Phytoremediation of toxic elemental and organic pollutants

Current Opinion in Plant Biology

Volumn 3, Issue 2, 2000, Pages 153-162

  Meagher, Richard B ^a  

^a Georgia 30602 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACCUMULATION; DETOXIFICATION; GENETIC ENGINEERING; HEAVY METAL REMOVAL; MINERALIZATION; PHYTOREMEDIATION; POLLUTANT; TRANSGENIC PLANT;

EID: 0034066584     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(99)00054-0     Document Type: Review

References (80)

1. Salt D.E., Smith R.D., Raskin I. Phytoremediation. Ann Rev Plant Physiol Plant Mol Biol. 49:1998;643-668. An excellent review on the uses of plants to clean-up the environment.
2. Rugh C.L., Bizily S.P., Meagher R.B. Phytoremediation of environmental mercury pollution. Ensley B., Raskin I. Phytoremediation of Toxic Metals: Using Plants to Clean-up the Environment. 1999;151-169 John Wiley and Sons, New York. This paper examines the phytoremediation of mercury pollution as an alternative to more commonly used physical methods.
3. Meagher R.B., Rugh C.L., Kandasamy M.K., Gragson G., Wang N.J. Engineered phytoremediation of mercury pollution in soil and water using bacterial genes. Terry W., Bañuelos G. Phytoremediation of Contaminated Soil and Water. 2000;201-219 Ann Arbor Press, Inc, Berkeley, California. The integration of a phytoremediation strategy for ionic and methyl mercury with the natural geochemical cycle for mercury is discussed in this paper in the light of concerns about methyl mercury biomagnification into predatory animal populations. The natural physiological properties of plants that make them excellent 'machines' for phytoremediation are outlined.
4. Cunningham S.D., Anderson T.A., Schwab P., Hsu F.C. Phytoremediation of soils contaminated with organic pollutants. Adv Agronomy. 56:1996;55-114.
5. Dittmer H.J. A quantitative study of the roots and root hairs of a winter rye plant (Secale cereale). Am J Bot. 24:1937;417-420.
6. Salt D.E., Prince R.C., Pickering I.J., Raskin I. Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 109:1995;1427-1433.
7. Salt D.E., Kramer U. Mechanisms of metal hyperaccumulation in plants. Raskin I., Enslely B.D. Phytoremediaton of Toxic Metals: Using Plants to Clean-up the Environment. 1999;231-246 John Wiley and Sons, New York.
8. Dushenkof S., Vasudev D., Kapulnik Y., Gleba D., Fleisher D., Ting K.C., Ensley B. Removal of uranium from water using terrestrial plants. Environ Sci Technol. 31:1997;3468-3474.
9. Heaton A.C.P., Rugh C.L., Wang N-J., Meagher R.B. Phytoremediation of mercury and methylmercury polluted soils using genetically engineered plants. J Soil Contam. 7:1998;497-509.
10. Raskin I., Smith R.D., Salt D.E. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol. 8:1997;221-226.
11. Dushenkov V., Nanda-Kumar P.B.A., Motto H., Raskin I. Rhizofiltration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Tech. 29:1995;1239-1245.
12. Maathuis F.J.M., Sanders D. Plasma membrane transport in context making sense out of complexity. Curr Opin Plant Biol. 2:1999;236-243. A review of the known genes and mechanisms effecting the plasma membrane transport of Ca(II), Na(I), K(I), Ba(II), Cd(II), phosphate, and nitrate.
13. Guerinot M.L., Eide D. Zeroing in on zinc uptake in yeast and plants. Curr Opin Plant Biol. 2:1999;244-249. A brief up-to-date examination of the biochemistry, molecular genetics, and known components involved in zinc uptake and transport.
14. Eng B.H., Guerinot M.L., Eide D., Saier M.H. Jr. Sequence, analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol. 166:1998;1-7. This paper publishes the sequence and predicted structural motifs of the ZIP family of heavy metal ion transporters. The Zrt- and Irt-related subclasses are defined.
15. Grotz N., Fox T., Connolly E., Park W., Guerinot M.L., Eide D. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA. 95:1998;7220-7224. The authors report the cloning of ZIP genes involved in root uptake and intracellular transport of zinc in Arabidopsis. The genes are characterized as to sequence, tissue specificity of expression, and mRNA induction during zinc deficiency.
16. Eide D., Broderius M., Fett J., Guerinot M.L. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA. 93:1996;5624-5628.
17. Cohen C.K., Fox T.C., Garvin D.F., Kochian L.V. The role of iron deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol. 116:1998;1063-1072. The uptake of Cd(II) in iron-deficient plants is shown to have at least two components: a concentration-dependent uptake into the cell wall and a saturatable uptake. The latter has a seven-times greater initial velocity when iron is deficient in comparison to conditions when adequate iron is available. Preliminary data suggest that Arabidopsis IRT1 could encode this transporter.
18. Yi Y., Guerinot M.L. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J. 10:1996;835-844.
19. + influx upon exposure to Al(III) at the root surface of the Al(III) resistant mutant alr-104. This influx resulted in an overall increase of 0.1 pH units at the root surface.
20. Pellet D.M., Grunes D.L., Kochian L.V. Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta. 196:1995;788-795.
21. Larsen P.B., Degenhardt J., Tai C.Y., Stenzler L.M., Howell S.H., Kochian L.V. Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol. 117:1998;9-18. Aluminum-resistant mutants of Arabidopsis mapping to one locus on chromosome I, alr-108, alr-128, alr-131, and alr-139, are shown to release greater amounts of citrate, malate, and/or pyruvate than wild-type plants and accumulate less aluminum.
22. de la Fuente J.M., Ramírez-Rodríguez V., Cabrera-Ponce J.L., Herrera-Estrella L. Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science. 276:1997;1566-1568.
23. 1H NMR and GC: analysis for organic osmolytes in crude tissue extracts. Anal Biochem. 214:1993;260-271.
24. Kinnersely A.M. The role of phytochelates in plant growth and productivity. Plant Growth Regul. 12:1993;207-217.
25. Huang J.W., Chen J., Berti W.R., Cunningham S.D. Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Tech. 31:1997;800-805.
26. 6 greater formation constant than Fe-EDDHA. J Plant Nutrition. 11:1988;1033-1050.
27. Vassil A.D., Kapulnik Y., Raskin I., Salt D.E. The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol. 117:1998;447-453. The use of 0.5 mM or more EDTA resulted in plants accumulating >1% w/w lead into shoot tissues in Pb-EDTA complexes; a 75-fold increase over the Pb concentration in the medium. Shoot Pb concentration is proportional to shoot EDTA levels and xylem sap shows the presence of Pb-EDTA complexes.
28. Baker A.J. Metal hyperaccumulator plants: a review of the biological resource for possible exploitation in the phytoremediation of metal-polluted soils. Terry N., Bañeulos G.S. Phytoremediation of Contaminated Soil and Water. 1999;85-107 CRC Press LLC, Boca Raton, Florida.
29. Kägi J.H., Schaffer A. Biochemistry of metallothionein. Biochemistry. 27:1988;8509-8515.
30. Chatthai M., Kaukinen K.H., Tranbarger T.J., Gupta P.K., Misra S. The isolation of a novel metallothionein-related cDNA expressed in somatic and zygotic embryos of Douglas-fir: regulation by ABA, osmoticum, and metal ions. Plant Mol Biol. 34:1997;243-254.
31. Zhou J., Goldsbrough P.B. Structure, organization and expression of the metallothionein gene family in Arabidopsis. Mol Gen Genet. 248:1995;318-328.
32. O'Halloran T., O'Halloran S.D. Metal responsive gene regulation and the zinc metalloregulatory model. Sigel H. Metal Ions in Biological Systems. 1995;558-578 Marcel Dekker, New York.
33. A in tandem arrays and its expression in transgenic tobacco plants. Protein Eng. 6:1993;755-762.
34. A can bind to metal in transgenic tobacco plants. Mol Gen Genet. 242:1994;666-674.
35. Brouwer M., Hoexum-Brouwer T., Cashon R.E. A putative glutathione-binding site in CdZn-metallothionein identified by equilibrium binding and molecular-modelling studies. Biochem J. 294:1993;219-225.
36. Salt D.E., Rauser W.E. MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 107:1995;1293-1301.
37. Pickering I.J., Prince R.C., George G.N., Rauser W.E., Wickramasinghe W.A., Watson A.A., Dameron C.T., Dance I.G., Fairlie D.P., Salt D.E. X-ray absorption spectroscopy of cadmium phytochelatin and model systems. Biochem Biophys Acta. 1429:1999;351-364.
38. Howden R., Andersen C.R., Goldsbrough P.B., Cobbett C.S. A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol. 107:1995;1067-1073.
39. Howden R., Goldsbrough P.B., Andersen C.R., Cobbett C.S. Cadmium-sensitive cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol. 107:1995;1059-1066.
40. Howden R., Cobbett C.S. Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 100:1992;100-107.
41. Zhu Y.L., Pilon-Smits E.A.H., Jouanin L., Terry N. Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119:1999;73-79. Expression of the Escherichia coli gshII gene in Indian mustard plants resulted in increased GSH and PC synthesis, suggesting glutathione synthetase catalyzes a rate-limiting step in PC synthesis.
42. Vatamaniuk O.K., Mari S., Lu Y.P., Rea P.A. AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci USA. 96:1999;7110-7115. Suppression cloning in yeast selected for heavy metal tolerance is used to isolate an Arabidopsis cDNA, AtPCS1, which encodes a 55 kDa putative phytochelatin synthase, gamma-glutamylcysteine dipeptidyl transpeptidase. Yeast expressing AtPSC1 accumulate excess Cd(II).
43. Clemens S., Kim E.J., Neumann D., Schroeder J.I. Tolerance to toxic metals by a gene family of phytochelatin syntheases from plants and yeast. EMBO J. 18:1999;3325-3333. Suppression cloning in yeast selected for heavy metal tolerance is used to isolate an expressed wheat cDNA, TaPCS1, encoding a 55 kDa PCS. PCS sequence homologues are identified in Arabidopsis, fission yeast, and lower animals; the first two of these also confer metal tolerance upon yeast. Genetic and biochemical studies demonstrate that this sequence in fission yeast encodes a bona fida PCS.
44. Baker A.J.M., Reeves R.D., Hajar A.S.H. Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl. (Brassicaceae). New Phytol. 127:1994;61-68.
45. Krämer U., Cotter-Howells J.D., Charnock J.M., Baker A.J.M., Smith J.A.C. Free histidine as a metal chelator in plants that accumulate nickel. Nature. 379:1996;635-638.
46. Salt D.E., Prince R.C., Baker A.J.M., Raskin I., Pickering I.J. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray adsorption spectroscopy. Environ Sci Tech. 33:1999;713-717.
47. Salt D.E., Kato N., Kramer U., Smith R.D., Raskin I. The role of root exudates in nickel hyperaccumulation and tolerance in accumulator and non-accumulator species of Thlaspi. Terry W., Bañuelos G. Phytoremediation of Contaminated Soil and Water. 2000;191-202 Ann Arbor Press, Inc, Berkeley, California.
48. Keating MH, Mahaffey KR, Schoeny R, Rice GE, Bullock OR, Ambrose RB, Swartout J, Nichols JW: Mercury Study Report to Congress. EPA452/R-9-003. US Environmental Protection Agency; 1997:1-51.
49. Harada M. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol. 25:1995;1-24.
50. Choi S.C., Chase J.T., Bartha R. Metabolic pathways leading to mercury methylation in Desulfovibrio desulfuricans LS. Appl Environ Microbiol. 60:1994;4072-4077.
51. Boischio A.A., Henshel D.S. Mercury contamination in the Brazilian Amazon. Environmental and occupational aspects. Water Air Soil Pollution. 80:1996;107-109.
52. Rugh C.L., Wilde D., Stack N.M., Thompson D.M., Summers A.O., Meagher R.B. Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci USA. 93:1996;3182-3187.
53. Rugh C.L., Senecoff J.F., Meagher R.B., Merkle S.A. Development of transgenic yellow-poplar for mercury phytoremediation. Nat Biotechnol. 16:1998;925-928. This paper reports the first trees engineered to clean-up a pollutant. Transgenic yellow poplar (Liriodendron tulipifera) calli and plants expressing the bacterial merA gene are shown to be resistant to Hg(II), which it detoxifies to rapidly volatized metallic Hg(0).
54. Meagher R.B., Rugh C.L. Phytoremediation of heavy metal pollution: ionic and methyl mercury. OECD Biotechnology for Water Use and Conservation Workshop. 1996;305-321 Organization for Economic Co-Operation and Development, Cocoyoc, Mexico.
55. Bizily S., Rugh C.L., Summers A.O., Meagher R.B. Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci USA. 96:1999;6808-6813. Plants expressing a bacterial organomercury lyase gene, merB, are resistant to a wide range of toxic levels of the environmental toxin methylmercury. Only a threshold level of MerB enzyme appears to be necessary to confer high level resistance, suggesting that complex kinetic and cell biological parameters effect resistance.
56. Bizily S., Rugh C.L., Meagher R.B. Efficient phytodetoxification of the environmental pollutant methylmercury by engineered plants. Nat Biotechnol. 2000;. in press. Plants expressing the two bacterial genes, merB and merA, are resistant to extremely high levels of the environmental toxin methylmercury. They volatilize 100-1000 times more Hg(0) than wild-type plants or controls expressing either gene alone. MerB enzyme levels appear to be rate limiting, but only account for 40% of the volatilization rate. Other unknown cell biological, biochemical, and kinetic parameters must play a significant role.
57. Pilon-Smits E.A., Hwang S., Mel Lytle C., Zhu Y., Tai J.C., Bravo R.C., Chen Y., Leustek T., Terry N. Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol. 119:1999;123-132. An Arabidopsis plastidic ATP sulfurylase gene (APS1) was over expressed in Indian mustard. APS1 activates not only sulfate but also selenate for uptake, and this appears to be a rate-limiting step for selanate reduction in plastids and for plant tolerance. Transgenic plants accumulate twice as much Se in shoots than do controls.
58. Neuhierl B., Bock A. On the mechanism of selenium tolerance in selenium-accumulating plants: purification and characterization of a specific selenocystein methyltransferase from cultured cells of Astragalus bisculatus. Eur J Biochem. 239:1996;235-238.
59. de Souza M.P., Pilon-Smits E.A., Lytle C.M., Hwang S., Tai J., Honma T.S., Yeh L., Terry N. Rate-limiting steps in selenium assimilation and volatilization by Indian mustard. Plant Physiol. 117:1998;1487-1494. The authors show that dimethylselenide is volatilized at two-to-three-times greater rates in plants supplied with selenite than those with selenate. Time-dependent kinetic studies showed that selenate was taken up twice as fast as selenite. Selenate was rapidly translocated to the shoot, away from the root which is the site of volatilization, ten-times more efficiently than selenite.
60. Terry N., Zayed A.M. Selenium volatilization by plants. Frankenberger W.T. Jr., Benson S. Selenium in the Environment. 1994;343-376 Marcel Dekker, Inc, New York.
61. Zayed A.M., Terry N. Selenium volatilization in roots and shoots: effects of shoot removal and sulfate level. J Plant Physiol. 143:1994;8-14.
62. de Souza M.P., Chu D., Zhao M., Zayed A.M., Ruzin S.E., Schichnes D., Terry N. Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol. 119:1999;565-574. When compared with axenic controls, plants inoculated with rhizosphere bacteria had five-times greater Se concentrations in roots (the site of volatilization) and four-times greater rates of Se volatilization. The presence of bacteria effected both root surface area and uptake.
63. Robinson N.J., Procter C.M., Connolly E.L., Guerinot M.L. A ferric-chelate reductase for iron uptake from soils. Nature. 397:1999;694-697. Iron deficiency afflicts > three billion people worldwide, and plants are the principal source of iron in most diets. The Arabidopsis FRO2 gene complements frd-1 mutations and encodes ferric-chelate reductase, a flavocytochrome that also transports electrons across a membrane. This activity is required for efficient iron uptake in many plants, and may result in the improved Fe-nutrition value of many crops.
64. Delhaize E. A metal-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 111:1996;849-855.
65. Tommasini R., Vogt E., Fromenteau M., Hortensteiner S., Matile P., Amrhein N., Martinoia E. An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J. 13:1998;773-780. AtMRPs are the Arabidopsis thaliana homologues of the human multidrug resistant protein, MRP. The Arabidopsis gene AtMRP3 is a homologue of the yeast genes MRP1 and yeast cadmium factor 1 (YCF1), which are ATP-binding-cassette-type GCPs. A cadmium-sensitive yeast mutant lacking endogenous GCP is complemented by AtMRP3 and definitive data are presented to show that AtMRP3 is a GCP.
66. Lu Y.P., Li Z.S., Drozdowicz Y.M., Hortensteiner S., Martinoia E., Rea P.A. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell. 10:1998;267-282.
67. Lu Y.P., Li Z.S., Rea P.A. 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. 94:1997;8243-8248.
68. Li Z.S., Alfenito M., Rea P.A., Walbot V., Dixon R.A. Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry. 45:1997;689-693.
69. 14C] trichoroethylene in the root zone of plants from a former solvent disposal site. Environ Toxicol Chem. 12:1996;2041-2047.
70. Anderson T.A., Guthrie E.A., Walton B.T. Bioremediation in the rhizosphere: plant roots and associated microbes clean contaminated soil. Environ Sci Tech. 27:1993;2630-2636.
71. 2 after several days of growth. In field trials, 95% of the TCE was removed from the influent water stream.
72. Wackett L.P., Sadowsky M.J., Newman L.M., Hur H.G., Li S. Metabolism of polyhalogenated compounds by a genetically engineered bacterium. Nature. 368:1994;627-629.
73. Best E.P., Zappi M.E., Fredrickson H.L., Sprecher S.L., Larson S.L., Ochman M. Screening of aquatic and wetland plant species for phytoremediation of explosives-contaminated groundwater from the Iowa Army Ammunition Plant. Ann NY Acad Sci. 829:1997;179-194.
74. Miskiniene V., Sarlauskas J., Jacquot J.P., Cenas N. Nitroreductase reactions of Arabidopsis thaliana thioredoxin reductase. Biochim Biophys Acta. 1366:1998;275-283. Arabidopsis thaliana NADPH:thioredoxin reductase catalyzed redox cycling of nitroaromatic compounds, including the explosives 2,4,6-trinitrotoluene and tetryl, and the herbicide 3,5-dinitro-o-cresol.
75. Hughes J.B., Shanks J., Vanderford M., Lauritzen J., Bhadra R. Transformation of TNT by aquatic plants and plant tissue cultures. Environ Sci Tech. 31:1997;266-271.
76. Goel A., Kumar G., Payne G.F., Dube S.K. Plant cell biodegradation of a xenobiotic nitrate ester, nitroglycerin. Nat Biotechnol. 15:1997;174-177.
77. Bhadra R., Wayment D.G., Hughes J.B., Shanks J.V. Confirmation of conjugation processes during TNT metabolism by axenic plant roots. Environ Sci Technol. 33:1999;446-452. The authors use numerous physical and biochemical techniques to examine the products of TNT reduction by cultures of Catharanthus roseus (see Figure 2).
78. French C.E., Rosser S.J., Davies G.J., Nicklin S., Bruce N.C. Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat Biotechnol. 17:1999;491-494. This work examines progress in the engineered phytoremediation of explosives. Expression of the bacterial pentaerythritol tetranitrate reductase gene in tobacco enables the growth and degradation of 1 mM glycerol trinitrate (GTN) or 0.05 mM trinitrotoluene (TNT), concentrations that inhibit the germination and growth of wild-type seeds.
79. Kas J., Burkard J., Demnerova K., Kostal J., Macek T., Mackova M., Pazlarova J. Perspectives in biodegradation of alkanes and PCBs. Pure Appl Chem. 69:1997;2357-2369.
80. Mackova M., Macek T., Ocenaskova J., Burkhard J., Demnerova K., Pazlarova J. Biodegradation of polychlorinated biphenyls by plant cells. Int Biodeterioration Biodegradation. 39:1997;317-324.