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New Perspectives on the Metabolism and Detoxification of Synthetic Compounds in Plants

  • Robert Edwards
  • David P. Dixon
  • Ian Cummins
  • Melissa Brazier-Hicks
  • Mark Skipsey
Chapter
Part of the Plant Ecophysiology book series (KLEC, volume 8)

Abstract

In attempting to understand the mechanisms by which plants process synthetic compounds we have developed the concept of the ‘Xenome’, which we define as ‘the biosystem responsible for the detection, transport and detoxification of xenobiotics.’ In particular the last 10 years have given us unprecedented insights into the proteins responsible for the metabolism and transport of xenobiotics within plant cells and how these systems are regulated. In this review we identify recent advances in our understanding of the xenome and its role in the detoxification and processing of pollutants and pesticides. In particular, we focus on the role of the phase 1 (oxidoreductase/ hydrolytic), phase 2 (bioconjugation), phase 3 (transport) and phase 4 (metabolic recycling) stages of xenobiotic metabolism and the biosensing systems which control their expression. Ultimately, by understanding the capability of the plant xenome to detoxify xenobiotics, we may be able to predict the likely fate and environmental risk of new synthetic compounds entering the environment and food chain.

Keywords

Xenobiotic Metabolism Glutathione Conjugate Xenobiotic Detoxification Cyhalofop Butyl Herbicide Metabolism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Axarli I, Dhavala P, Papageorgiou AC, Labrou NE (2009) Crystallographic and functional ­characterization of the fluorodifen-inducible glutathione transferase from Glycine max reveals an active site topography suited for diphenylether herbicides and a novel L-site. J Mol Biol 385:984–1002PubMedGoogle Scholar
  2. Baerson SR, Sánchez-Moreiras A, Pedrol-Bonjoch N, Schulz M, Kagan IA, Agarwal AK, Reigosa MJ, Duke SO (2005) Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2 (3H)-one. J Biol Chem 280:21867–21881PubMedGoogle Scholar
  3. Barrett M (2000) The role of cytochrome P450 enzymes in herbicide metabolism. In: Cobb AH, Kirkwood RC (eds) Herbicides and their mechanisms of action. Sheffield Academic Press, SheffieldGoogle Scholar
  4. Beck A, Lendzian K, Oven M et al (2003) Phytochelatin synthase catalyzes key step in turnover of glutathione conjugates. Phytochemistry 62:423–431PubMedGoogle Scholar
  5. Beynon ER, Symons ZC, Jackson RG et al (2009) The role of oxophytodienoate reductases in the detoxification of the explosive 2, 4, 6-trinitrotoluene by Arabidopsis. Plant Physiol 151:253–261PubMedGoogle Scholar
  6. Blum R, Beck A, Korte A et al (2007) Function of phytochelatin synthase in catabolism of glutathione-conjugates. Plant J 49:740–749PubMedGoogle Scholar
  7. Brazier-Hicks M, Edwards LA, Edwards R (2007a) Selection of plants for roles in phytomediation: the importance of glucosylation. Plant Biotechnol J 5:627–635PubMedGoogle Scholar
  8. Brazier-Hicks M, Offen WA, Gershater MC et al (2007b) Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proc Ntl Acad Sci USA 104:20238–20243Google Scholar
  9. Brazier-Hicks M, Evans KM, Cunningham OD et al (2008) Catabolism of glutathione conjugates in Arabidopsis thaliana – role in metabolic reactivation of the herbicide safener fenclorim. J Biol Chem 283:21102–21112PubMedGoogle Scholar
  10. Chen L, Yang J (2008) Biochemical characterization of the tetrachlorobenzoquinone reductase involved in the biodegradation of pentachlorophenol. Int J Mol Sci 9:198PubMedGoogle Scholar
  11. Clemens S, Peršoh D (2009) Multi-tasking phytochelatin synthases. Plant Sci 177:266–271Google Scholar
  12. Cole DJ, Edwards R (2000) Secondary metabolism of agrochemcials in plants. In: Roberts TR (ed) Agrochemicals and plant protection. Wiley, ChichesterGoogle Scholar
  13. Cummins I, Edwards R (2004) Purification and cloning of an esterase from the weed black-grass (Alopecurus myosuroides), which bioactivates aryloxyphenoxypropionate herbicides. Plant J 39:894–904PubMedGoogle Scholar
  14. Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292PubMedGoogle Scholar
  15. Cummins I, Burnet M, Edwards R (2001) Biochemical characterisation of esterases active in hydrolysing xenobiotics in wheat and competing weeds. Phys Planta 113:477–485Google Scholar
  16. Cummins I, Landrum M, Steel PG, Edwards R (2007) Structure activity studies with xenobiotic substrates using carboxylesterases isolated from Arabidopsis thaliana. Phytochemistry 68:811–818PubMedGoogle Scholar
  17. Cummins I, Bryant DN, Edwards R (2009) Safener responsiveness and multiple herbicide ­resistance in the weed black-grass (Alopecurus myosuroides). Plant Biotechnol J 7:807–820PubMedGoogle Scholar
  18. Davies J, Caseley JC (1999) Herbicide safeners: a review. Pestic Sci 55:1043–1058Google Scholar
  19. De Veylder L, Van Montagu M, Inz D (1997) Herbicide safener-inducible gene expression in Arabidopsis thaliana. Plant Cell Physiol 38:568–577PubMedGoogle Scholar
  20. Del Buono D, Scarponi L, Espen L (2007) Glutathione S-transferases in Festuca arundinacea: Identification, characterization and inducibility by safener benoxacor. Phytochemistry 68:2614–2624PubMedGoogle Scholar
  21. DeRidder BP, Goldsbrough PB (2006) Organ-specific expression of glutathione S-transferases and the efficacy of herbicide safeners in Arabidopsis. Plant Physiol 140:167–175PubMedGoogle Scholar
  22. Didierjean L, Gondet L, Perkins R et al (2002) Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol 130:179–189PubMedGoogle Scholar
  23. Dixit P, Mukherjee P, Sherkhane P, Kale S, Eapen S (2009) Phytoremediation of anthracene by transgenic tobacco plants with a fungal glutathione-S-transferase gene. New Biotechnol 25:S291–S292Google Scholar
  24. Dixon DP, Edwards R (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J Biol Chem 284:21249–21256PubMedGoogle Scholar
  25. Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266PubMedGoogle Scholar
  26. Dixon DP, Cole DJ, Edwards R (2000) Characterisation of a zeta class glutathione transferase from Arabidopsis thaliana with a putative role in tyrosine catabolism. Arch Biochem Biophys 384:407–412PubMedGoogle Scholar
  27. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants - Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869PubMedGoogle Scholar
  28. Dixon DP, McEwen AG, Lapthorn AJ, Edwards R (2003) Forced evolution of a herbicide detoxifying glutathione transferase. J Biol Chem 278:23930–23935PubMedGoogle Scholar
  29. Dixon DP, Lapthorn A, Madesis P et al (2008) Binding and glutathione conjugation of ­porphyrinogens by plant glutathione transferases. J Biol Chem 283:20268–20276PubMedGoogle Scholar
  30. Dixon DP, Hawkins T, Hussey PJ, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:1207–1218PubMedGoogle Scholar
  31. Doty SL, James CA, Moore AL et al (2007) Enhanced phytoremediation of volatile environmental pollutants with transgenic trees. Proc Ntl Acad Sci USA 104:16816–16821Google Scholar
  32. Durst F, O’Keefe DP (1995) Plant cytochromes P450: an overview. Drug Metab Drug Interact 12:171Google Scholar
  33. Edwards R, Dixon DP (2000) The role of glutathione transferases in herbicide metabolism. In: Cobb AH, Kirkwood RC (eds) Herbicides and their mechanisms of action. Sheffield Academic Press, Sheffield, UKGoogle Scholar
  34. Edwards R, Dixon DP (2005) Plant glutathione transferases: Glutathione transferases and gamma-glutamyl transpeptidases. Methods Enzymol 401:169–186PubMedGoogle Scholar
  35. Edwards R, Owen WJ (1986) Comparison of glutathione S-transferases of Zea mays responsible for herbicide detoxification in plants and suspension-cultured cells. Planta 169:208–215Google Scholar
  36. Edwards R, Brazier-Hicks M, Dixon DP, Cummins I (2005a) Chemical manipulation of ­antioxidant defences in plants. Adv Bot Res 42:1–32Google Scholar
  37. Edwards R, Del Buono D, Fordham M et al (2005b) Differential induction of glutathione ­transferases and glucosyltransferases in wheat, maize and Arabidopsis thaliana by herbicide safeners. Zeit f Naturforsch 60c:307–316Google Scholar
  38. Ertunç T, Schmidt B, Kühn H et al (2004) Investigation on the chemical structure of nonextractable residues of the fungicide cyprodinil in spring wheat using 13C-C 1-phenyl-cyprodinil on 13C-depleted plants: an alternative approach to investigate nonextractable residues. J Environ Sci Health B 39:689–707PubMedGoogle Scholar
  39. Farkas MH, Berry JO, Aga DS (2007) Chlortetracycline detoxification in maize via induction of glutathione S-transferases after antibiotic exposure. Environ Sci Technol 41:1450–1456PubMedGoogle Scholar
  40. Foyer CH (2001) Prospects for enhancement of the soluble antioxidants, ascorbate and glutathione. Biofactors 15:75–78PubMedGoogle Scholar
  41. Frear DS (1968) Purification and properties of UDP-glucose:arylamine N-glucosyltransferase from soybean. Phytochemistry 7:381–390Google Scholar
  42. Frear DS, Swanson HR, Tanaka FS (1969) N-Demethylation of substituted 3-(phenyl)-1-­methylureas - isolation and characterization of a microsomal mixed function oxidase from cotton. Phytochemistry 8:2157–2163Google Scholar
  43. Frova C (2006) Glutathione transferases in the genomics era: new insights and perspectives. Biomol Eng 23:149–169PubMedGoogle Scholar
  44. Gallandt ER, Balke NE (1995) Xenobiotic glucosyltransferase activity from suspension cultured Glycine max cells. Pestic Sci 43:31–40Google Scholar
  45. Geisler M, Girin M, Brandt S et al (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15:3393PubMedGoogle Scholar
  46. Gershater M, Edwards R (2007) Regulating biological activity in plants with carboxylesterases. Plant Sci 173:579–588Google Scholar
  47. Gershater M, Sharples K, Edwards R (2006) Carboxylesterase activities toward pesticide esters in crops and weeds. Phytochemistry 67:2561–2567PubMedGoogle Scholar
  48. Gershater MC, Cummins I, Edwards R (2007) Role of a carboxylesterase in herbicide bioactivation in Arabidopsis thaliana. J Biol Chem 282:21460–21466PubMedGoogle Scholar
  49. Griesser M, Vitzthum F, Fink B, Bellido ML, Raasch C, Munoz-Blanco J, Schwab W (2008) Multi-substrate flavonol O-glucosyltransferases from strawberry (Fragaria x ananassa) achene and receptacle. J Exp Bot 59:2611–2625PubMedGoogle Scholar
  50. Grill E, Löffler S, Winnacker E, Zenk M (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl ­transpeptidase (phytochelatin synthase). Proc Ntl Acad Sci USA 86:6838–6842Google Scholar
  51. Grzam A, Martin MN, Hella R, Meyer AJ (2007) γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Letts 581:3131–3138Google Scholar
  52. Guengerich FP (2001) Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 14:611–650PubMedGoogle Scholar
  53. Hall LM, Moss SR, Powles SB (1997) Mechanisms of resistance to aryloxyphenoxypropionate herbicides in two resistant biotypes of Alopecurus myosuroides (blackgrass): herbicide ­metabolism as a cross-resistance mechanism. Pestic Biochem Physiol 57:87–98Google Scholar
  54. Haslam R, Raveton M, Cole DJ et al (2001) The identification and properties of apoplastic ­carboxylesterases from wheat that catalyse deesterification of herbicides. Pestic Biochem Physiol 71:178–189Google Scholar
  55. Hatzios KK, Burgos N (2004) Metabolism-based herbicide resistance: regulation by safeners. Weed Sci 52:454–467Google Scholar
  56. Hefner T, Arend J, Warzecha H et al (2002) Arbutin Synthase, a novel member of the NRDIβ glycosyltransferase family, is a unique multifunctional enzyme converting various natural products and xenobiotics. Bioorg Med Chem 10:1731–1741PubMedGoogle Scholar
  57. Hirase K, Hoagland RE (2006) Characterization of aryl acylamidase activity from propanil-resistant barnyardgrass (Echinochloa crus-galli [L.] Beauv.). Weed Biol Manage 6:197–203Google Scholar
  58. Huber C, Bartha B, Harpaintner R, Schröder P (2009) Metabolism of acetaminophen (paracetamol) in plants-two independent pathways result in the formation of a glutathione and a glucose conjugate. Environ Sci Pollut Res 16:206–213Google Scholar
  59. Inui H, Shiota N, Motoi Y et al (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 26:28–40Google Scholar
  60. Jakobsson PJ, Morgenstern R, Mancini J et al (1999) Common structural features of MAPEG – a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci 8:689–692PubMedGoogle Scholar
  61. Karavangeli M, Labrou NE, Clonis YD, Tsaftaris A (2005) Development of transgenic tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide herbicides ­phytoremediation. Biomol Eng 22:121–128PubMedGoogle Scholar
  62. Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABC) subfamily of ATP-binding cassette transporters in plants. FEBS Letts 580:1112–1122Google Scholar
  63. Labrou NE, Kotzia GA, Clonis YD (2004) Engineering the xenobiotic substrate specificity of maize glutathione S-transferase I. Protein Eng Design Selec 17:741–748Google Scholar
  64. Lamoureux GL, Rusness DG (1993) Glutathione in the metabolism and detoxification of xenobiotics in plants. In: De Kok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants. SPB Academic Publishing, The HagueGoogle Scholar
  65. Lao S, Loutre C, Brazier M et al (2003) 3, 4-Dichloroaniline is detoxified and exported via ­different pathways in Arabidopsis and soybean. Phytochemistry 63:653–661PubMedGoogle Scholar
  66. Leah J, Caseley J, Riches C, Valverde B (1994) Association between elevated activity of aryl acylamidase and propanil resistance in jungle-rice, Echinochloa colona. Pest Manage Sci 42:281–289Google Scholar
  67. Liu G, Sánchez-Fernández R, Li ZS, Rea PA (2001) Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J Biol Chem 276:8648PubMedGoogle Scholar
  68. Loutre C, Dixon DP, Brazier M et al (2003) Isolation of a glucosyltransferase from Arabidopsis thaliana active in the metabolism of the persistent pollutant 3, 4-dichloroaniline. Plant J 34:485–495PubMedGoogle Scholar
  69. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Ann Rev Plant Physiol Plant Mol Biol 47:127–158Google Scholar
  70. Marshall S, Putterill J, Plummer K, Newcomb R (2003) The carboxylesterase gene family from Arabidopsis thaliana. J Mol Evo 57:487–500Google Scholar
  71. Martin MN, Saladores PH, Lambert E et al (2007) Localization of members of the γ-glutamyl transpeptidase family identifies sites of glutathione and glutathione S-conjugate hydrolysis. Plant Physiol 144:1715–1732PubMedGoogle Scholar
  72. Martinoia E, Grill E, Tommasini R et al (1993) ATP-dependent glutathione S-conjugate export pump in the vacuolar membrane of plants. Nature 364:247–249Google Scholar
  73. Menendez J, Prado RD (1996) Diclofop-methyl cross-resistance in a chlorotoluron-resistant ­biotype of Alopecurus myosuroides. Pestic Biochem Physiol 56:123–133Google Scholar
  74. Milligan AS, Daly A, Parry MAJ et al (2001) The expression of a maize glutathione S-transferase gene in transgenic wheat confers herbicide tolerance, both in planta and in vitro. Mol Breed 7:301–315Google Scholar
  75. Morant M, Bak S, Møller BL, Werck-Reichhart D (2003) Plant cytochromes P450: tools for ­pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol 14:151–162PubMedGoogle Scholar
  76. Novakova M, Mackova M, Chrastilova Z et al (2009) Cloning the bacterial bphC gene into Nicotiana tabacum to improve the efficiency of PCB phytoremediation. Biotech Bioeng 102:29–37Google Scholar
  77. Ohkama-Ohtsu N, Zhao P, Xiang CB, Oliver DJ (2007) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888PubMedGoogle Scholar
  78. Ohkama-Ohtsu N, Oikawa A, Zhao P et al (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613PubMedGoogle Scholar
  79. Pflugmacher S, Sandermann H Jr (1998) Taxonomic distribution of plant glucosyltransferases acting on xenobiotics. Phytochemistry 49:507–511Google Scholar
  80. Poppenberger B, Berthiller F, Lucyshyn D et al (2003) Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914PubMedGoogle Scholar
  81. Prade L, Huber R, Bieseler B (1998) Structures of herbicides in complex with their detoxifying enzyme glutathione S-transferase – explanations for the selectivity of the enzyme in plants. Structure 6:1445–1452PubMedGoogle Scholar
  82. Preston C, Tardif FJ, Powles SB (1995) Multiple mechanisms and multiple herbicide resistance in Lolium rigidum. In: Brown TM (ed) ACS Agrochemicals-Division Special Conference VI on Molecular Genetics and Ecology of Pesticide Resistance. Mt ACS Press, Big SkyGoogle Scholar
  83. Prosecka J, Orlov AV, Fantin YS et al (2009) A novel ATP-binding cassette transporter is responsible for resistance to viologen herbicides in the cyanobacterium Synechocystis sp. PCC 6803. FEBS J 276:4001–4011PubMedGoogle Scholar
  84. Raichaudhuri A, Peng MS, Naponelli V et al (2009) Plant vacuolar ATP-binding cassette transporters that translocate folates and antifolates in vitro and contribute to antifolate tolerance in vivo. J Biol Chem 284:8449–8460PubMedGoogle Scholar
  85. Ruiz-Santaella JP, Heredia A, De Prado R (2006) Basis of selectivity of cyhalofop-butyl in Oryza sativa L. Planta 223:191–199PubMedGoogle Scholar
  86. Rylott EL, Jackson RG, Edwards J et al (2006) An explosive-degrading cytochrome P450 activity and its targeted application for the phytoremediation of RDX. Nat Biotechnol 24:216–219PubMedGoogle Scholar
  87. Sánchez-Fernández R, Davies T, Coleman J, Rea P (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244PubMedGoogle Scholar
  88. Sandermann H Jr, Schmitt R, Eckey H, Bauknecht T (1991) Plant biochemistry of xenobiotics – isolation and properties of soybean O-glucosyl and N-glucosyl and O-malonyltransferase and N-malonyltransferase for chlorinated phenols and anilines. Arch Biochem Biophys 287:341–350PubMedGoogle Scholar
  89. Schoch G, Goepfert S, Morant M et al (2001) CYP98A3 from Arabidopsis thaliana is a 3’-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574PubMedGoogle Scholar
  90. Scott-Craig JS, Casida JE, Poduje L, Walton JD (1998) Herbicide safener-binding protein of maize. Plant Physiol 116:1083–1089PubMedGoogle Scholar
  91. Skipsey M, Cummins I, Andrews CJ et al (2005) Manipulation of plant tolerance to herbicides through co-ordinated metabolic engineering of a detoxifying glutathione transferase and thiol cosubstrate. Plant Biotechnol J 3:409–420PubMedGoogle Scholar
  92. Sonoki T, Kajita S, Ikeda S et al (2005) Transgenic tobacco expressing fungal laccase promotes the detoxification of environmental pollutants. Appl Microbiol Biotechnol 67:138–142PubMedGoogle Scholar
  93. Taguchi G, Nakamura M, Hayashida N, Okazaki M (2003) Exogenously added naphthols induce three glucosyltransferases, and are accumulated as glucosides in tobacco cells. Plant Sci 164:231–240Google Scholar
  94. Rea PA (2007) Plant ATP-binding cassette transporters. Ann Rev Plant Biol 58:347–375Google Scholar
  95. Taguchi G, Shitchi Y, Sakiko S et al (2005) Molecular cloning, characterization, and downregulation of an acyltransferase that catalyzes the malonylation of flavonoid and naphthol glucosides in tobacco cells. Plant J 42:481–491PubMedGoogle Scholar
  96. Tanaka S, Brentner LB, Merchie KM et al (2007) Analysis of gene expression in poplar trees (Populus deltoides Nigra, DN34) Exposed to the Toxic Explosive Hexahydro-1, 3, 5-Trinitro-1, 3, 5-Triazine (RDX). Int J Phytorem 9:15–30Google Scholar
  97. Theodoulou FL, Clark IM, He XL et al (2003) Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manage Sci 59:202–214Google Scholar
  98. Uchida E, Ouchi T, Suzuki Y et al (2005) Secretion of bacterial xenobiotic-degrading enzymes from transgenic plants by an apoplastic expressional system: an applicability for phytoremediation. Environ Sci Technol 39:7671PubMedGoogle Scholar
  99. Van Eerd LL, Hoagland RE, Zablotowicz RM, Hall JC (2009) Pesticide metabolism in plants and microorganisms. Weed Sci 51:472–495Google Scholar
  100. Verrier PJ, Bird D, Burla B et al (2008) Plant ABC proteins – a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159PubMedGoogle Scholar
  101. Wang G-D, Li Q-J, Luo B, Chen X-Y (2004) Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat Biotechnol 22:893–897PubMedGoogle Scholar
  102. Wang L, Samac DA, Shapir N, Wackett LP, Vance CP, Olszewski NE, Sadowsky MJ (2005) Biodegradation of atrazine in transgenic plants expressing a modified bacterial atrazine ­chlorohydrolase (atzA) gene. Plant Biotechnol J 3:475–486PubMedGoogle Scholar
  103. Watanabe T (2002) Transcuticular penetration of foliar-applied pesticides—its analysis by a logistic-kinetic penetration model. In: Böger P, Wakabayashi K, Hirai K (eds) Herbicide classes in development. Springer-Verlag, BerlinGoogle Scholar
  104. Windsor B, Roux S, Lloyd A (2003) Multiherbicide tolerance conferred by AtPgp1 and apyrase overexpression in Arabidopsis thaliana. Nat Biotechnol 21:428–433PubMedGoogle Scholar
  105. Wolf AE, Dietz K-J, Schröder P (1996) Degradation of glutathione S-conjugates by a carboxy­peptidase in the plant vacuole. FEBS Lett 384:31–34PubMedGoogle Scholar
  106. Wünschmann J, Krajewski M, Letzel T, Huber EM, Ehrmann A, Grill E, Lendzian KJ (2010) Dissection of glutathione conjugate turnover in yeast. Phytochemistry 71:54–61PubMedGoogle Scholar
  107. Yuan JS, Tranel PJ, Stewart CN (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13PubMedGoogle Scholar
  108. Zhang Q, Xu FX, Lambert KN, Riechers DE (2007) Safeners coordinately induce the expression of multiple proteins and MRP transcripts involved in herbicide metabolism and detoxification in Triticum tauschii seedling tissues. Proteomics 7:1261–1278PubMedGoogle Scholar
  109. Zhao Y, Chow T, Puckrin RS, Alfred SE, Korir AK, Larive CK, Cutler SR (2007) Chemical genetic interrogation of natural variation uncovers a molecule that is glycoactivated. Nat Chem Biol 3:716–721PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Robert Edwards
    • 1
  • David P. Dixon
    • 2
  • Ian Cummins
    • 2
  • Melissa Brazier-Hicks
    • 2
  • Mark Skipsey
    • 2
  1. 1.The Food and Environment AgencySand Hutton, YorkUK
  2. 2.Centre for Bioactive ChemistryDurham University, School of Biological and Biomedical SciencesDurhamUK

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