Advances in development of transgenic plants for remediation of xenobiotic pollutants

Biotechnology Advances

Volumn 25, Issue 5, 2007, Pages 442-451

  Eapen, Susan ^a   Singh, Sudhir ^a   D'Souza, S F ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

Phytoremediation; Transgenic plants; Xenobiotics

Indexed keywords

PHYTOREMEDIATION; XENOBIOTIC COMPOUNDS; XENOBIOTIC DEGRADATION; XENOBIOTIC POLLUTANTS;

ETHYLENE; GENES; MICROORGANISMS; TOXIC MATERIALS;

PLANTS (BOTANY);

XENOBIOTIC AGENT;

BIODEGRADATION; DETOXIFICATION; GENE TRANSFER; ORGANIC POLLUTANT; PHYTOREMEDIATION; TRANSGENIC PLANT; XENOBIOTICS;

BIOLOGICAL MODEL; BIOREMEDIATION; BIOTECHNOLOGY; CHEMISTRY; DANGEROUS GOODS; ECOSYSTEM RESTORATION; GENETIC ENGINEERING; METABOLISM; METHODOLOGY; MUTAGENESIS; PLANT; POLLUTION; REVIEW; RISK ASSESSMENT; SOIL POLLUTANT; TRANSGENIC PLANT; WATER POLLUTANT;

BIODEGRADATION, ENVIRONMENTAL; BIOTECHNOLOGY; ENVIRONMENTAL POLLUTION; ENVIRONMENTAL REMEDIATION; GENETIC ENGINEERING; HAZARDOUS SUBSTANCES; MODELS, BIOLOGICAL; MUTAGENESIS; PLANTS; PLANTS, GENETICALLY MODIFIED; RISK ASSESSMENT; SOIL POLLUTANTS; WATER POLLUTANTS, CHEMICAL; XENOBIOTICS;

EUKARYOTA;

EID: 34447259825     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2007.05.001     Document Type: Review

References (104)

1. Adamia G., Ghoghoberidze M., Graves D., Khatisashvili G., Kvesitadze G., Lomidze E., et al. Absorption distribution and transformation of TNT in higher plants. Ecotoxicol Environ Saf 64 (2006) 136-145
2. Agostini E., Coniglio M.S., Milrad S.R., Tigier H.A., and Giulietti A.M. Phytoremediation of 2, 4-dichlorophenol by Brassica napus hairy root cultures. Biotechnol Appl Biochem 37 (2003) 139-144
3. Araujo B.S.-d., Charlwood B.V., and Pletsch M. Tolerance and metabolism of phenol and chloro derivatives by hairy root cultures of Daucus carota L. Environ Pollut 117 2 (2002) 329-335
4. Araujo B.S.-d., Dec J., Bollag J.M., and Pletsch M. Uptake and transformation of phenol and chlorophenols by hairy root cultures of Daucus carota, Ipomoea batatus and Solanum aviculare. Chemosphere 63 (2006) 642-651
5. Banerjee S., Shang T.Q., Wilson A.M., Moore A.L., Strand S.E., Gordon M.P., et al. Expression of functional mammalian P450 2EI in hairy root cultures. Biotechnol Bioeng 77 (2002) 462-466
6. Bhadra R., Wayment D.G., Hughes J.B., and Shanks J.V. Confirmation of conjugation processes during TNT metabolism by axenic plant roots. Environ Sci Technol 33 3 (1999) 446-452
7. Bhadra R., Wayment D.G., Williams R.K., Barman S.N., Stone M.B., Hughes J.B., et al. Studies on plant mediated fate of the explosives RDX and HMX. Chemosphere (2001) 1259-1264
8. Brandt R., Merkl N., Schultze-Kraft R., Infante C., and Broll G. Potential of vetiver (Vetiveria zizanoides L. Nash) for phytoremediation of hydrocarbon contaminated soils in Venezuela. Int J Phytoremediation 8 (2006) 273-284
9. Burken J.G., and Schnoor J.L. Uptake and metabolism of atrazine by poplar trees. Environ Sci Technol 31 (1997) 1399-1406
10. Burken J.G., Shanks J.V., and Thompson P.L. Phytoremediation and plant metabolism of explosives and nitroaromatic compounds. In: Spian J., Hughes J.B., and Knackmuss H.J. (Eds). Biodegradation of nitroaromatic compounds and explosives (2000), Lewin Publishers, Boca Raton 357-395
11. Castro S., Davis L.C., and Erickson L.E. Phytotransformation of benzotriazoles. Int J Phytoremediation 5 (2003) 245-265
12. Cherian S., and Oliveira M. Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Tech 39 (2005) 9377-9390
13. Coleman J.O.D., Blake-Kalff M.A.A., and Emyr Davis T.G. Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentalisation. Trends Plant Sci 2 (1997) 144-151
14. Coleman J.O., Frova C., Schroder P., and Tussut M. Exploiting plant metabolism for phytoremediation of persistent herbicides. Environ Sci Pollut Res Int 9 (2002) 18-28
15. Cunningham S.D., Berti W.R., and Huang J.W. Phytoremediation of contaminated soils. Trends Biotechnol 13 (1995) 393-397
16. Cunningham S.D., Anderson T.A., Schwab A.P., and Hsu F. Phytoremediation of soils contaminated with organic pollutants. Adv Agron 56 (1996) 55-114
17. Davison J. Risk mitigation of genetically modified bacteria and plants designed for bioremediation. J Ind Microbiol Biotech 32 (2005) 639-650
18. Didierjean L., Gondet L., Perkins R., Lau S.M., Schaller H., O'Keefe, et al. Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol 130 (2002) 179-189
19. Dietz A.C., and Schnoor J.L. Advances in phytoremediation. Environ Health Perspect 109 (2001) 163-168
20. Doty S.L., Shang T.Q., Wilson A.M., Tangen J., Westergreen A.D., Newman L.A., et al. Enhanced metabolism of halogenated hydrocarbons in transgenic plants containing mammalian cytochrome P450 2E1. Proc Natl Acad Sci U S A 97 (2000) 6287-6291
21. Doty S.L., Shang T.Q., Wilson A.M., Moore A.L., Newman L.A., Strand S.E., et al. Metabolism of the soil and groundwater contaminants, ethylene dibromide and trichloroethylene by the tropical leguminous tree, Leuceana leucocephala. Water Res 37 (2003) 441-449
22. Eapen S., and D'Souza S.F. Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23 (2005) 97-114
23. Eckman D.R., Lorenz W.W., Przybyla A.E., Wolfe N.L., and Dean J.F.D. SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiol 133 (2003) 1397-1406
24. Edwards R.J. Targeting antipeptide antibodies towards cytochrome P450 enzymes. In: Philips I.R., and Shepard E.A. (Eds). Methods in molecular biology vol. 107 (1998), Humana press, Totawa, NJ 239-249
25. Edwards R., Dixon D.P., and Walbot V. Plant glutathione-S-transferase: enzyme with multiple functions in sickness and in health. Trends Plant Sci 5 (2000) 193-198
26. Fletcher J.S., Donelly P.K., and Hedge R.S. Biostimuation of PCB-degrading bacteria by compounds released from plant roots. In: Hinchee R.E., Anderson D.B., and Hoeppel R.E. (Eds). Bioremediation of recalcitrant organics (1995), Battelle Press, Columbia 131-136
27. Flocco C.G., Lindblom S.D., and Smits E.A.H.P. Overexpression of enzymes involved in glutathione synthesis enhances tolerance to organic pollutants in Brassica juncea. Int J Phytoremediation 6 (2004) 289-304
28. Francova K., Macek T., Demnerova, and Mackova M. Transgenic plants-a potential tool for decontamination of environmental pollutants. Chem Listy 95 (2001) 630-637
29. Francova K., Sura M., Macek T., Szekeres M., Bancos S., Demnerova K., et al. Preparation of plants containing bacterial enzyme for degradation of polychlorinated biphenyls. Fresenius Environ Bull 12 (2003) 309-313
30. French C.E., Rosser S.J., Davies G.J., Nicklin S., and Bruce N.C. Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat Biotechnol 17 (1999) 491-494
31. Goel A., Kumar G., Payne G.F., and Dube S.K. Plant cell biodegradation of a xenobiotic nitrate ester nitroglycerin. Nat Biotechnol 15 (1997) 174-177
32. Goldstein R.M., Mallory L.M., and Alexander M. Reasons for possible failure of inoculation to enhance bioremediation. Appl Environ Microbiol 50 (1985) 977-983
33. Groom C.A., Halasz A., Paquet L., Morris N., Olivier L., Dubois C., et al. Accumulation of HMX (Octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine) in indigenous and agricultural plants grown in HMX-contaminated anti-tank firing-range soil. Environ Sci Technol 36 (2002) 112-118
34. Hannink N.K., Rosser S.J., French C.E., Basran A., Murray J.A.H., Nicklin S., et al. Phyto-detoxification of TNT by transgenic plants expressing a bacterial nitroreductase. Nat Biotechnol 19 (2001) 1168-1172
35. Hannink N.K., Rosser S.J., French C.E., and Bruce N.C. Uptake and metabolism of TNT and GTN by plants expressing bacterial pentaerythritol tetranitrate reductase. Water Air Soil Pollut 3 3 (2003) 251-258
36. Hatzios K.K. Regulation of enzymatic system detoxifying xenobiotics in plants: a brief overview and directions for future research. In: Hatzios K.K. (Ed). Regulation of enzymatic systems detoxifying xenobiotics in plants (1997), Kluwer Acad. Pub., Netherlands 1-5
37. Hatzios K.K., and Burgos N. Metabolism based herbicide resistance: regulation by safeners. Weed Sci 52 (2004) 454-467
38. Hirose S., Kawahigashi H., Inoue T., Inui H., Ohkawa H., and Ohkawa Y. Enhanced expression of CYP2C9 and tolerance to sulfonylurea herbicides in transgenic rice plants. Plant Biotechnol 22 (2005) 89-96
39. Hughes J.B., Shanks J., Vanderford M., Lauritzen J., and Bhadra R. Transformation of TNT by aquatic plants and plant tissue cultures. Environ Sci Technol 31 (1997) 266-271
40. Inui H., and Ohkawa H. Herbicide resistance in transgenic plants with mammalian P450 monooxygenase genes. Pest Manag Sci 61 (2005) 286-291
41. Jansen M.A.K., Hill L.M., and Thorneley R.N.F. A novel stress-acclimation response in Spirodela punctata (Lemnaceae): 2,4,6-trichlorophenol triggers an increase in the level of an extracellular peroxidase, capable of the oxidative dechlorination of this xenobiotic pollutant. Plant Cell Environ 27 (2004) 603-613
42. Karavangeli M., Labrou N.E., Clonis Y.D., and Tsaftaris A. Development of transgenic tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide herbicides phytoremediation. Biomol Eng 22 (2005) 121-128
43. Kawahigashi H., Hirose S., Hayashi E., Ohkawa H., and Ohkawa Y. Phytotoxicity and metabolism of ethofumesate in transgenic rice plants expressing human CYP2B6 gene. Pestic Biochem Physiol 74 (2002) 139-147
44. Kawahigashi H., Hirose S., Ohkawa H., and Ohkawa Y. Phytoremediation of metolachlor by transgenic rice plants expressing human CYP2B6. J Agric Food Chem 53 (2005) 9155-9160
45. Kawahigashi H., Hirose S., Ohkawa H., and Ohkawa Y. Transgenic rice plants expressing human CYP1A1 remediate the triazine herbicides Atrazine and Simazine. J Agric Food Chem 53 (2005) 8557-8564
46. Kawahigashi H., Hirose S., Ozawa K., Ido Y., Kojima M., Ohkawa H., et al. Analysis of substrate specificity of pig CYP2B22 and CYP2C49 towards herbicides by transgenic rice plants. Transgenic Res 14 (2005) 907-917
47. Kawahigashi H., Hirose S., Ohkawa H., and Ohkawa Y. Phytoremediation of herbicide atrazine and metolachlor by transgenic rice plants expressing human CYP1A1, CYP2B6 and CYP2C19. J Agric Food Chem 54 (2006) 2985-2991
48. Kawahigashi H., Hirose S., Ohkawa H., and Ohkawa Y. Broad range of herbicide tolerance of glutinous upland rice variety 'Yumenohatamochi' carrying human cytochrome P450 genes. Plant Biotechnol 23 (2006) 227-231
49. Kawagashi H., Hirose S., Ohkawa H., and Ohkawa Y. Herbicide resistance of transgenic rice plants expressing human CYP1A1. Biotechnol Adv 25 (2007) 75-85
50. Knuteson S.L., Whitwell T., and Klaine S.J. Influence of plant age and size on simazine toxicity and uptake. J Environ Qual 31 (2002) 2096-2103
51. Komives T., and Gullner G. Phase I xenobiotic metabolic systems in plants. Z Naturforsch [C] 60 (2005) 179-185
52. Kucerova P., Mackova M., Polachova L., Burkhard J., Demnerova K., and Macek T. Correlation of PCB transformation by plant tissue cultures with their morphology and peroxidase activity changes. Collect Czechoslov Chem Commun 64 (1999) 1497-1509
53. Kucerova P., Mackova M., Chroma L., Burkhard J., Triska J., Demnerova K., et al. Metabolism of polychlorinated biphenyls by Solanum nigrum hairy root clone SNC-90 and analysis of transformation products. Plant Soil 225 (2000) 109-115
54. Kucerova P., In der Wiesche C., Wolter M., Macek T., Zadrazil F., and Mackova M. The ability of different plant species to remove polycyclic aromatic hydrocarbons and polychlorinated biphenyls from incubation media. Biotechnol Lett 23 (2001) 1355-1359
55. Kurumata M., Takahashi M., Sakamotoa A., Ramos J.L., Nepovim A., Vanek T., et al. Tolerance to and uptake and degradation of 2,4,6-trinitrotoluene (TNT) are enhanced by the expression of a bacterial nitroreductase gene in Arabidopsis thaliana. Z Naturforsch [C] 60 (2005) 272-278
56. Lee I., and Fletcher J.S. Involvement of mixed function oxidase systems in PCB metabolism by plant cells. Plant Cell Rep 11 (1992) 97-100
57. Li H., Sheng G., Sheng W., and Xu O. Uptake of trifluralin and lindane from water by ryegrass. Chemosphere 48 (2002) 335-341
58. Limura Y., Ikeda S., Sonoki T., Hayakawa T., Kajita S., Kimbara K., et al. Expression of a gene for Mn-peroxidase from Coriolus versicolor in transgenic tobacco generates potential tools for phytoremediation. Appl Microbiol Biotechnol 59 (2002) 246-251
59. Ma X., and Burken J.G. TCE diffusion to the atmosphere in phytoremediation applications. Environ Sci Technol 37 (2003) 2534-2539
60. Ma X., Richter A.R., Albers S., and Burken J.G. Phytoremediation of MTBE with hybrid poplar trees. Int J Phytoremediation 6 2 (2004) 157-167
61. Macek T., Mackova M., and Kas J. Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18 (2000) 23-34
62. Mackova M., Macek T., Ocenaskova J., Burkhard J., Demnerova K., and Pazlarova J. Biodegradation of polychlorinated biphenyls by plant cells. Int Biodeterior Biodegrad 39 (1997) 317-325
63. Mackova M., Macek T., Kucerova P., Burkhard J., Pazlarova J., and Demnerova K. Degradation of polychlorinated biphenyls by hairy root cultures of Solanum nigrum. Biotechnol Lett 19 (1997) 787-790
64. Mackova M., Macek T., Kucerova P., Polachova I., Burkhard J., and Triska I. The beneficial effects of plant on detoxification of environmental pollutants. Biologia (1999) 76-77
65. Martinois E., Grill E., Tommaslnl R., Kreuz K., and Amrheln N. ATP dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364 (1993) 247-249
66. Mayer A.M., and Staples R.C. Laccase: new functions for an old enzyme. Phytochem 60 (2002) 551-565
67. Meagher R.B. Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3 (2000) 153-162
68. Mezzari M.P., Walters K., Jelinkova M., Shih M.-C., Just C.L., and Schnoor J.L. Gene expression and microscopic analysis of Arabidopsis exposed to chloroacetanilide herbicides and explosive compounds. A phytoremediation approach. Plant Physiol 138 (2005) 858-869
69. Mohammadi M., Chalavi V., Novakova-Sura M., Laliberte J.F., and Sylvestre M. Expression of bacterial biphenyl-chlorophenyl dioxygenase genes in tobacco plants. Biotechnol Bioeng 97 3 (2007) 496-505
70. Morant M., Bak S., Moller B.L., and Werck-Reichhart D. Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol 14 (2003) 151-162
71. Newman L.A., and Arnold C.W. Phytoremediation of MTBE-a review of the state of the technology. In: Moyer E.E., and Kostecki P.T. (Eds). MTBE remediation handbook (2003), Massachusetts Amherst Scientific Publishers, Amherst 279-288
72. Newman L.A., and Reynolds C.M. Phytodegradation of organic compounds. Curr Opin Biotechnol 15 (2004) 225-230
73. Newman L.A., Strand S.E., Choe N., Duffy J., Ekuan G., Ruszaj M., et al. Uptake and biotransformation of trichloroethylene by hybrid poplars. Environ Sci Technol 31 (1997) 1062-1067
74. O'Keefe D.P., Tepperman J.M., Dean C., Leto K.J., Erbes D.L., and Odell J.T. Plant expression of a bacterial cytochrome P450 that catalyzes activation of a sulfonylurea pro-herbicide. Plant Physiol 105 (1994) 473-824
75. Oller A.L.W., Agostini E., Talano M.A., Capozucca C., Milrad S.R., Tigier A., et al. Overexpression of a basic peroxidase in transgenic tomato (Lycopersicon esculentum Mill cv Pera) hairy roots increases phytoremediation of phenol. Plant Sci 169 (2005) 1102-1111
76. Peterson F.J., Mason R.P., Hovsepian J., and Holtzman J.L. Oxygen-sensitive and insensitive nitroreduction by Escherichia coli and rat hepatic microsomes. J Biol Chem 254 (1979) 4009-4014
77. Pflugmacher S., Schroder P., and Sandermann H. Taxonomic distribution of plant glutathione S-transferase acting on xenobiotics. Phytochemistry 54 (2000) 267-273
78. Plewa M.J., and Wagner E.D. Activation of promutagens by green plants. Annu Rev Gen 27 (1993) 93-113
79. Pradhan S.P., Conrad J.R., Paterek J.R., and Srivastava V.J. Potential of phytoremediation for treatment of PAHs in soil at MGP sites. J Soil Contam 7 (1998) 467-480
80. Rosser S.J., French C.E., and Bruce N.C. Special symposium: phytoremediation: engineering plants for the phytodetoxification of explosives. In vitro cell. Dev Biol-Plant 37 (2001) 330-333
81. Rylott E.L., Jackson R.G., Edwards J., Womack G.L., Seth-Smith H.M.B., Rathbone D.A., et al. An explosive-degrading cytochrome P450 activity and its targeted application for phytoremediation of RDX. Nat Biotechnol 24 (2006) 216-219
82. Salt D.E., Smith R.D., and Raskin I. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol Biol 49 (1998) 643-668
83. Sandermann H. Plant metabolism of xenobiotics. Trends Biochem Sci 17 (1992) 82-84
84. Sandermann H. Higher plant metabolism of xenobiotics: the green liver concept. Pharmacogenetics 4 (1994) 225-241
85. Schaffner A., Messener B., Langebartels C., and Sandermann H. Genes and enzymes for in-planta phytoremediation of air, water and soil. Acta Biotechnol 22 (2002) 141-151
86. Schnoor J.L., Licht L.A., McCutcheon S.C., Wolfe N.L., and Carreira L.H. Phytoremediation of organic and nutrient contaminants. Environ Sci Technol 28 (1995) 318-323
87. Schroder P., and Collins C. Conjugating enzymes involved in xenobiotic metabolism of organic xenobiotics in plants. Int J Phytoremediation 4 (2002) 247-265
88. 14C-TNT in different biochemical compartments of the monocotyledonous Triticum aestivum. Environ Pollut 104 1 (1999) 113-119
89. 14C) trichloroethylene by poplar suspension cells. Chemosphere 47 (2003) 957-962
90. Siminszky B., Corbin F.T., Ward E.R., Fleischmann T.J., and Dewey R.E. Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenylurea herbicides. Proc Natl Acad Sci U S A 96 4 (1999) 1750-1755
91. 2. J Biotechnol 123 1 (2006) 43-49
92. Sonoki T., Kajita S., Ikeda S., Uesugi M., Tatsumi K., Katayama Y., et al. Transgenic tobacco expressing fungal laccase promotes the detoxification of environmental pollutants. Appl Microbiol Biotechnol 67 (2005) 138-142
93. Stiborova M., and Anzenbacher P. What are the principal enzymes oxidising xenobiotics in plants: cytochrome P-450 or peroxidase? (A hypothesis). Gen Physiol Biophys 10 2 (1991) 209-216
94. Sundberg S.E., Ellington J.J., Evans J.J., Keys D.A., and Fisher J.W. Accumulation of perchlorate in tobacco plants: development of a plant kinetic model. J Environ Monit 5 3 (2003) 505-512
95. Sung K., Munster C.L., Rhykerd R., Drew M.C., and Corapcioglu M.Y. The use of vegetation to remediate soil freshly contaminated by recalcitrant contaminants. Water Res 37 (2003) 2408-2418
96. Suresh B., Sherkhane P.D., Kale S., Eapen S., and Ravishankar G.A. Uptake and degradation of DDT by hairy root cultures of Cichorium intybus and Brassica juncea. Chemosphere 61 9 (2005) 1288-1292
97. Uchida E., Ouchi T., Suzuki Y., Yoshida T., Habe H., Yamaguchi I., et al. Secretion of bacterial xenobiotic degrading enzymes from transgenic plants by an apoplastic expressional system: an applicability for phytoremediation. Environ Sci Technol 39 (2005) 7671-7677
98. Van Aken B., Yoon J.M., and Schnoor J.L. Biodegradation of nitro-substituted explosives 2,4,6-trinitrotoluene, hexahydro-1,3,5-trinitro-1,3,5-triazine and octahydro-1,3,5,7-tetranitro-1,3,5-tetrazocine by photosymbiotic Methylbacterium sp. associated with poplar tissues (Populus deltoids × nigra DN-34). Appl Environ Microbiol 70 (2004) 508-517
99. Wand H., Kuschk P., Soltmann U., and Stottmeister U. Enhanced removal of xenobiotics by helophytes. Acta Biotechnol 22 (2002) 175-181
100. Wang C., Lyon D.Y., Hughes J.B., and Bennet G.N. Role of hydroxylamine intermediates in the phytotransformation of 2,4,6-trinitrotoluene by Myriophyllum aquaticum. Environ Sci Technol 37 (2003) 3595-3600
101. Wang G.D., Li Q.J., Luo B., and Chen X.Y. Ex-planta phytoremediation of trichlorophenol and phenol allelochemicals via an engineered secretory laccase. Nat Biotechnol 22 (2004) 893-897
102. Wang L., Samac D.A., Shapir A., Wackett L.P., Vance C.P., Olszewski N.E., et al. Biodegradation of atrazine in transgenic plants expressing a modified bacterial atrazine chlorohydrolase (atzA) gene. Plant Biotech J 3 (2005) 475-486
103. Yoon J.M., Oh B.T., Just C.L., and Schnoor J.L. Uptake and leaching of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by hybrid poplar trees. Environ Sci Tech 36 (2002) 4649-4655
104. Yoon J.M., Oliver D.J., and Shanks J.V. Phytoremediation of 2,4-dinitrotoluene in Arabidopsis thaliana: toxicity, fate and gene expression studies in vitro. Biotechnol Prog 22 (2006) 1524-1531