Responses and Adaptations of Plants to Metal Stress

  • David Salt
Part of the Springer Handbook Series of Plant Ecophysiology book series (KLEC, volume 1)


“Over 200 papers, 3 reviews, a small book, and now a big book. What is it about this curious and unimportant character that has merited such attention?” This is the opening sentence from “The Essential Qualities”, an article discussing the “curious and unimportant character” of how plants adapt to elevated concentrations of trace metals in their environment (Bradshaw et al.,1990). Bradshaw and co-authors found the study of plant metal tolerance to be a valuable tool for the investigation of natural selection in plants (Bradshaw et al., 1990). However, in the proceeding ten years since the publication of this article, the “curious and unimportant character” of metal tolerance has attracted even more attention; and given rise to a new field of study termed phytoremediation. Because of the attractiveness of using plants to remove pollutant metals from the environment, numerous researchers have now begun to investigate phytoremediation, generating over 200 publications and millions of dollars of grant funding. However, at the center of all this new attention is still that “curious and unimportant character” highlighted by Bradshaw and coworkers. What do we know about its physiological, biochemical and molecular nature?


Transgenic Plant Heavy Metal Stress Indian Mustard Zinc Transport Nickel Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Arazi, T., Ramanjulu, S., Kaplan, B. and Fromm, H. 1999. A tobacco plasma membrane calmodulin-binding transporter confers Nit+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J. 20, 171–182.PubMedCrossRefGoogle Scholar
  2. Baker, A.J.M 1981. Accumulators and excluders — strategies in the response of plants to heavy metals. J. Plant Nutr.3, 643–654.CrossRefGoogle Scholar
  3. Belouchi, A., Kwan, T. and Gros P. 1997. Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol. Biol.33, 1085–1092.PubMedCrossRefGoogle Scholar
  4. Bizily, S.P., Rugh, CL. and Meagher, R.B. 2000. Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nature Biotechnol. 18, 213–217.CrossRefGoogle Scholar
  5. Bizily, S.P., Rugh, C.L., Summers, A.O. and Meagher, R.B. 1999. Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thalianaconfers resistance to organomercurials. Proc. Natl. Acad. Sci. USA96, 6808–6813.PubMedCrossRefGoogle Scholar
  6. Blarney, F.P.C., Joyce, D.C., Edwards, D.G. and Asher C.J. 1986. Role of trichomes in sunflower tolerance to manganese toxicity. Plant Soil91, 171–180.CrossRefGoogle Scholar
  7. Bradshaw, A.D., McNeilly, T. and Putwain, P.D. 1990. “The essential qualities”. In: Heavy Metal Tolerance in Plants: Evolutionary Aspects, ed. A.J. Shaw, pp. 323–334, CRC Press, Inc., Boca Raton.Google Scholar
  8. Brown, T.A. and Shrift, A. 1982. Selenium: toxicity and tolerance in higher plants. Biol. Rev.57, 59–84.CrossRefGoogle Scholar
  9. Brune, A., Urbach, W. and Dietz, K-J. 1994. Compartmentation and transport of zinc in barley primary leaves as basic mechanisms involved in zinc tolerance. Plant. Cell. Environ.17, 153–162.CrossRefGoogle Scholar
  10. Clarkson, D.T. and Hanson, J.B. 1986. Proton fluxes and the activity of a stelar proton pump in onion roots. J. Exp. Bot.37, 1136–1150.CrossRefGoogle Scholar
  11. Clemens, S., Kim, E.J., Neumann, D. and Schroeder, J.I. 1999. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBOJ. 18, 3325–3333.Google Scholar
  12. Crowell, D. and Amasino, R.M. 1991. Induction of specific mRNA’s in cultured soybean cells during cytokinin or auxin starvation. Plant Physiol. 95, 711–715.PubMedCrossRefGoogle Scholar
  13. De Boer, A.H., Prins, H.B.A. and Zanstra, P.E. 1983. Bi-phasic composition of trans-root electrical potential in roots of Plantagospecies: involvement of spatially separated electrogenic pumps. Planta157, 259–266.CrossRefGoogle Scholar
  14. De Miranda, J.R., Thomas, M.A., Thurman, D.A. and Tomsett, A.B. 1990. Metallothionein genes from the flowing plant Mimulus guttatus. FEBS Leu. 260: 277–280.CrossRefGoogle Scholar
  15. Delhaize, E., Ryan, P.R. and Randall, J. 1993. Aluminum tolerance in wheat (Triticum aestivumL.) II. Aluminum-stimulated excretion of malic acid from root apicies. Plant Physiol. 103, 695–670.PubMedGoogle Scholar
  16. Eide, D., Broderius, M., Fett, J. and Guerinot, M-L. 1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Nat. Acad. Sci. USA93, 5624–5628.PubMedCrossRefGoogle Scholar
  17. Grill, E., Winnacker, E-L. and Zenk, M.H. 1985. Phytochelatins: the principle heavy metal complexing peptides of higher plants. Science230, 674–676.CrossRefGoogle Scholar
  18. Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M-L. and Eide, D. 1998. Identification of a family of zinc transporter genes from Arabidopsisthat respond to zinc deficiency. Proc. Nat. Acad. Sci. USA95, 7220–7224.PubMedCrossRefGoogle Scholar
  19. Ha, S-B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O’Connell, M.J., Goldsbrough, P.B. and Cobbett, C.S. 1999. Phytochelatin synthase genes from Arabidopsisand the yeast Schizosaccharomyces pombe. Plant Cell 11, 1153 - 1163.Google Scholar
  20. Heath, S.M., Southworth, D. and D’Allura, J.A. 1997. Localization of nickel in epidermal subsidiary cells of leaves of Thlaspi montanumvar. siskiyouense(Brassicaceae) using energy-dispersive x-ray microanalysis. Int. J. Plant. Sci.158, 184–188.CrossRefGoogle Scholar
  21. Higuchi, K., Suzuki, K., Nakanishi, H., Yamaguchi, H., Nishizawa, N-K. and Mori, S. 1999. Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 119, 471–479.CrossRefGoogle Scholar
  22. Himelblau, E., Mira, H., Lin, S-J., Culotta, V.C., Penarrubia, and Amasino, R.M. 1998. Identification of a functional homolog of the yeast copper homeostasis gene ATX1from Arabidopsis. Plant Physiol.117, 1227–1234.CrossRefGoogle Scholar
  23. Howden, R. and Cobbett, C.S 1992. Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 99, 100–107.CrossRefGoogle Scholar
  24. Howden, R., Goldsbrough, P.B., Andersen, C.R. and Cobbett, C.S. 1995. Cadmium-sensitive, cad]mutants of Arabidopsis thalianaare phytochelatin deficient. Plant Physiol. 107, 1059–1066.PubMedCrossRefGoogle Scholar
  25. Kochian, L.V. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol.46, 237–260.CrossRefGoogle Scholar
  26. Krämer, U., Cotter-Howells, J.D., Charnock, J.M., Baker, A.J.M. and Smith, J.A.C. 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature379, 635–638.CrossRefGoogle Scholar
  27. Krämer, U., Smith, R.D., Wenzel, W., Raskin, I. and Salt, D.E. 1997a. The role of nickel transport and tolerance in nickel hyperaccumulation by Thlaspi goesingenseHâlâcsy. Plant Physiol. 115, 1641–1650.Google Scholar
  28. Krämer, U., Grime, G.W., Smith, J.A.C., Hawes, C.R. and Baker, A.J.M. 1997b. MicroPIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nucl. Instr. Meth. Phys. Res. B. 130, 346–350.CrossRefGoogle Scholar
  29. Krämer, U., Pickering, LJ., Prince, R.C., Raskin, I. and Salt, D.E. 2000. Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspispecies. Plant Physiol. 122, 1343–1353.PubMedCrossRefGoogle Scholar
  30. Köpper, H., Zhao, F.J. and McGrath, S.P. 1999. Cellular compartmentalization of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol. 119, 305–311.CrossRefGoogle Scholar
  31. Lasat, M.M., Baker, A.J.M. and Kochian, L.V. 1996. Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol. 112: 1715–22Google Scholar
  32. Lasat, M.M., Baker, A.J.M. and Kochian, L.V. 1998. Altered zinc compartmentation in the root symplasm and stimulated zinc absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol. 118, 875–883.CrossRefGoogle Scholar
  33. Läuchli, A. 1993. Selenium in plants: uptake, functions, and environmental toxicity. Bot. Acta106, 455–468.Google Scholar
  34. Leustek, T, and Saito, K. 1999. Sulfate transport and assimilation in plants. Plant Physiol. 120, 637–643.PubMedCrossRefGoogle Scholar
  35. Lim, C.O., Kim, H.Y., Kim, M.G., Lee, S.I., Chung, W.S., Park, S.H., Hwang, I. and Cho. M..J. 1996. Expressed sequence tags of chinese cabbage flower bud cDNA. Plant Physiol. 111, 577–588.PubMedCrossRefGoogle Scholar
  36. Manuel de la Fuente, J., Ramírez-Rodriguez, V., Cabrera-Ponce, J.L., Herrera-Estrella, L. 1997. Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science276, 1566–1568.CrossRefGoogle Scholar
  37. Marschner, H. 1995. Mineral Nutrition of Higher Plants, 2nd edition, Academic Press, London.Google Scholar
  38. Martell, E.A. 1974. Radioactivity of tobacco trichomes and insoluble cigarette smoke particles. Nature249, 215–217.PubMedCrossRefGoogle Scholar
  39. Mesjasz-Przybylowicz, J., Balkwill, K., Przybylowicz, W.J. and Annegarn, H.J. 1994. Proton microprobe and X-ray fluorescence investigations of nickel distribution in serpentine flora from South Africa. Nucl. Instr. Meth. B.89, 208–212.CrossRefGoogle Scholar
  40. Miyasaka, S.C., Buta, J.G., Howell, R.K. and Foy, C.D. 1991. Mechanism of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol. 96, 737–743.PubMedCrossRefGoogle Scholar
  41. Murphy, A.S., Eisinger, W.R., Shaff, J.E., Kochian, L.V. and Taiz. L. 1999. Early copper-induced leakage of K’ from Arabidopsisseedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiol. 121, 1375–1382.PubMedCrossRefGoogle Scholar
  42. Neuhierl, B. and Böck, A. 1996. On the mechanism of selenium tolerance in selenium-accumulating plants. Purification and characterization of a specific selenocysteine methyltransferase from cultured cells of Astragalus bisculatus. Eur. J. Biochem. 239, 235238.Google Scholar
  43. Neuhierl, B., Thanbichler, M., Lottspeich, F. and Böck, A. 1999. A family of Smethylmethionine-depenent thiol/selenol methyltransferases. Role in selenium tolerance and evolutionary relation. J. Biol. Chem.274, 5407–5414.PubMedCrossRefGoogle Scholar
  44. Neumann, D., zur Nieden, U., Lichtenberger, O. and Leopold, I. 1995. How does Armeria maritimatolerate high heavy metal concentrations? J. Plant Physiol.146, 704–717.CrossRefGoogle Scholar
  45. Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D. and Kochian, L.V. 2000. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Nat. Acad. Sci. USA97, 4956–60.CrossRefGoogle Scholar
  46. Persans, M. and Salt, D.E. 2000. Possible molecular mechanisms involved in nickel, zinc and selenium hyperaccumulation in plants. Biotech. Gen. Eng. Rev.17, 385–409.Google Scholar
  47. Persans, M.W., Albrecht, C., Nieman, K.S., Shaffer, I.N., Motley, P.L. and Salt, D.E. 1999a. Molecular dissection of the cellular mechanisms involved in nickel hyperaccumulation. Abstracts of the American Society of Plant Physiology, Annual Meeting, Baltimore, MD., USA.Google Scholar
  48. Persans, M., Xiange, Y., Patnoe, J.M.M.L., Krämer, U. and Salt, D.E. 1999b. Molecular dissection of histidine’s role in nickel hyperaccumulation in Thlaspi goesingense(HSlâcsy). Plant Physiol. 121, 1–10.CrossRefGoogle Scholar
  49. Pickering, I.J., Prince, R.C., George, J.M., Smith, R.D., George, G.N. and Salt, D.E. 2000. Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 122, 1171–1177.PubMedCrossRefGoogle Scholar
  50. Pilon-Smits, E.A.H., Hwang, S., Lytle, C.M., Zhu, Y., Tai, J.C., Bravo, R.C., Chen, Y., Leustek, T. and Terry, N. 1999. Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol119, 123–132.PubMedCrossRefGoogle Scholar
  51. Pitman, M.G. 1972. Uptake and transport of ions in barley seedlings. II. Evidence for two active stages in transport to the shoot. Aust. J. Biol. Sci.25, 243–257.Google Scholar
  52. Rauser, W.E. 1999. Structure and function of metal chelators produced by plants. Cell Biochem. Biophys.31, 19–48.PubMedCrossRefGoogle Scholar
  53. Roberts, S.K. and Tester, M. 1995. Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. Plant J. 8, 811–825.CrossRefGoogle Scholar
  54. Roberts, S.K. and Tester, M. 1997. Permeation of Cat+ and monovalent cations through an outwardly rectifying channel in maize root stelar cells. J. Exp. Bot. 48, 839–84. 6.Google Scholar
  55. Rugh, C.L., Wilde, H.D., Stack, N.M., Thompson, D.M., Summers, A.O. and Meagher, R.B. 1996. Mercuric ion reduction and resistance in transgenic Arabidopsis thalianaplants expressing a modified bacterial merA gene. Proc. Nat. Acad. Sci. USA93, 3182–3187.PubMedCrossRefGoogle Scholar
  56. Rugh, C.L., Senecoff, J.F., Meagher, R.B. and Merkle, S.A. 1998. Development of transgenic yellow poplar for mercury phytoremediation. Nature Biotechnol. 16, 925–928.CrossRefGoogle Scholar
  57. Sagner, S., Kneer, R., Wanner, G., Cosson, J-P., Deus-Neumann, B. and Zenk, M.H. 1998. Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry47, 339–347.CrossRefGoogle Scholar
  58. Salt, D.E. and Wagner, G.J. 1993. Cadmium transport across tonoplast of vesicles from oat roots. Evidence for a Cd/H antiport activity. J. Biol. Chem.268, 12297–12302.PubMedGoogle Scholar
  59. Salt, D.E. and Rauser, W.E. 1995. MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 107, 1293–1301.PubMedGoogle Scholar
  60. Salt, D.E., Prince, R.C., Pickering, I.J. and Raskin, I. 1995. Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 109, 1427–1433.PubMedGoogle Scholar
  61. Salt, D.E. 1998. Arboreal alchemy. Nature Biotechnol. 16, 905.CrossRefGoogle Scholar
  62. Salt, D.E., Smith, R.D., Raskin, I. 1998. Phytoremediation. Ann. Rev. Plant Physiol. Plant Mol. Biol.49, 643–668.CrossRefGoogle Scholar
  63. Salt, D.E., Kato, N., Krämer, U., Smith, R.D. and Raskin, I. 1999a. “The role of root exudates in nickel hyperaccumulation and tolerance in accumulator and non-accumulator species of Thlaspi”. In: Phytoremediation of Contaminated Soil and Water, eds. N. Terry and G.S. Banuelos, pp. 191–202. CRC Press LLC, Boca Raton.Google Scholar
  64. Salt, D.E., Prince, R.C., Baker, A.J.M., Raskin, I. and Pickering, I.J. 1999b. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescensas determined using X-ray absorption spectroscopy. Environ. Sci. Tech.33, 713–717.CrossRefGoogle Scholar
  65. Schmoger, M.E., Oven, M. and Grill, E. 2000. Detoxification of arsenic by phytochelatins in plants. Plant Physiol. 122, 793–802.PubMedCrossRefGoogle Scholar
  66. Shrift, A. 1969. Aspects of selenium metabolism in higher plants. Ann. Rev. Plant Physiol.20, 475–495.CrossRefGoogle Scholar
  67. Thomine, S., Wang, R., Ward, J.M., Crawford, N.M. and Schroeder, J.I. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsiswith homology to nramp genes. Proc. Nat. Acad. Sci. USA97, 4991–4996.PubMedCrossRefGoogle Scholar
  68. Van der Zaal, B.J., Neuteboom, L.W., Pinas, J.E., Chardonnes, A.N., Schat, H., Verkleji, J.A.C. and Hooykaas, P.J.J. 1999. Overexpression of a novel Arabidopsisgene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol. 119, 1047–1055.PubMedCrossRefGoogle Scholar
  69. Vatamaniuk, O.K., Mari, S., Lu, Y-P. and Rea, P.A. 1999. AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitroreconstitution. Proc. Nat. Acad. Sci. USA96, 7110–7115.PubMedCrossRefGoogle Scholar
  70. Vatamaniuk, O.K., Mari, S., Lu, Y.P., Rea, P.A. 2000. Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthasecatalyzed transpeptidation of glutathione and related thiol peptides. J. Biol. Chem.275, 31451–32459.PubMedCrossRefGoogle Scholar
  71. Vazquez, M.D., Barceló, J., Poschenrieder, Ch., Madico, J., Hatton, P., Baker, A.J.M. and Cope, G.H. 1992. Localization of zinc and cadmium in Thlaspi caerulescens(Brassicaceae), a metallophyte that can hyperaccumulate both metals. J. Plant Physiol.140, 350–355.CrossRefGoogle Scholar
  72. Vazquez, M.D., Poschenrieder, Ch., Barceló, J., Baker, A.J.M., Hatton, P. and Cope, G.H. 1994. Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J andC Presl. Bot. Acta107, 243–250.Google Scholar
  73. Vögeli-Lange, R. and Wagner, G.J. 1990. Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiol. 92, 1086–1093PubMedCrossRefGoogle Scholar
  74. Wegner, L.H. and Raschke, K. 1994. Ion channels in the xylem parenchyma of barley roots. Plant Physiol. 105, 799–813.PubMedGoogle Scholar
  75. White, M.C., Baker, F.D., Chaney, R.F. and Decker, A.M. 1981. Metal complexation in xylem fluid. Plant Physiol. 67, 301–310.PubMedCrossRefGoogle Scholar
  76. Zhao, H. and Eide, D. 1996. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271, 23203–23210.Google Scholar
  77. Zhu, Y.L., Pilon-Smits, E.A., Tanin, A.S., Weber, S.U., Jouanin, L. and Terry, N. 1999a. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing yglutamylcysteine synthetase. Plant Physiol. 121, 1169–1177.CrossRefGoogle Scholar
  78. Zhu, Y.L., Pilon-Smits, E.A., Jouanin, L. and Terry, N. 1999b. Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119, 73–79.CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2001

Authors and Affiliations

  • David Salt
    • 1
  1. 1.Chemistry DepartmentNorthern Arizona UniversityFlagstaffUSA

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