. Harper, J. A. C. Smith, The genetic basis of metal hyperaccumulation in plants, Crit. Rev. Plant Sci. 2002, 21, 539-566.
111. E. J. Sun, F. Y. Wu, Along-vein necrosis as indicator symptom on water spinach caused by nickel in water culture, Bot. Bull. Acad. Sin. 1998, 39, 255-259.
112. H. Rahman, S. Sabreen, S. Alam, S. Kawai, Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution, J. Plant Nutr. 2005, 28, 393-404.
113. J. Molas, Comparison of nickel toxicity and resistance strategies of cabbage plants grown in soil with addition of inorganic and organic Ni (II) complexes, Dev. Plant Soil Sci. 2001, 92, 464-465.
114. A. Nedhi, L. J. Singh, S. I. Singh, Effect of cadmium and nickel on germination, early seedling growth and photosynthesis of wheat and pigeon pea, Int. J. Trop. Agr. 1990, 8, 141-147.
115. R. Boominathan, P. M. Doran, Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii, New Phytol. 2002, 156, 205-215.
116. J. Molas, Changes in morphological and anatomical structure of cabbage (Brassica oleracera L.) outer leaves and in ultrastructure of their chloroplasts caused by an in vitro excess of nickel, Photosynthetica 1997, 34, 513-522.
117. J. Balaguer et al., Tomato growth and yield affected by nickel presented in the nutrient solution, Acta. Hort. 1998, 458, 269-272.
118. 2+ on growth and metabolism of cabbage, Plant Sci. 2002, 163, 753-758.
119. B. Szalontai et al., Molecular rearrangements of thylakoids after heavy metal poisoning, as seen by Fourier transform infrared (FTIR) and electron spin resonance (ESR) spectroscopy, Photosynth. Res. 1999, 61, 241-252.
120. E. Gajewska, M. Sklodowska, Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves, BioMetals 2007, 20, 27-36.
121. P. C. Bethkey, M. C. Drew, Stomatal and non-stomatal components to inhibition of photosynthesis in leaves of Capsium annum during progressive exposure to NaCl salinity, Plant Physiol. 1992, 99, 219-226.
122. 2+, Biochim. Biophys. Acta 1981, 638, 217-224.
123. F. Van Assche, H. Clijsters, Effects of metals on enzyme activity in plants, Plant Cell Environ. 1990, 13, 195-206.
124. 2+ toxicity in rice: Effect on membrane functionality and plant water content, Plant Physiol. Biochem. 2008, 46, 905-910.
125. B. Y. Khalid, J. Tinsley, Some effects of nickel toxicity on ryegrass, Plant Soil 1980, 55, 139-144.
126. R. Hasinur, S. Shamima, A. Shah, K. W. Shigenao, Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution, J. Plant Nutr. 2005, 28, 393-404.
127. 2+ on growth, oxygen evolution and photosynthetic electron transport in Cylindrospermum IU 942, J. Plant Physiol. 1989, 134, 406-412.
128. S. Boisvert et al., Inhibition of the oxygen-evolving complex of photosystem II and depletion of extrinsic polypeptides by nickel, BioMetals 2007, 20, 879-889.
129. R. Gopal et al., Laser-induced chlorophyll fluorescence spectra of mung plants growing under nickel stress, Curr. Sci. 2002, 83, 880-884.
130. L. Wisniewski, N. M. Dickinson, Toxicity of copper to Quercus robur (English Oak) seedlings from a copper-rich soil, Environ. Exp. Bot. 2003, 50, 99-107.
131. P. Aravind, M. N. V. Prasad, Zn protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte, Plant Sci. 2004, 166, 1321-1327.
132. B. C. Tripathy, B. Bhatia, P. Mohanty, Cobalt ions inhibit electron transport activity of photosystem II without affecting photosystem I, Biochim. Biophys. Acta 1983, 722, 88-93.
133. N. Mohanty, J. Vass, S. Demeter, Impairment of photosystem II activity at the level of secondary quinine electron acceptor in chloroplasts treated with cobalt, nickel and zinc ions, Physiol. Plant. 1989, 76, 386-390.
134. M. M. El-Sheekh, Inhibition of photosystem II in the green alga Scenedesmus obliguus by nickel, Biochem. Physiol. Pflanzen 1993, 188, 363-372.
135. L. Taiz, E. Zeiger, Plant Physiology, 3rd ed., Sinauer Associates, Sunderland, MA, 2002, pp. 607-611.
136. E. L. Heale, D. P. Ormrod, Effects of nickel and copper on Acer rubrum, Cornus stolonifers, Lonicera tatarica, and Pinus resinosa, Can. J. Bot. 1982, 60, 2674-2681.
137. H. Marschner, Mineral Nutrition of Higher Plants, Academic Press, London 1986, pp. 674.
138. H. Küpper, F. Küpper, M. Spiller, Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants, J. Exp. Bot. 1996, 47, 259-266.
139. R. Gabbrielli, T. Pandolfini, O. Vergnano, M. R. Palandri, Comparison of two serpentine species with different nickel tolerance strategies, Plant Soil 1990, 122, 271-277.
140. M. I. Rubio et al., Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids, Plant Growth Regul. 1994, 14, 151-157.
141. I. Genrich, G. I. Burd, D. G. Dixon, B. R. Glick, A plant growth-promoting bacterium that decreases nickel toxicity in seedlings, Appl. Environ. Microbiol. 1998, 64, 3663-3668.
142. S. C. Gon-alves et al., Genetic diversity and differential in vitro responses to Ni in Cenococcum geophilum isolates from serpentine soils in Portugal, Mycorrhiza 2007,17, 677-686.
143. G. Ouzounidou, M. Moustakas, L. Symeonidis, S. Karataglis, Response of wheat seedlings to Ni stress: Effects of supplemental calcium, Arch. Environ. Contam. Toxicol. 2006, 50, 346-352.
144. 2+ on the response to nickel toxicity in a serpentine endemic and nickel-accumulating species, Physiol. Plant. 1984, 62, 540-544.
145. T. M. Nieminen, Effects of soil copper and nickel on survival and growth of Scots pine, J. Environ. Monit. 2004, 6, 888-896.
146. B. K. Parida, I. M. Chhibba, V. K. Nayyar, Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition, Sci. Hortic. 2003, 98, 113-119.
147. H. Küpper, F. Küpper, M. Spiller, In situ detection of heavy metal substituted chlorophylls in water plants, Photosynth. Res. 1998, 58, 125-133.
148. J. F. Souza, W. E. Rauser, Maize and radish sequester excess cadmiumand zinc in different ways, Plant Sci. 2003, 65, 1009-1022.
149. 2+ reacts with different components of the NADPH:protochlorophyllide oxidoreductase macrodomains, Plant Biol. 2004, 6, 358-363.
150. C. Gonnelli, F. Galardi, R. Gabbrielli, Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa, Physiol. Plant. 2001, 113, 507-514.
151. P. O'Brien, H. J. Salacinski, Evidence that the reactions of cadmium in the presence of metallothionein can produce hydroxyl radicals, Arch. Toxicol. 1998, 72, 690-700.
152. A. Galan et al., The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays), Eur. J. Cell Biol. 2001, 80, 312-320.
153. S. J. Stohs, D. Bagchi, E. Hassoun, M. Bagchi, Oxidative mechanisms in the toxicity of chromium and cadmium ions, J. Environ. Pathol. Toxicol. Oncol. 2001, 20, 77-88.
154. F. Hao, X. Wang, J. Chen, Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings, Plant Sci. 2006, 170, 151-158.
155. T. Pandolfini, R. Gabbrielli, C. Comparini, Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L, Plant Cell Environ. 1992, 15, 719-725.
156. S. Baccouch, A. Chaoui, E. E. Ferjani, Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots, Plant Physiol. Biochem. 1998, 36, 689-694.
157. S. Baccouch, A. Chaoui, E. E. Ferjani, Nickel toxicity induces oxidative damage in Zea mays roots, J. Plant Nutr. 2001, 24, 1085-1097.
158. E. Gajewska, M. Sklodowska, Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress, Acta Physiol. Plant. 2005, 27, 329-339.
159. H. Schickler, H. Caspi, Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum, Physiol. Plant. 1999, 105, 39-44.
160. R.A. Gomes-Juniora et al., Nickel elicits a fast antioxidant response in Coffea arabica cells, Plant Physiol. Biochem. 2006, 44, 420-429.
161. S. A. El-Maraghy, M. Z. Gad, A. T. Fahim, M. A. Hamdy, Effect of cadmium and aluminum intake on the antioxidant status and lipid peroxidation in rat tissues, J. Biochem. Mol. Toxicol. 2001, 15, 207-214.
162. E. Tatrai et al., Comparative in vitro toxicity of cadmium and lead on redox cycling in type II pneumocytes, J. Appl. Toxicol. 2001, 21, 479-483.
163. E. M. Del Carmen et al., Cadmium induces alpha(1) collagen (I) and metallothionein II gene and alters the antioxidant system in rat hepatic stellate cells, Toxicology 2002, 170, 63-73.
164. B. Chakravarty, S. Srivastava, Toxicity of some heavy metals in vivo and in vitro in Helianthus annuus, Mutat. Res. 1992, 283, 287-294.
165. R. Von Burg, Nickel and some nickel compounds, J. Appl. Toxicol. 1997, 17, 425-431.
166. M. Costa, Carcinogenic metals, Sci. Prog. 1998, 81, 329-339.
167. S. Knasmuller et al., Detection of genotoxic effects of heavy metal contaminated soils with plant bioassays, Mutat. Res. 1998, 420, 37-48.
168. W. Bal et al., Ni(II) specifically cleaves the C-terminal tail of the major variant of histone H2A and forms an oxidative damagemediating complex with the cleaved-off octapeptide, Chem. Res. Toxicol. 2000, 13, 616-624.
169. W. Bal, K. S. Kasprzak, Induction of oxidative DNA damage by carcinogenic metals, Toxicol. Lett. 2002, 127, 55-62.
170. E. G. Papazoglou, G. A. Karantounias, S. N. Vemmos, D. L. Bouranis, Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni, Environ. Int. 2005, 31, 243-249.
171. K. J. Dietz, M. Baier, U. Kramer, in Heavy Metal Stress in Plants: from Molecules to Ecosystems, (Eds.: M. N. V. Prasad, J. Hagemeyer), Springer- Verlag, Berlin 1999, pp. 73-97.
172. E. Kukkola, P. Rautio, S. Huttunen, Stress indications in copperand nickel-exposed Scots pine seedlings, Environ. Exp. Bot. 2000, 43, 197-210.
173. A. J. M. Baker, S. P. McGrath, R. G. Reeves, in Phytoremediation of Contaminated Soil and Water (Eds.: T. Norman, B. Gary), CRC Press, Boca Raton, FL 2000, pp. 85-107.
174. M. N. V. Prasad, Nickelophilous plants and their significance in phytotechnologies, Braz. J. Plant Physiol. 2005, 17, 113-128.
175. M. J. Milner, L. V. Kochian, Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system, Ann. Bot. 2008, 102, 3-13.
176. R. L. Chaney et al., Phytoremediation of soil metals, Curr. Opin. Biotechnol. 1997, 8, 279-284.
177. R. L. Chaney et al. Using hyperaccumulator plants to phytoextract soil Ni and Cd, Z. Naturforsch. 2005, 60, 190-198.
178. R. D. Reeves, A. J. M. Baker, A. Borhidi, R. Berezain, Nickel-accumulating plants from the ancient serpentine soils of Cuba, New Phytol. 1996, 133, 217-224.
179. R. D. Reeves, A. J. M. Baker, in Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment (Eds: I. Raskin and B. D. Ensley), John Wiley & Sons, New York 2000, pp. 193-229.
180. R. R. Brooks et al., Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae), Proc. R. Soc. London Sect. B 1979, 203, 387-403.
181. G. N. Batianoff, R. L. Specht, in The Ecology of Ultramafic (Serpentine) Soils, Intercept Ltd., Andover, UK 1992, pp. 109-128.
182. N. P. Bhatia, PhD Thesis, Central Queensland University, Australia 2003.
183. R. B. Shutes et al., An experimental constructed wetland system for the treatment of highway runoff in the U.K., Water Sci. Technol. 2001, 44, 571-578.
184. H. R. Hadad, M. A. Maine, C. A. Bonetto, Macrophyte growth in a pilot-scale constructed wetland for industrial wastewater treatment, Chemosphere 2006, 63, 1744-1753.
185. M. Scholz, P. Anderson, B. I. Forman, Treatment of gully pot liquor containing heavy metals with constructed wetlands in Scotland, Water Sci. Technol. 2005, 51, 251-258.
186. C. Bragato, H. Brix, M. Malagoli, Accumulation of nutrients and heavy metals in Phragmites australis (Cav.) Trin. ex Steudel and Bolboschoenus maritimus (L.) Palla in a constructed wetland of the Venice lagoon watershed, Environ. Pollut. 2006, 144, 967-975.
187. A. S. El-Gendy, N. Biswas, J. K. Bewtra, Municipal landfill leachate treatment for metal removal using water hyacinth in a floating aquatic system, Water Environ. Res. 2006, 78, 951-964.
188. N. Mallick, Shardendu, L. C. Rai, Removal of heavy metals by two free floating aquatic macrophytes, Biomed. Environ. Sci. 1996, 9, 399-407.
189. M. Khosravi, R. Rakhshaee, M. T. Ganji, Pre-treatment processes of Azolla filiculoides to remove Pb(II), Cd(II), Ni(II) and Zn(II) from aqueous solution in the batch and fixed-bed reactors, J. Hazard Mater. 2005, 127, 228-237.
190. N. Axtell, S. Sternberg, K. Claussen, Lead and nickel removal using Microspora and Lemna minor, Bioresour. Technol. 2003, 89, 41-48.
191. P. Miretzky, A. Saralegui, A. Fernandez Cirelli, Aquatic macrophytes potential for the simultaneous removal of heavy metals (Buenos Aires, Argentina), Chemosphere 2004, 57, 997-1005.
192. V. K. Mishra, A. R. Upadhyaya, S. K. Pandey, B. D. Tripathi, Heavy metal pollution induced due to coal mining effluent on surrounding aquatic ecosystem and its management through naturally occurring aquatic macrophytes, Bioresour. Technol. 2008, 99, 930-936.
193. P. K. Rai, Heavy metal pollution in aquatic ecosystems and its phytoremediation using wetland plants: An ecosustainable approach, Int. J. Phytoremediation 2008, 10, 131-158.
194. R. S. Boyd, S. N. Martens, in The Vegetation of Ultramafic (Serpentine) Soils (Eds: A. J. M. Baker, J. Proctor, R. D. Reeves), Intercept Ltd., Andover, UK 1992, pp. 279-289.
195. R. S. Boyd, S. N. Martens, The significance of metal hyperaccumulation for biotic interactions, Chemoecology 1998, 8, 1-7.
196. R. S. Boyd, Ecology of metal hyperaccumulation, New Phytol. 2004, 162, 563-567.
197. A. J. M. Baker, S. P. McGrath, C. M. D. Sidoli, R. D. Reeves, The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants, Resour. Conserv. Recycl. 1994, 11, 41-49.
198. M. D. Schwartz, M. A. Wall, Melanotrichus boydi, a new species of plant bug (Heteroptera: Miridae: Orthotylini) restricted to the nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae), Pan-Pacific Entomol. 2001, 77, 39-44.
199. S. N. Whiting, P. M. Neumann, A. J. M. Baker, Nickel and zinc hyperaccumulation by Alyssum murale and Thlaspi caerulescens (Brassicaceae) do not enhance survival and whole-plant growth under drought stress, Plant Cell Environ. 2003, 2, 351-360.
200. M. M. Abou Auda, L. Symeonidis, E. Hatzistavrou, T. Yupsanis, Nucleolytic activities and appearance of a new DNase in relation to nickel and manganese accumulation in Alyssum murale, J. Plant Physiol. 2002, 159, 1087-1095.
201. K. Fujimori, D. Ohta, Heavy metal induction of Arabidopsis serine decarboxylase gene expression, Biosci. Biotechnol. Biochem. 2003, 67, 896-898.
202. R. A. Ingle et al., Constitutive high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants, Plant Cell 2005, 17, 2089-2106.
203. W. Qu et al., Mechanisms of arsenic-induced cross-tolerance to nickel cytotoxicity, genotoxicity, and apoptosis in rat liver epithelial cells, Toxicol. Sci. 2001, 63, 189-195.
204. E. Denkhaus, K. Salnikow, Nickel essentiality, toxicity, and carcinogenicity, Crit. Rev. Oncol. Hematol. 2002, 42, 35-56.
205. C. N. Mulligan, R. N. Yong, B. F. Gibbs, Remediation technologies for metal-contaminated soils and groundwater: An evaluation, Eng. Geol. 2001, 60, 193-207.
206. M. Puschenreiter, G. Stoger, E. Lombi, O. Horak, W. W. Wenzel, Phytoextraction of heavy metal contaminated soils with Thlaspi goesingense and Amaranthus hybridus: Rhizosphere manipulation using EDTA and ammonium sulfate, J. Plant Nutr. Soil Sci. 2001, 164, 615-621.
207. D. L. LeDuc, N. Terry, Phytoremediation of toxic trace elements in soil and water, J. Ind. Microbiol. Biotechnol. 2005, 32, 514-520.