Biodegradation of atrazine in transgenic plants expressing a modified bacterial atrazine chlorohydrolase (atzA) gene

Plant Biotechnology Journal

Volumn 3, Issue 5, 2005, Pages 475-486

  Wang, Lin ^a   Samac, Deborah A ^a   Shapir, Nir ^a   Wackett, Lawrence P ^a   Vance, Carroll P ^a   Olszewski, Neil E ^a   Sadowsky, Michael J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Atrazine; Atrazine chlorohydrolase; AtzA; Phytoremediation; Transgenic plants

Indexed keywords

AGROBACTERIUM; ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); CASSAVA VEIN MOSAIC VIRUS; MANIHOT ESCULENTA; MEDICAGO SATIVA; NEGIBACTERIA; NICOTIANA TABACUM; RHIZOBIUM;

EID: 33746728686     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2005.00138.x     Document Type: Article

References (63)

1. Anderson, P.C. and Georgeson, M. (1989) Herbicide tolerant mutants of corn. Genome, 34, 994-999.
2. Aragao, F.J.L., Sarokin, L., Vianna, G.R. and Rech, E.L. (2000) Selection of transgenic meristematic cells utilizing a herbicidal molecule results in the recovery of fertile transgenic soybean [Glycine max (L.) Merril] plants at a high frequency. Theor. Appl. Genet. 101, 1-6.
3. Arntzen, C.J., Pfister, K. and Steinback, K.E. (1982) The mechanism of chloroplast triazine resistance: alterations in the site of herbicide action. In Herbicide Resistance in Plants (LeBaron, H.M. and Gressel, J., eds), p. 185. New York: Wiley-Intersciences.
4. Austin, S., Bingham, E.T., Mathews, D.E., Shahan, M.N., Will, J. and Burgess, R.R. (1995) Production and field performance of transgenic alfalfa (Medicago sativa) expressing alpha-amylase and manganese-dependent lignin peroxidase. Euphytica, 85, 381-395.
5. Belluck, D.A., Benjamin, S.L. and Dawson, T. (1991) Groundwater contamination by atrazine and its metabolites: risk assessment, policy, and legal implications. In Pesticide Transformation Products: Fate and Significance in the Environment. (Somasundaram, L. and Coats, J.R., eds), pp. 254-273. Washington, DC: American Chemical Society.
6. Bingham, E.T. (1991) Registration of alfalfa hybrid Regen SY germplasm for tissue culture and transformation research. Crop Sci. 31, 1098.
7. Birch, R.G. (1997) Plant transformation: problems and strategies for practical application. Annu. Rev. Plant Physiol. Mol. Biol. 48, 297-326.
8. Bizily, S., Rugh, C.L., Summers, A.O. and Meagher, R. (1999) Phytoremediation of methyl mercury pollution: merB expression on Arabidopsis thaliana confers resistance to organomecurials. Proc. Natl. Acad. Sci. USA, 96, 6808-6813.
9. Bode, M., Stöbe, P., Thiede, B., Schuphan, I. and Schmidt, B. (2003) Biotransformation of atrazine in transgenic tobacco cell culture expressing human P450. Pest Manag. Sci. 60, 49-58.
10. Burken, J. and Schnoor, J. (1997) Uptake and metabolism of atrazine by poplar trees. Environ. Sci. Technol. 31, 1399-1406.
11. Cheung, A.Y., Bogorad, L., Van Montagu, M. and Schell, J. (1988) Relocating a gene for herbicide tolerance: a chloroplast gene is converted into a nuclear gene. Proc. Natl. Acad. Sci. USA, 85, 391-395.
12. Clay, S.A. and Koskinen, W.C. (1990) Characterization of alachlor and atrazine desorption from soils. Weed Sci. 38, 74-80.
13. Comai, L., Facciotti, D., Hiatt, W., Thompson, G., Rose, R. and Stalker, D. (1985) Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature, 317, 741-744.
14. Dietz, A.C. and Schnoor, J.L. (2001) Advances in phytoremediation. Environ. Health Perspect, 109 (Suppl. 1), 163-168.
15. Doty, S.L., Shang, T.Q., Wilson, A.M., Tangen, J., Westergreen, A.D., Newman, L.A., Strand, S.E. and Gordon, M.P. (2000) Enhanced metabolism of halogenated hydrocarbons in transgenic plants containing mammalian cytochrome P450 2E1. Proc. Natl. Acad. Sci. USA, 97, 6287-6291.
16. Erickson, E.L. and Lee, K.H. (1989) Degradation of atrazine and related s-triazines. Crit. Rev. Environ. Contam. 19, 1-3.
17. Erikson, O., Hertzberg, M. and Näsholm, T. (2004) A conditional marker gene allowing both positive and negative selection in plants. Nat. Biotechnol. 22, 455-458.
18. French, C.E., Rosser, S.J., Davies, G.J., Nicklin, S. and Bruce, N.C. (1999) Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat. Biotechnol. 17, 491- 494.
19. Freyssinet, G., Pelissier, B., Freyssinet, M. and Delon, R. (1996) Crops resistant to oxynils: from the laboratory to the market. Field Crops Res. 45, 125-133.
20. Goswami, K. and Green, R.E. (1971) Microbial degradation of the herbicide atrazine and its 2-hydroxy analog in submerged soils. Environ. Sci. Technol. 5, 426-429.
21. Gullner, G., Kömives, T. and Rennenberg, H. (2001) Enhanced tolerance of transgenic poplar plants overexpressing γ-glutamylcysteine synthetase towards chloroacetanilide herbicides. J. Exp. Bot. 52, 971-979.
22. Gysin, H. and Knuesli, E. (1960) Chemistry and herbicidal properties of triazine derivatives. In Advances in Pest Control Research, Vol. III (Metcalf, R., ed.), pp. 289-358. New York: Wiley (Interscience).
23. Hannink, N., Rosser, S.J., French, C.E., Basran, A., Murray, J.A.H., Nicklin, S. and Bruce, N.C. (2001) Phytodetoxification of TNT by transgenic plants expressing a bacterial nitroreductase. Nat. Biotechnol. 19, 1168-1172.
24. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J. and Schilperoort, R.A. (1983) A binary plant vector strategy based on separation of the Vir- and T-region of the Agrobacterium tumefaciens Ti plasmid. Nature, 303, 179-180.
25. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. (1986) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
26. Inui, H., Shiota, N., Motoi, Y., Ido, Y., Inoue, T., Kodama, T., Ohkawa, Y. and Ohkawa, H. (2001) Metabolism of herbicides and other chemicals in human cytochrome P450 species and in transgenic potato plants co-expressing human CYP1A1, CYP2B6 and CYP2C19. J. Pestic. Sci. 26, 28-40.
27. Inui, H., Ueyama, Y., Shiota, N., Ohkawa, Y. and Ohkawa, H. (1999) Herbicide metabolism and cross-tolerance in transgenic potato plants expressing Human CYP1A1. Pestic. Biochem. Physiol. 64, 33-46.
28. Koncz, C. and Schell, J. (1986) The promoter of T-L DNA Gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
29. Kozak, M. (1991) Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266, 19 867-19 870.
30. Lermontova, I. and Grimm, B. (2000) Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenylether herbicide acifluorfen. Plant Physiol. 122, 75-83.
31. Lichtenstein, C. and Draper, J. (1986) Genetic engineering of plants. In DNA Cloning, A Practical Approach, Vol. 2 (Glover, D.M., ed.), pp. 67-119. Washington, DC: IRL Press.
32. Lutz, K.A., Knapp, J.E. and Maliga, P. (2001) Expression of bar in the plastid genome confers herbicide resistance. Plant Physiol. 125, 1585-1590.
33. Mandelbaum, R.T., Allan, D.L. and Wackett, L.P. (1995) Isolation and characterization of a Pseudomonas sp. that mineralizes the s-triazine herbicide atrazine. Appl. Environ. Microbiol. 61, 1451-1457.
34. Martinez, B., Tomkins, J., Wackett, L.P., Wing, R. and Sadowsky, M.J. (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J. Bacteriol. 183, 5684-5697.
35. Miki, B. and McHugh, S. (2004) Selectable marker genes in transgenic plants: applications, alternatives, and biosafety. J. Biotechnol. 107, 193-232.
36. Miller, S.S., Driscoll, B.T., Gregerson, R.G., Gantt, J.S. and Vance, C.P. (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J. 15, 173-184.
37. Mullineaux, P.M. (1992) Genetically engineered plants for herbicide resistance. In Plant Genetic Manipulation for Crop Protection (Gatehouse, A., Hilder, V. and Boulter, D., eds), pp. 75-107. Wallingford: CAB International.
38. Naested, H., Fennema, M., Hao, L., Andersen, M., Janssen, D.B. and Mundy, J. (1999) A bacterial haloalkane dehalogenase gene as a negative selectable marker in Arabidopsis. Plant J. 18, 571-576.
39. Olszewski, N.E., Martin, F.B. and Ausubel, F.M. (1988) Specialized binary vector for plant transformation: expression of the Arabidopsis thaliana AHAS gene in Nicotiana tabacum. Nucleic Acids Res. 16, 10 765-10 781.
40. Ruiz, O.N., Hussein, H.S., Terry, N. and Daniell, H. (2003) Phytoremediation of organomecurial compounds via chloroplast genetic engineering. Plant Physiol. 132, 1344-1352.
41. Sadowsky, M.J. and Wackett, L.P. (2001) Genetics of atrazine and s-triazine degradation by Pseudomonas sp. strain ADP and other bacteria. In Pesticide Biotransformations in Plants and Microorganisms (Hall, J.C., Hoagland, R.E. and Zablotowic, R.M., eds), pp. 268-282. ACS Symp. Ser. 777. Washington, DC: Oxford University Press.
42. Samac, D.A., Tesfaye, M., Dornbusch, M., Purev, S. and Temple, S.J. (2004) A comparison of constitutive promoters for expression of transgenes in alfalfa (Medicago sativa). Transgenic Res. 13, 349-361.
43. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Schluter, K., Futterer, J. and Potrykus, I. (1995) 'Horizontal' gene transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs - if at all - at an extremely low frequency. Biotechnology, 13, 1094-1098.
45. Seffernick, J.L., Johnson, G., Sadowsky, M.J. and Wackett, L.P. (2000) Substrate specificity of atrazine chlorohydrolase and atrazine-catabolizing bacteria. Appl. Environ. Microbiol. 66, 4247-4252.
46. Seffernick, J.L., McTavish, H., Osborne, J.P., de Souza, M.L., Sadowsky, M.J. and Wackett, L.P. (2002) Atrazine chlorohydrolase from Pseudomonas sp strain ADP is a metalloenzyme. Biochemistry, 41, 14 430-14 437.
47. Shimizu, M., Kimura, T., Koyama, T., Suzuki, K., Ogawa, N., Miyashita, K., Sakka, K. and Ohmiya, K. (2002) Molecular breeding of transgenic rice plants expressing a bacterial chlorocatechol dioxygenase gene. Appl. Environ. Microbiol. 68, 4061-4066.
48. Siminszky, B., Corbin, F.T., Ward, E.R., Fleischmann, T.J. and Dewey, R.E. (1999) Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenyl urea herbicides. Proc. Natl. Acad. Sci. USA, 96, 1750-1755.
49. Singh, O.V., Labana, S., Pandey, G., Budhiraja, R. and Jain, R.K. (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl. Microbiol. Biotechnol. 61, 405-412.
50. de Souza, M.L., Newcombe, D., Alvey, S., Crowley, D.E., Hay, A., Sadowsky, M.J. and Wackett, L.P. (1998b) Molecular basis of a bacterial consortium: interspecies catabolism of atrazine. Appl. Environ. Microbiol. 64, 178-184.
51. de Souza, M.L., Sadowsky, M.J., Seffernick, J., Martinez, B. and Wackett, L.P. (1998a) The atzABC genes encoding atrazine catabolism are widespread and highly conserved. J. Bacteriol. 180, 1951-1954.
52. de Souza, M.L., Sadowsky, M.J. and Wackett, L.P. (1996) Atrazine chlorohydrolase from Pseudomonas sp. ADP: gene sequence, enzyme purification and protein characterization. J. Bacteriol. 178, 4894-4900.
53. de Souza, M.L., Wackett, L.P., Boundy-Mills, K.L., Mandelbaum, R.T. and Sadowsky, M.J. (1995) Cloning, characterization, and expression of a gene region from Pseudomonas sp. strain ADP involved in the dechlorination of atrazine. Appl. Environ. Microbiol. 61, 3373-3378.
54. Stalker, D.M., McBride, K.E. and Malyj, L.D. (1988) Herbicide resistance in transgenic plants expressing a bacterial detoxification gene. Science, 242, 419-423.
55. Streber, W.R. and Willmitzer, L. (1989) Transgenic tobacco plants expressing a bacterial detoxifying enzyme are resistant to 2,4-D. Bio/Technology, 7, 811-816.
56. Strong, L.C., McTavish, H., Sadowsky, M.J. and Wackett, L.P. (2000) Field-scale remediation of atrazine-contaminated soil using recombinant Escherichia coli expressing atrazine chlorohydrolase. Environ. Microbiol. 2, 91-98.
57. Verdaguer, B., de Kochko, A., Beachy, R.N. and Fauquet, C. (1996) Isolation and expression in transgenic tobacco and rice plants of the cassava vein mosaic virus (CVMV) promoter. Plant Mol. Biol. 31, 1129-1139.
58. Wackett, L.P., Sadowsky, M.J., Martinez, B. and Shapir, N. (2002) Biodegradation of atrazine and related triazine compounds: from enzymes to field studies. Appl. Microbiol. Biotechnol. 58, 39-45.
59. Weeks, J.T., Koshiyama, K.Y., Maier-Greiner, U., Schäeffner, T. and Anderson, O.D. (2000) Wheat transformation using cyanamide as a new selective agent. Crop Sci. 40, 1749-1754.
60. Wych, R.D. and Rain, D.W. (1978) Simultaneous measurement of nitrogen fixation estimated by acetylene-ethylene assay and nitrate absorption by soybean. Plant Physiol. 62, 443-448.
61. Yamada, T., Ishige, T., Shiota, N., Inui, H., Ohkawa, H. and Ohkawa, Y. (2002) Enhancement of metabolizing herbicides in young tubers of transgenic potato plants with the rat CYP1A1 gene. Theor. Appl. Genet. 105, 515-520.
62. Ye, G.N., Stone, D., Pang, S.Z., Creely, W., Gonzalez, K. and Hinchee, M. (1999) Arabidopsis ovule is the target for Agrobacterium in planta vacuum infiltration transformation. Plant J. 19, 249-257.
63. Zhou, H., Arrowsmith, J.W., Fromm, M.E., Hironaka, C.M., Taylor, M.L., Rodriguez, D., Pajeau, M.E., Brown, S.M., Santino, C.G. and Fry, C.G. (1995) Glyphosate-tolerant CP4 and GOX genes as a selectable marker in wheat transformation. Plant Cell Rep. 15, 159-163.