Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic

  • Richard B. Meagher
  • Andrew C. P. Heaton
Environmental Biotechnology


Plants have many natural properties that make them ideally suited to clean up polluted soil, water, and air, in a process called phytoremediation. We are in the early stages of testing genetic engineering-based phytoremediation strategies for elemental pollutants like mercury and arsenic using the model plant Arabidopsis. The long-term goal is to develop and test vigorous, field-adapted plant species that can prevent elemental pollutants from entering the food-chain by extracting them to aboveground tissues, where they can be managed. To achieve this goal for arsenic and mercury, and pave the way for the remediation of other challenging elemental pollutants like lead or radionucleides, research and development on native hyperaccumulators and engineered model plants needs to proceed in at least eight focus areas: (1) Plant tolerance to toxic elementals is essential if plant roots are to penetrate and extract pollutants efficiently from heterogeneous contaminated soils. Only the roots of mercury- and arsenic-tolerant plants efficiently contact substrates heavily contaminated with these elements. (2) Plants alter their rhizosphere by secreting various enzymes and small molecules, and by adjusting pH in order to enhance extraction of both essential nutrients and toxic elements. Acidification favors greater mobility and uptake of mercury and arsenic. (3) Short distance transport systems for nutrients in roots and root hairs requires numerous endogenous transporters. It is likely that root plasma membrane transporters for iron, copper, zinc, and phosphate take up ionic mercuric ions and arsenate. (4) The electrochemical state and chemical speciation of elemental pollutants can enhance their mobility from roots up to shoots. Initial data suggest that elemental and ionic mercury and the oxyanion arsenate will be the most mobile species of these two toxic elements. (5) The long-distance transport of nutrients requires efficient xylem loading in roots, movement through the xylem up to leaves, and efficient xylem unloading aboveground. These systems can be enhanced for the movement of arsenic and mercury. (6) Aboveground control over the electrochemical state and chemical speciation of elemental pollutants will maximize their storage in leaves, stems, and vascular tissues. Our research suggests ionic Hg(II) and arsenite will be the best chemical species to trap aboveground. (7) Chemical sinks can increase the storage capacity for essential nutrients like iron, zinc, copper, sulfate, and phosphate. Organic acids and thiol-rich chelators are among the important chemical sinks that could trap maximal levels of mercury and arsenic aboveground. (8) Physical sinks such as subcellular vacuoles, epidermal trichome cells, and dead vascular elements have shown the evolutionary capacity to store large quantities of a few toxic pollutants aboveground in various native hyperaccumulators. Specific plant transporters may already recognize gluthione conjugates of Hg(II) or arsenite and pump them into vacuole.


Methylmercury Biomagnification Arabidopsis Cottonwood merA, merB, ArsC, ECS 



I would like to thank Drs. Aaron Smith, Gay Gragson, and Tehryung Kim for editorial comments on this manuscript. This work was supported by grants from Department of Energy’s Environmental Management Sciences program (DEG0796ER20257) and Biological and Environmental Research program (DEFG0203ER63620).


  1. 1.
    Agostini E, Hernandez-Ruiz J, Arnao MB, Milrad SR, Tigier HA, Acosta M (2002) A peroxidase isoenzyme secreted by turnip (Brassica napus) hairy-root cultures: inactivation by hydrogen peroxide and application in diagnostic kits. Biotechnol Appl Biochem 35:1–7CrossRefPubMedGoogle Scholar
  2. 2.
    Anderson TA, Guthrie EA, Walton BT (1993) Bioremediation in the rhizosphere: plant roots and associated microbes clean contaminated soil. Environ Sci Technol 27:2630–2636CrossRefGoogle Scholar
  3. 3.
    Arabidopsis GI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefPubMedGoogle Scholar
  4. 4.
    Arango M, Gevaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365PubMedGoogle Scholar
  5. 5.
    Baker AJ (2000) Metal hyperaccumulator plants: a review of the biological resource for possible exploitation in the phytoremediaton of metal-polluted soils. In: Terry N, Baneulos GS (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, FL, pp 85–107Google Scholar
  6. 6.
    Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal accumulating plants. Resour Conserv Recycling 11:41–49CrossRefGoogle Scholar
  7. 7.
    Baldwin JC, Karthikeyan AS, Raghothama KG (2001) Leps2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125:728–737PubMedGoogle Scholar
  8. 8.
    Barinaga M (1997) Making plants aluminum tolerant. Science 276:1497CrossRefGoogle Scholar
  9. 9.
    Barkay T, Turner R, Saouter E, Horn J (1992) Mercury biotransformations and their potential for remediation of mercury contamination. Biodegradation 3:147–159CrossRefGoogle Scholar
  10. 10.
    Bizily S (2001) Genetic engineering of plants with the bacterial genes merA and merB for the phytoremediation of methylmercury contaminated sediments. PhD Thesis, Genetics Department, University of GeorgiaGoogle Scholar
  11. 11.
    Bizily S, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci USA 96:6808–6813PubMedGoogle Scholar
  12. 12.
    Bizily S, Rugh CL, Meagher RB (2000) Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biotechnol 18:213–217CrossRefPubMedGoogle Scholar
  13. 13.
    Bizily S, Kim T, Kandasamy MK, Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol 131:463–471CrossRefPubMedGoogle Scholar
  14. 14.
    Brands A, Ho TH (2002) Function of a plant stress-induced gene, HVA22. Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic. Plant Physiol 130:1121–1131PubMedGoogle Scholar
  15. 15.
    Bucking H, Heyser W (2003) Uptake and transfer of nutrients in ectomycorrhizal associations: interactions between photosynthesis and phosphate nutrition. Mycorrhiza 13:59–68PubMedCrossRefGoogle Scholar
  16. 16.
    Burkle L, Cedzich A, Dopke C, Stransky H, Okumoto S, Gillissen B et al (2003) Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J 34:13–26CrossRefPubMedGoogle Scholar
  17. 17.
    Che DS, Meagher RB, Heaton ACP, Lima A, Merkle SA (2003) Expression of mercuric ion reductase in eastern cottonwood confers mercuric ion reduction and resistance. Plant Biotechnol 1:311–319CrossRefGoogle Scholar
  18. 18.
    Cherel I (2004) Regulation of K+ channel activities in plants: from physiological to molecular aspects. J Exp Bot 55:337–351CrossRefPubMedGoogle Scholar
  19. 19.
    Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T et al (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213:45–50CrossRefPubMedGoogle Scholar
  20. 20.
    Cobbett C, Meagher R (2002) Phytoremediation and the Arabidopsis proteome. Meyerowitz E, Somerville C (eds) Arabidopsis. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY, pp 1–22Google Scholar
  21. 21.
    Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072CrossRefPubMedGoogle Scholar
  22. 22.
    Cunningham SD, Berti WR (1993) Remediation of contaminated soils with green plants: an overview. In Vitro Cell Dev Biol 29:207–212Google Scholar
  23. 23.
    Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719PubMedGoogle Scholar
  24. 24.
    Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol 13:393–397CrossRefGoogle Scholar
  25. 25.
    Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20:581–586CrossRefPubMedGoogle Scholar
  26. 26.
    Darwin C (1900) The variation of animals and plants under domestication. Appleton, New York, pp 413–414Google Scholar
  27. 27.
    Debette J, Blondeau R (1980) Presence of Pseudomonas maltophilia in the rhizosphere of several cultivated plants. Can J Microbiol 26:460–463PubMedGoogle Scholar
  28. 28.
    De la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568PubMedGoogle Scholar
  29. 29.
    Delorme TA, Gagliardi JV, Angle JS, Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J.& C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can J Microbiol 47:773–776CrossRefPubMedGoogle Scholar
  30. 30.
    De Souza MP, Chu D, Zhao M, Zayed AM, Ruzin SE, Schichnes D et al (1999) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol 119:565–574CrossRefPubMedGoogle Scholar
  31. 31.
    Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF et al (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145CrossRefPubMedGoogle Scholar
  32. 32.
    Doty SL, Shang TQ, Wilson AM, Tangen J, Westergreen AD, Newman LA et al (2000) Enhanced metabolism of halogenated hydrocarbons in transgenic plants containing mammalian cytochrome P450 2E1. Proc Natl Acad Sci USA 97:6287–6291PubMedGoogle Scholar
  33. 33.
    Ebbs SD, Lasat MM, Brady DJ, Cornish J, Gordon R, Kochian LV (1997) Phytoextraction of cadmium and zinc from a contaminated soil. J Environ Qual 26:1424–1430Google Scholar
  34. 34.
    El-Gibaly MH, El-Reweiny FM, Abdel-Nasser M, El-Dahtory TA (1977) Studies on phosphate-solubilizing bacteria in soil and rhizosphere of different plants. I. Occurrence of bacteria, acid producers, and phosphate dissolvers. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 132:233–239PubMedGoogle Scholar
  35. 35.
    Eng BH, Guerinot ML, Eide D, Saier MH Jr (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166:1–7CrossRefPubMedGoogle Scholar
  36. 36.
    Fan TW, Lane AN, Pedler J, Crowley D, Higashi RM (1997) Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatography-mass spectrometry. Anal Biochem 251:57–68CrossRefPubMedGoogle Scholar
  37. 37.
    Fan TW, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57:209–221CrossRefPubMedGoogle Scholar
  38. 38.
    Fischer WN, Loo DD, Koch W, Ludewig U, Boorer KJ, Tegeder M et al (2002) Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J 29:717–731CrossRefPubMedGoogle Scholar
  39. 39.
    Fox T, Gueriont M (1998) Molecular biology of cation transport in plants. Annu Rev Plant Physiol Plant Mol Biol 49:669–696CrossRefPubMedGoogle Scholar
  40. 40.
    Foy C, Burns G, Brown J, Fleming A (1965) Differential aluminum tolerance of two wheat varieties associated with plant-induced pH changes around their roots. Soil Sci Soc Am Proc 29:64–67CrossRefGoogle Scholar
  41. 41.
    French CE, Rosser SJ, Davies GJ, Nicklin S, Bruce NC (1999) Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat Biotechnol 17:491–494CrossRefPubMedGoogle Scholar
  42. 42.
    Gessler A, Weber P, Schneider S, Rennenberg H (2003) Bidirectional exchange of amino compounds between phloem and xylem during long-distance transport in Norway spruce trees (Picea abies [L.] Karst). J Exp Bot 54:1389–1397CrossRefPubMedGoogle Scholar
  43. 43.
    Gillespie AR, Pope PE (1991) Consequences of rhizosphere acidification on delivery and uptake kinetics of soil phosphorus. Tree Physiol 8:195–204PubMedGoogle Scholar
  44. 44.
    Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60CrossRefPubMedGoogle Scholar
  45. 45.
    Grotz N, Guerinot ML (2002) Limiting nutrients: an old problem with new solutions? Curr Opin Plant Biol 5:158–163CrossRefPubMedGoogle Scholar
  46. 46.
    Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95:7220–7224CrossRefPubMedGoogle Scholar
  47. 47.
    Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198PubMedGoogle Scholar
  48. 48.
    Hakanson L (1997) Health impacts of large releases of radionuclides. Transport and processes in freshwater ecosystems. Ciba Found Symp 203:46–64PubMedGoogle Scholar
  49. 49.
    Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902CrossRefPubMedGoogle Scholar
  50. 50.
    Hannink N, Rosser SJ, French CE, Basran A, Murray JA, Nicklin S et al (2001) Phytodetoxification of TNT by transgenic plants expressing a bacterial nitroreductase. Nat Biotechnol 19:1168–1172CrossRefPubMedGoogle Scholar
  51. 51.
    Haran S, Logendra S, Seskar M, Bratanova M, Raskin I (2000) Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol 124:615–626CrossRefPubMedGoogle Scholar
  52. 52.
    Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327CrossRefPubMedGoogle Scholar
  53. 53.
    Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133CrossRefPubMedGoogle Scholar
  54. 54.
    Heaton ACP, Rugh CL, Wang N-J, Meagher RB (1998) Phytoremediation of mercury and methylmercury polluted soils using genetically engineered plants. J Soil Contam 7:497–509CrossRefGoogle Scholar
  55. 55.
    Heaton ACP, Rugh CL, Kim T, Wang NJ, Meagher RB (2003) Toward detoxifying mercury-polluted aquatic sediments using rice genetically engineered for mercury resistance. Environ Toxicol Chem 22:2940–2947CrossRefPubMedGoogle Scholar
  56. 56.
    Heaton ACP, Rugh CL, Wang N-J, Meagher RB (2005) Physiological responses of transgenic merA-tobacco (Nicotiana tabacum) to foliar and root mercury exposure. Water Air Soil Pollut 161:137–155 CrossRefGoogle Scholar
  57. 57.
    Higashi RM, Fan TW-M, Lane AN (1998) Association of desferrioxamine with humic substances and their interaction cadmium(II) as studied by pyrolysis-gas chromatography-mass spectrometry and nuclear magnetic resonance spectroscopy. Analyst 123:911–918CrossRefGoogle Scholar
  58. 58.
    Hirner B, Fischer WN, Rentsch D, Kwart M, Frommer WB (1998) Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. Plant J 14:535–544CrossRefPubMedGoogle Scholar
  59. 59.
    Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2003) Three rice nicotianamine synthase genes, OsNAS1 OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J 36:366–381CrossRefPubMedGoogle Scholar
  60. 60.
    Ivry B (2004) Uprooting toxic waste, cheaply. Pop Sci 264:41–44Google Scholar
  61. 61.
    Johansen JE, Binnerup SJ (2002) Contribution of cytophaga-like bacteria to the potential of turnover of carbon, nitrogen, and phosphorus by bacteria in the rhizosphere of barley (Hordeum vulgare L.). Microb Ecol 43:298–306CrossRefPubMedGoogle Scholar
  62. 62.
    Kagan IA, Rimando AM, Dayan FE (2003) Chromatographic separation and in vitro activity of sorgoleone congeners from the roots of sorghum bicolor. J Agric Food Chem 51:7589–7595CrossRefPubMedGoogle Scholar
  63. 63.
    Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233PubMedGoogle Scholar
  64. 64.
    Kerkeb L, Kramer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724CrossRefPubMedGoogle Scholar
  65. 65.
    Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A et al (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14:775–784PubMedGoogle Scholar
  66. 66.
    Kramer U, Chardonnens AN (2001) The use of transgenic plants in the bioremediation of soils contaminated with trace elements. Appl Microbiol Biotechnol 55:661–672CrossRefPubMedGoogle Scholar
  67. 67.
    Kramer U, CotterHowells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638CrossRefGoogle Scholar
  68. 68.
    Kupper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84CrossRefPubMedGoogle Scholar
  69. 69.
    Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117:9–18CrossRefPubMedGoogle Scholar
  70. 70.
    Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA (1997) A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc Natl Acad Sci USA 94:42–47CrossRefPubMedGoogle Scholar
  71. 71.
    Liu G, Sanchez-Fernandez R, Li ZS, Rea PA (2001) Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J Biol Chem 276:8648–8656CrossRefPubMedGoogle Scholar
  72. 72.
    Lu YP, Li ZS, Rea PA (1997) AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc Natl Acad Sci USA 94:8243–8248CrossRefPubMedGoogle Scholar
  73. 73.
    Luo YM, Christie P, Baker AJ (2000) Soil solution Zn and pH dynamics in non-rhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cd-contaminated soil. Chemosphere 41:161–164CrossRefPubMedGoogle Scholar
  74. 74.
    Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579CrossRefPubMedGoogle Scholar
  75. 75.
    Macy JM, Nunan K, Hagen KD, Dixon DR, Harbour PJ, Cahill M et al (1996) Chrysiogenes arsenatis gen. nov., sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. Int J Syst Bacteriol 46:1153–1157PubMedCrossRefGoogle Scholar
  76. 76.
    Marschner H (1995) Mineral nutrition of higher plants. Academic, New YorkGoogle Scholar
  77. 77.
    Matsui T, Nakayama H, Yoshida K, Shinmyo A (2003) Vesicular transport route of horseradish C1a peroxidase is regulated by N- and C-terminal propeptides in tobacco cells. Appl Microbiol Biotechnol 62:517–522CrossRefPubMedGoogle Scholar
  78. 78.
    Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162CrossRefPubMedGoogle Scholar
  79. 79.
    Meagher RB, Rugh CL (1996) Phytoremediation of heavy metal pollution: ionic and methyl mercury. OECD Biotechnology for Water Use and Conservation Workshop, pp 305–321Google Scholar
  80. 80.
    Meagher RB, Rugh CL, Kandasamy MK, Gragson G, Wang NJ (2000) Engineered phytoremediation of mercury pollution in soil and water using bacterial genes. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL, pp 203–221Google Scholar
  81. 81.
    Miller SS, Liu J, Allan DL, Menzhuber CJ, Fedorova M, Vance CP (2001) Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiol 127:594–606CrossRefPubMedGoogle Scholar
  82. 82.
    Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987CrossRefPubMedGoogle Scholar
  83. 83.
    Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK (2003) Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiol 132:1989–1997CrossRefPubMedGoogle Scholar
  84. 84.
    Monni S, Bucking H, Kottke I (2002) Ultrastructural element localization by EDXS in Empetrum nigrum. Micron 33:339–351CrossRefPubMedGoogle Scholar
  85. 85.
    Morikawa H, Erkin OC (2003) Basic processes in phytoremediation and some applications to air pollution control. Chemosphere 52:1553–1558CrossRefPubMedGoogle Scholar
  86. 86.
    Muchhal US, Raghothama KG (1999) Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci USA 96:5868–5872CrossRefPubMedGoogle Scholar
  87. 87.
    Noble AD, Sumner ME, Alva AK (1988) The pH dependency of aluminum phytotoxicity alleviation by calcium sulfate. Soil Sci Soc Am J 52:1398–1402CrossRefGoogle Scholar
  88. 88.
    Nriagu E (1994) Arsenic in the environment. In: Nriagu JO (ed) Part I: cycling and characterization. Wiley, New York, p 430Google Scholar
  89. 89.
    Nublat A, Desplans J, Casse F, Berthomieu P (2001) sas1, an Arabidopsis mutant overaccumulating sodium in the shoot, shows deficiency in the control of the root radial transport of sodium. Plant Cell 13:125–137CrossRefPubMedGoogle Scholar
  90. 90.
    Odunfa SA, Werner D (1981) Root exudates in relation to growth and nitrogenase activity of Rhizobium japonicum. Z Allg Mikrobiol 21:601–606PubMedGoogle Scholar
  91. 91.
    Park SW, Lawrence CB, Linden JC, Vivanco JM (2002) Isolation and characterization of a novel ribosome-inactivating protein from root cultures of pokeweed and its mechanism of secretion from roots. Plant Physiol 130:164–178CrossRefPubMedGoogle Scholar
  92. 92.
    Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795CrossRefGoogle Scholar
  93. 93.
    Persans MW, Yan X, Patnoe JM, Kramer U, Salt DE (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halacsy). Plant Physiol 121:1117–1126CrossRefPubMedGoogle Scholar
  94. 94.
    Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiol 122:1171–1177CrossRefPubMedGoogle Scholar
  95. 95.
    Pomeroy LR, Darley WM, Dunn EL, Gallagher JL, Haines EB, Whitney DM (1981) Salt marsh populations: primary production. In: Pomeroy LR, Wiegert RG (eds) The ecology of the salt marsh. Springer, Berlin Heidelberg New York, pp 39–67Google Scholar
  96. 96.
    Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113–1122CrossRefPubMedGoogle Scholar
  97. 97.
    Raghothama K (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693CrossRefPubMedGoogle Scholar
  98. 98.
    Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187PubMedGoogle Scholar
  99. 99.
    Raghothama KG (2000) Phosphorus acquisition; plant in the driver’s seat!. Trends Plant Sci 5:412–413CrossRefPubMedGoogle Scholar
  100. 100.
    Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G et al (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470CrossRefPubMedGoogle Scholar
  101. 101.
    Rea P (1999) MRP subfamily ABC transporters from plants and yeast. J Exp Bot 50:895–913CrossRefGoogle Scholar
  102. 102.
    Reeves RD, Baker AJM, Brooks RR (1995) Abnormal accumulation of trace metals by plants. Min Environ Manage 3:1–19Google Scholar
  103. 103.
    Reid R, Hayes J (2003) Mechanisms and control of nutrient uptake in plants. Int Rev Cytol 229:73–114PubMedCrossRefGoogle Scholar
  104. 104.
    Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649CrossRefPubMedGoogle Scholar
  105. 105.
    Rothman J, Stevens T (1986) Protein sorting in yeast: mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway. Cell 47:1041–1051CrossRefPubMedGoogle Scholar
  106. 106.
    Rougier M (1981) Secretory activity of the root cap. In: Tannar W, Loewus FA (eds) Encyclopedia of plant physiology: plant carbohydrates II: NS. Springer, Berlin Heidelberg New York, pp 542–574Google Scholar
  107. 107.
    Rugh CL, Wilde D, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci USA 93:3182–3187CrossRefPubMedGoogle Scholar
  108. 108.
    Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928CrossRefPubMedGoogle Scholar
  109. 109.
    Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352CrossRefPubMedGoogle Scholar
  110. 110.
    Salt DE, Kramer U (1999) Mechanisms of metal hyperaccumulation in plants. In: Raskin I, Enslely BD (eds) Phytoremediaton of toxic metals: using plants to clean up the environment. Wiley, New York, pp 231–246Google Scholar
  111. 111.
    Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann JL, Traverse A et al (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826CrossRefPubMedGoogle Scholar
  112. 112.
    Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084CrossRefPubMedGoogle Scholar
  113. 113.
    Schneiker S, Keller M, Droge M, Lanka E, Puhler A, Selbitschka W (2001) The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res 29:5169–5181CrossRefPubMedGoogle Scholar
  114. 114.
    Shann JR (1995) The role of plants and plant/microbial systems in the reduction of exposure. Environ Health Perspect 103[Suppl 5]:13–15Google Scholar
  115. 115.
    Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. Plant Cell 14:465–477CrossRefPubMedGoogle Scholar
  116. 116.
    Siebrecht S, Herdel K, Schurr U, Tischner R (2003) Nutrient translocation in the xylem of poplar–diurnal variations and spatial distribution along the shoot axis. Planta 217:783–793CrossRefPubMedGoogle Scholar
  117. 117.
    Snowden KC, Gardner RC (1993) Five genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiol 103:855–861CrossRefPubMedGoogle Scholar
  118. 118.
    Spaink HP (1994) The molecular basis of the host specificity of the Rhizobium bacteria. Antonie Van Leeuwenhoek 65:81–98CrossRefPubMedGoogle Scholar
  119. 119.
    Takahashi H, Brown CS, Dreschel TW, Scott TK (1992) Hydrotropism in pea roots in a porous-tube water delivery system. HortScience 27:430–432Google Scholar
  120. 120.
    Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182CrossRefPubMedGoogle Scholar
  121. 121.
    Tanner W, Beevers H (2001) Transpiration, a prerequisite for long-distance transport of minerals in plants? Proc Natl Acad Sci USA 98:9443–9447CrossRefPubMedGoogle Scholar
  122. 122.
    Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844CrossRefPubMedGoogle Scholar
  123. 123.
    Tommasini R, Vogt E, Fromenteau M, Hortensteiner S, Matile P, Amrhein N et al (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll-catabolite transport activity. Plant J 13:773–780CrossRefPubMedGoogle Scholar
  124. 124.
    Tordoff GM, Baker AJ, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228CrossRefPubMedGoogle Scholar
  125. 125.
    Vassilev A, Schwitzguebel JP, Thewys T, Van Der Lelie D, Vangronsveld J (2004) The use of plants for remediation of metal-contaminated soils. Sci World J 4:9–34Google Scholar
  126. 126.
    Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233CrossRefPubMedGoogle Scholar
  127. 127.
    Waldron LJ, Terry N (1975) Effect of mercury vapor on sugar beets. J Environ Qual 4:58–60CrossRefGoogle Scholar
  128. 128.
    Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135:400–411CrossRefPubMedGoogle Scholar
  129. 129.
    Watanabe T, Osaki M (2002) Role of organic acids in aluminum accumulation and plant growth in Melastoma malabathricum. Tree Physiol 22:785–792PubMedGoogle Scholar
  130. 130.
    Webb SM, Gaillard JF, Ma LQ, Tu C (2003) XAS speciation of arsenic in a hyper-accumulating fern. Environ Sci Technol 37:754–760CrossRefPubMedGoogle Scholar
  131. 131.
    Wegner LH, Zimmermann U (2002) On-line measurements of K+ activity in the tensile water of the xylem conduit of higher plants. Plant J 32:409–417CrossRefPubMedGoogle Scholar
  132. 132.
    Wolz S, Fenske RA, Simcox NJ, Palcisko G, Kissel JC (2003) Residential arsenic and lead levels in an agricultural community with a history of lead arsenate use. Environ Res 93:293–300CrossRefPubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology 2005

Authors and Affiliations

  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA

Personalised recommendations