Exploiting plant metabolism for the phytoremediation of persistent herbicides

  • Julian O. D. Coleman
  • Carla Frova
  • Peter Schröder
  • Michel Tissut
Phytoremediation: Persistent Herbicides


Weed control by herbicides has helped us to create the green revolution and to provide food for at least the majority of human beings living today. However, some herbicides remain in the environment and pose an ecological problem. The present review describes the properties and fate of four representative herbicides known to be presistent in ecosystems. Metabolic networks are depiced and it is concluded that removal of these comopounds by the ecologically friendly technique of phytoremediation is possible. The largest problem is seen in the uptake of the compounds into suitable plants and the time needed for such an approach.


Atrazine chloroacetanilides, isoproturon metolachlor persistent herbicides phytoremediation plant metabolism 


  1. Anderson TA, Coats JR (1995): Screening rhizosphere soil samples for the ability to mineralize elevated concentrations of atrazine and metolachlor. Journal of Science and Health B30, 473–484Google Scholar
  2. Anon A (1979): Herbicide residue levels and redrilling of failed cereals. MAFF ADAS South East Region Agricultural Science Service. Annual Report, HMSO, LondonGoogle Scholar
  3. Behrendt H, Brüggemann R (1993): Modelling the fate of organic chemicals in the soil plant environment: Model study of root uptake of pesticides. Chemosphere 12, 2325–2332CrossRefGoogle Scholar
  4. Bester K, Hühnerfuss H, Brockmann U, Rick HJ (1995): Biological effects of triazine herbicide contamination on marine phytoplankton, Arch Environ Contam Toxicol 23, 277–283CrossRefGoogle Scholar
  5. Bintein S, Devillers J (1996): Evaluating the environmental fate of lindane in France. Chemosphere 32, 2427–2440CrossRefGoogle Scholar
  6. Blair AM, Martin TD, Brain P, Cotterill EG (1991): The interaction between planting depth of four winter wheat cultivars,Alopecurus myosuroides Huds. andBromus sterilis L. and their susceptibility to post-emergent applications of isoproturon and chlortoluron. Weed Res 31, 285–293Google Scholar
  7. Blair AM, Martin TD, Walker A, Welch SJ (1990): Measurement and prediction of isoproturon movement and persistence in three soils. Crop Protection 9, 289–294CrossRefGoogle Scholar
  8. Buffaut P (1992): Produits phytosanitaires: teneures actuelles des eaux en France. Colloque Phyt’eau — Produits Phytosanitaires — Usages Agricoles et Connexe 21, 5–19Google Scholar
  9. Castelfranco P, Foy CL, Deutsch DB (1961): Nonenzymatic detoxication of 2-chloro-4,6-bis (etymalmino)-s-triazine (simazíne) by extracts ofZea mays. Weed 9, 580CrossRefGoogle Scholar
  10. Cole DJ, Cummings I, Hatton PJ, Dixon D, Edwards R (1997): Glutathione transferases in crops and major weeds. In: Hatzios KK (Ed): Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI series Vol 37, Kluwer Academic Publishers, Dordrecht, pp 139–154Google Scholar
  11. Cottingham CK, Hatzios KK (1992): Basis of differential tolerance of two corn hybrids (Zea mays) to metolachlor. Weed Sci 40, 359–363Google Scholar
  12. Cottingham CK, Hatzios KK, Meredith SA (1993): Comparative responses of selected corn (Zea mays) hybrids to EPTC and metolachlor. Weed Res 33, 161–170CrossRefGoogle Scholar
  13. Coupland D (1991): Detoxification of herbicides in plants. In: Caseley JC, Cussan GW, Atkin RK (Eds): Herbicide resistance in weeds and crops, Wiley, New York, pp 263–278Google Scholar
  14. Dixon DP, Cole DJ, Edwards R (1998): Purification, regulation and cloning of a glutathione transferase (GST) from Maize resembling the auxin-inducible type-Ill GSTs. Plant Molecular Biology 36, 75–87CrossRefGoogle Scholar
  15. Edwards R, Dixon DP, Walbot V (2000): Plant glutathione S-transferases: Enzymes with multiple functions in sickness and in health. Trends in Plant Science 5, 193–198CrossRefGoogle Scholar
  16. European Commission’s Directive on Drinking Water 80-778-EEC (1980): European Commission, BrusselsGoogle Scholar
  17. Farago S, Kreuz K, Brunold C (1993): Decreased glutathione levels enhance the susceptibility of maize seedlings to metolachlor. Pestic Biochem Physiol 47, 199–205CrossRefGoogle Scholar
  18. Fedke C (1982): Biochemistry and physiology of herbicide action, Springer Verlag, Berlin Heidelberg New York, 148–158Google Scholar
  19. Frear DS, Swanson HR, Tanaka FS (1972): Herbicide metabolism in plants. In: Runeckles VC, Tso TC (Eds): Structural and functional aspects of phytochemistry. Recent advances in phytochemistry, Acad Press, New York, 225–247Google Scholar
  20. Fuerst EP (1987): Understanding the mode of action of the chloroacetanilide and thiocarbammate herbicides. Weed Technol 1, 270–277Google Scholar
  21. Fuertet-Mazel A, Grollier T, Grouselle M, Ribeyre F, and Boudou A (2000): Experimental study of bioaccumulation and effects of the herbicide isoproturon on freshwater rooted macrophytes (Elodea densa andLudwigia natans). Chemosphere 32, 1499–1512CrossRefGoogle Scholar
  22. Gaillard C, Dufaud A, Tommasini R, Kreuz K, Amrhein N, Martinoia E (1994): A herbicide antidote (safener) induces the activity of both the herbicide detoxifying enzyme and of a vacuolar transporter for the detoxified herbicide. FEBS Letters 352 [FEBS 14574], 219–221CrossRefGoogle Scholar
  23. Gläßgen WE, Komoßa D, Bohnenkämper O, Haas M, Hertkorn N, May RG, Szymczak W, Sandermann H (1999): Metabolism of the herbicide Isoproturon in wheat and soybean cell suspension cultures. Pestic Biochem Physiol 63, 97–113CrossRefGoogle Scholar
  24. Good NE (1963) Carbon dioxide and the Hill reaction. Plant Physiol 38, 298–304Google Scholar
  25. Goolsby DA, Thurman EM, Pomes ML, Meyer MT, Battaglin WA (1997): Herbicides and their metabolites in rainfall-Origin, transport, and deposition patterns across the Midwestern and Northeastern United States, 1990–1991: Environmental Science & Technology 31, 1325–1333CrossRefGoogle Scholar
  26. Glotfelty DE (1978) The atmosphere as a sink for applied pesticides. J Air Pollut Control Assoc 28, 917–921Google Scholar
  27. Glotfelty DE, Williams GH, Freeman HP, Leech MM (1990) Regional atmospheric transport and deposition of pesticides in Maryland. In: Kurtz D (Ed): Long Range Transport of Pesticides, Lewis Publishing Co, Chelsea, pp 199–222Google Scholar
  28. Gronwald JW (1989): Influence of herbicide safeners on herbicide metabolism. In: Hatzios KK, Hoagland RE (Eds): Crop safeners for herbicides: development, uses and mechanisms of action, Academic Press, San Diego, pp 163–175Google Scholar
  29. Gross D, Laanio T, Dupuis G, Esser HO (1979): The metabolic behaviour of chlortoluron in wheat and soil. Pestic Biochem Physiol 10, 49CrossRefGoogle Scholar
  30. Gunderson EL (1995): FDA Total Diet Study, July 1986–April 1991, Dietary Intakes of Pesticides, Selected Elements, and Other Chemicals, Journal of AOAC Intl 78, 6Google Scholar
  31. Haas M (1997): Metabolisierung von Xenobiotika durch pflanzliche Zellkulturen und Enzyme. Dissertation TU-München. Shaker Verlag, Aachen, GermanyGoogle Scholar
  32. Han S, Hatzios KK (1991): Effects of the herbicide pretilachlor and the safener fenclorium on glutathione content and glutathionedependent enzyme activity of rice. Zeitschrift für Naturforschung 46c, 861–865Google Scholar
  33. Hatzios KK (1997): Regulation of xenobiotics degrading enzymes with herbicide safeners. In: Hatzios KK (Ed): Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI series Vol 37, Kluwer Academic Publishers, Dordrecht, pp 275–288Google Scholar
  34. Inui H, Kodama T, Ohkawa Y, Ohkawa H (2000): Herbicide metabolism and cross-tolerance in transgenic potato plants co-expressing human CYP1A1, CYP2B6, and CYP2C19. Pestic Biochem Physiol 66, 116–129CrossRefGoogle Scholar
  35. Izryk GP, Fuerst EP (1997): Characterization and induction of maize glutathione S-transferases involved in herbicide detoxification. In: Hatzios KK (Ed): Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI Series Vol 37, Kluwer Academic Publishers, Dordrecht, pp 155–170Google Scholar
  36. Jepson I, Lay VJ, Holt DC, Bright SWJ, Greenland AJ (1994): Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione S-transferase isoforms I, II and IV. Plant Molecular Biology 26, 1855–1866CrossRefGoogle Scholar
  37. Jepson I, Holt DC, Roussel V, Wright SY, Greenland AJ (1997): Transgenic plant analysis as a tool for the study of glutathione Stransferases. In: Hatzios K.K. (Ed): Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI Series Vol 37, Kluwer Academic Publishers, Dordrecht, pp 313–323Google Scholar
  38. Kreuz K, Gaudin J, Ebert E (1989): effects of the safeners CGA 154281, oxabetrinil and fenclorim on uptake and degradation of metolachlor in corn (Zea mays L.) seedlings. Weed Research 29, 399–405CrossRefGoogle Scholar
  39. Kulshresta G (1982): Hydrolysis of isoproturon in aqueous medium and its persistence in soil and plants. Ind J Weed Sci 14, 96–102Google Scholar
  40. Lamoureux GL and Rusness DG (1989a): The role of glutathione and glutathione S-transferases in pesticide metabolism, selectivity and mode of action in plants and insects. In: Dolphin D, Poulson R, Avramovic O (Eds): Glutathione: Chemical biochemical and medical aspects, Vol IIIB, Ser: Enzyme and Cofactors, J. Wiley & Sons, New York, pp 153–196Google Scholar
  41. Lamoureux GL and Rusness DG (1989b): Propachlor metabolism in soybean plants, excised soybean tissues, and soil. Pestic Biochem Physiol 34, 187–204CrossRefGoogle Scholar
  42. Lamoureux GL, Rusness DG, Schröder P, Rennenberg H (1991): Diphenyl ether herbicide metabolism in a spruce cell suspension culture: The identification of two novel metabolites derived from a glutathione conjugate. Pestic Biochem Physiol 39, 291–301CrossRefGoogle Scholar
  43. Lamoureux GL, Simoneaux B, Larson J (1998): The metabolism of atrazine and related 2-chloro-4,6-bis(alkylamino)-s-triazines in plants. In: Ballantine LG, McFarland JE, Hacket DS (Eds): Triazine Herbicides: Risk Assessment, Washington, D.C., American Chemical SocietyGoogle Scholar
  44. Le Baron MH, McFarland JE, Simoneaux BJ (1988): Metolachlor. In: Kearney PC, Kaufmann DD (Eds): Herbicides: Chemistry, Degradation and Mode of Action, Vol 3, Marcel Dekker, New York, pp 336–383Google Scholar
  45. Mandelbaum RT, Allan DL, Wackett LP (1995): Isolation and characterization of aPseudomonas sp. that mineralizes the s-triazine herbicide atrazine. Appl Environ Microbiol 61, 1451–1457Google Scholar
  46. Marrs KA (1996): The functions and regulation of glutathione Stransferases in plants. Annu Rev Plant Physiol 47, 127–158CrossRefGoogle Scholar
  47. Martinoia E, Grill E, Tommasini R, Kreuz K, Amrhein N (1993): ATP-dependent glutathione S-conjugate ‘export’ pump in the vacuolar membrane of plants. Nature 364, 247–249CrossRefGoogle Scholar
  48. Masaphy S, Henis Y, Levanon D (1996): Manganese-enhanced biotransformation of atrazine by the white rot fungusPleurotus pulmonarius and its correlation with oxidation activity. Appl Environ Microbiol 62, 3587–3593Google Scholar
  49. Matthes B, Schmalfuss J, Boger P (1998): Chloroacetamide mode of action, II: Inhibition of very long chain fatty acid synthesis in higher plants. Z Naturforsch 53c, 1004–1011Google Scholar
  50. Mauch F, Dudler R (1993): Differential induction of distinct glutathione-s-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol 102, 1193–1201CrossRefGoogle Scholar
  51. Mazur BJ, Falco SC (1989): The development of herbicide resistant crops. Annu Rev Plant Physiol Plant Mol Biol 40, 441–470CrossRefGoogle Scholar
  52. McGonigle B, Keeler S, Lau S-MC, Koeppe M, O’Keefe DP (2000): A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiology 124, 1105–1120CrossRefGoogle Scholar
  53. Mirgain I, Schenck C, Monteil H (1993): Atrazine Contamination of Groundwaters in Eastern France in Relation to the Hydrogeological Properties of the Agricultural Land. Environmental Technology 14, 741–751Google Scholar
  54. Moreland DE, Corbin FT, Novitzky WP, Parker CE, Tomer KB (1990): Metabolism of metolachlor by a microsomal fraction isolated from grain sorghum (Sorghum bicolor) shoots. Z Naturforsch 45c, 558–564Google Scholar
  55. Moreland DE, Corbin FT, McFarland JE (1993): Effects of safeners on the oxidation of multiple substrates by grain sorghum microsomes. Pestic Biochem Physiol 45, 43–53CrossRefGoogle Scholar
  56. Moreland DE, Corbin FT, Fleischmann TJ, McFarland JE (1995): Partial characterization of microsomes isolated from mung bean cotyledons. Pestic Biochem Physiol 52, 98–108CrossRefGoogle Scholar
  57. Moss SR (1979): The influence of tillage and method of straw disposal on the survival and growth of black grassAlopecurus myosuroides and its control by chlortoluron and isoproturon. Ann Appl Biol. 91, 91–100CrossRefGoogle Scholar
  58. O’Connell K, Breaux E, Fraley R (1988): Different rates of metabolism of two chloroacetamide herbicides in pioneer 3320 corn. Plant Physiol 86, 359–363Google Scholar
  59. Obrigawitch T, Abernathy JR, Gipson JR (1980): Response of yellow (Cyperus esculentus) and purple (Cyperus rotundus) nutsage to metolachlor. Weed Sci 28, 708–715Google Scholar
  60. Ostrofsky A, Jellison J, Smith K, Shortle W (1997): Cation concentrations in red spruce wood undergoing fungal biodegradation. Can J For 27, 567–571Google Scholar
  61. Perkow W (1988): Wirksubstanzen der Pflanzenschutz- und Schädlingsbekämpfungsmittel. Paul Parey, Berlin-HamburgGoogle Scholar
  62. Ponte-Freitas A, Haddad G, Tissut M, Ravanel P (1991): Distribution of isoproturon, a photosystem II inhibitor, inside wheat leaf fragments. Plant Physiol Biochem 29, 67–74Google Scholar
  63. Raveton M, Ravanel P, Serre AM, Nurit F, Tissut M (1997): Kinetics of uptake and metabolism of atrazine in model plant systems. Pestic Sci 49, 157–163CrossRefGoogle Scholar
  64. Rea PA (1999): MRP subfamily ABC transporters from plants and yeast. J Exp Bot 50, 895–913CrossRefGoogle Scholar
  65. Riechers DE, Irzyk GP, Jones SS, Fuerst EP (1997): Partial characterization of glutathione S-transferases from wheat (Triticum spp) and purification of a safener-induced glutathione S-transferase fromTriticum tauschii. Plant Physiol 114, 1461–1470CrossRefGoogle Scholar
  66. Roberts TE (1998): Metabolic pathways of agrochemicals. Part 1: Herbicides and and plant growth regulators. Royal Society of Chemistry, Cambridge, UKGoogle Scholar
  67. Rossini L, Jepson J, Greenland AE, Sari Gorla M (1996): Characterization of glutathione S-transferase isoforms in three maize inbred lines exhibiting differential sensitivity to alachlor. Plant Physiol 112, 1595–1600Google Scholar
  68. Rossini L, Frova C, Pè ME, Mizzi L, Sari Gorla M (1998): Alachlor regulation of maize glutathione S-transferase genes. Pestic Biochem Physiol 60, 205–211CrossRefGoogle Scholar
  69. Sánchez-Fernández R, Davies TGE, Coleman, JOD, Rea PA (2001): TheArabidopsis thaliana ABC protein superfamily: a complete inventory. J Biol Chem 276, 30231–30244CrossRefGoogle Scholar
  70. Sandermann H, Schmitt H, Eckey R, Bauknecht T (1991): Plant biochemistry of xenobiotics: Isolation and properties of soybean O- and N-glucosyl- and O- and N-malonyltransferases for chlorinated phenols and anilines. Arch Biochem Biophys 287, 341–350CrossRefGoogle Scholar
  71. Sari Gorla M, Ferrario S, Rossini L, Frova C, Villa M (1993): Developmental expression of glutathione S-transferase in maize and its possible connection with herbicide tolerance. Euphytica 67, 221–230CrossRefGoogle Scholar
  72. Schmalfuss J, Matthes B, Knuth K, Boger P (2000): Inhibition of Acyl-CoA elongation by chloroacetamide herbicides in microsomes from leek seedlings. Pestic Biochem Physiol 67, 25–35CrossRefGoogle Scholar
  73. Schmitt R, Sandermann H (1982): Specific localisation of β-glucoside conjugates of 2,4-dichlorophenoxyacetic acid in soybean vacuoles, Z. Naturforsch 37c, 772–777Google Scholar
  74. Schröder P (1997): Fate of glutathione S-conjugates in plants: Cleavage of the glutathione moiety. In: Hatzios KK (Ed): Regulation of enzymatic systems detoxifying xenobiotics in plants, NATO ASI Series Vol 37, Kluwer Academic Publishers, Dordrecht, The Netherlands, 233–244Google Scholar
  75. Scheunert I, Schröder P (1998): Formation, Characterization and Release of Non-Ectractable Residues of [C-14]-Labeled Organic Xenobiotics in Soils. ESPR — Environ Sci & Pollut Res 5, 238–245CrossRefGoogle Scholar
  76. Schülein J, Gläßgen WE, Hertkorn N, Schröder P, Sandermann H, Kettrup A (1996): Detection and identification of the herbicide isoproturon and its metabolites in soil solution, runoff and surface water after a heavy rainfall event. Int J Env Analyt Chem 65, 193–202CrossRefGoogle Scholar
  77. Shah DM, Horsch RB, Klee HJ, Kishore GM, Winter JA, Turner NE, Hironaka CM, Sanders PR, Gasser CS, Aykent S, Siegel NR, Rogers SG, Fraley RT (1986): Engineering herbicide tolerance in transgenic plants. Science 233, 478–481CrossRefGoogle Scholar
  78. Shao ZQ, Behki R (1995): Cloning of the genes for degradation of the herbicides EPTC (S-Ethyl Dipropylthiocarbamate) and Atrazine fromRhodococcus sp. Strain TE1. Applied and Environmental Microbiology 61, 2061–2065Google Scholar
  79. Shimabukuro RH, Frear DS, Swanson HR, Walsh WC (1971): Glutathione conjugation. An enzymatic basis for atrazine resistance in corn. Plant Physiol 47, 10–14CrossRefGoogle Scholar
  80. Skipsey M, Andrews CJ, Towson JK, Jepson I, Edwards R (1997): Substrate and thiol specificity of a stress-inducible glutathione transferase from soybean. FEBS Lett 409, 370–374CrossRefGoogle Scholar
  81. Smith AE (1988): Transformations in soil, environmental chemistry of herbicides, R. Grover, Boca Raton, FLA, CRC Press, pp 171–200Google Scholar
  82. Tasli S, Patty L, Boetti H, Ravanel P, Vachaud G, Scharff C, Favre-Bonvin J, Kaouadji M, Tissut M (1996): Persistence and leaching of atrazine in corn culture in the experimental site of La Cote Saint Andre (Isere, France). Arch Environ Contam Toxicol 30, 203–212CrossRefGoogle Scholar
  83. Thurman E. M., Goolsby D.A., Aga D.S., Pomes M.L., Meyer M.T. (1996): Occurrence of alachlor and its sulphonated metabolite in rivers and reservoirs of the midwestern United States: the importance of sulphonation in the transport of chloroacetanilide herbicides. Environ. Science & Technology 30, 569–574CrossRefGoogle Scholar
  84. Timmerman KP (1989): Molecular charaterization of corn glutathione S-transferase isozymes involved in herbicide detoxication. Physiologia Plantarum 77, 465–471CrossRefGoogle Scholar
  85. Wiegand RC, Shah DM, Mozer TJ, Harding EI, Diaz-Collier J, Saunders C, Jaworsky EG, Tiemeier DC (1986): Messenger RNA encoding a glutathione S-transferase responsible for herbicide tolerance in maize is induced in response to safener treatment. Plant Mol Biol 7, 235–243CrossRefGoogle Scholar
  86. Wilson RD, Geronimo J, Armbruster JA (1997): 2,4-D Dissipation in field soils after applications of 2,4-D dimethylamine salt and 2,4-D 2-ethylhexyl ester. Environmental Toxicology and Chemistry 16, 1239–1246CrossRefGoogle Scholar
  87. Wittmann C, Hock B (1991): Development of an ELISA for the analysis of atrazine metabolites deethylatrazine and deisopropylatrazine. J Agric Food Chem 39, 1194–1200CrossRefGoogle Scholar
  88. Wolf AE, Dietz KJ, Schroeder P (1996): Degradation of glutathione S-conjugates by a carboxypeptidase in the plant vacuole. FEBS Letters 384, 31–34CrossRefGoogle Scholar
  89. Wu J, Omokawa H, Hatzios KK (1996): Glutathione S-transferase activity in unsafened and fenchlorim-safened rice (Oryza sativa). Pestic Biochem Physiol 54, 220–229CrossRefGoogle Scholar
  90. Wu J, Cramer CL, Hatzios KK (1999): Characterization of two cDNAs encoding glutathione S-transferases in rice and induction of their transcription by the herbicide safener fenchlorim. Physiol Plantarum 105, 102–108CrossRefGoogle Scholar
  91. Yadav A, Malik RK (1988): Persistence of isoproturon in different soils. Haryana Agric Univ J Res 18, 198–206Google Scholar

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© Ecomed Publishers 2002

Authors and Affiliations

  • Julian O. D. Coleman
    • 1
  • Carla Frova
    • 2
  • Peter Schröder
    • 3
  • Michel Tissut
    • 4
  1. 1.School of Biological and Molecular SciencesOxford Brookes UniversityOxfordUK
  2. 2.Department of Genetics and MicrobiologyUniversity of MilanoMilanoItaly
  3. 3.GSF-Institute for Soil EcologyGSF Research Centre for Environment and HealthNeuherbergGermany
  4. 4.Laboratoire Ecosystèmes et Changements EnvironnementauxUniversité J. FourierGrenoble cedex 9France

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