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Induction and inactivation of a cytochrome P450 confering herbicide resistance in wheat seedlings

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Summary

Cytochrome P450-dependent enzymes from wheat catalyze the oxidation of endogenous compounds (lauric and oleic acids) and of several herbicides (diclofop, chlortoluron, bentazon). Treatment of wheat seedlings with the safener, naphthalic anhydride and with phenobarbital increases dramatically several P450-dependent enzyme activities including diclofop and lauric acid hydroxylation. The parallel induction of lauric acid (ω-1)-hydroxylase and diclofop hydroxylase activities suggests that both compounds proceeds from the same or very similar forms of P450. To test whether either one or multiple P450 forms are involved in these oxidations, we have designed selective irreversible inhibitors of lauric acid (ω-1)-hydroxylase. Results of in vivo and in vitro experiments with acetylenic analogs of lauric acid (10- and 11-dodecynoic acids) strongly suggest that a single P450 catalyzes both laurate and diclofop hydroxylation. Treatment of wheat seedlings with these acetylenes results in a strong inhibition of the in vivo metabolism of diclofop although oxidation of chlortoluron and bentazon are not affected. Our results suggest that at least three distinct P450 forms are involved in the detoxification process of the three herbicides. Interestingly, we also demonstrate that herbicides themselves are potent inducers of the amount of total P450 and laurate/diclofop hydroxylase activies. This increased capacity of wheat to detoxify the herbicide through the induction of P450 enzymes seems to be for a large extend the mechanism which confers a tolerance on various herbicides.

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References

  1. McFadden J. J., Frear D. S., Mansager E. R. (1989) Aryl hydroxylation of diclofop by a cytochrome P450-dependent monooxygenase from wheat. Pestic. Biochem. Physiol., 34, 92–100.

    Article  CAS  Google Scholar 

  2. Sweetser P. B., Show G. S., Hutchison J. M. (1982): Metabolism of chlorsulfuron by plants: biological basis for selectivity of a new herbicide for cereals. Pestic. Biochem. Physiol., 17, 18–23.

    Article  CAS  Google Scholar 

  3. Cabanne C. F., Huby D., Gaillardon P., Scalla R., Durst F. (1987): Effect of the cytochrome P450 inactivator 1-aminobenzotriazole on the metabolism of chlortoluron and isoproturon in wheat. Pestic. Biochem. Physiol., 28, 371–380.

    Article  CAS  Google Scholar 

  4. Shimabukuro R. H., Walsh W. C., Jacobson A. (1987): Aryl-O-glucoside of diclofop: a detoxication product in wild oat and wheat. J. Agric. Food Chem., 35, 393–397.

    Article  CAS  Google Scholar 

  5. Burton J. D., Gronwald J. W., Somers D. A., Gengenbach B. G., Wyse D. L. (1987): Inhibition of plant acetyl-coenzyme A carboxylase by the herbicides sethoxydim and haloxyfop. Biochem. Biophys. Res. Commun., 148, 1039–1044.

    Article  PubMed  CAS  Google Scholar 

  6. Shimabukuro R. H., Walsh W. C., Hoerauf R. A. (1979): Metabolism and selectivity of diclofop-methyl in wild oat and wheat. J. Agric. Food Chem., 27, 615–623.

    Article  PubMed  CAS  Google Scholar 

  7. Zimmerlin A., Durst F. (1990): Xenobiotic metabolism in higher plants: aryl hydroxylation of diclofop by a cytochrome P-450 enzyme from wheat. Phytochemistry, 29, 1729–1732.

    Article  CAS  Google Scholar 

  8. Zimmerlin A., Salalin J. P., Durst F., Mioskowski C. (1992): Cytochrome P-450-dependent hydroxylation of lauric acid at the subterminal position and oxidation of unsaturated analogs in wheat microsomes. Plant Physiol., 100, 868–873.

    Article  PubMed  CAS  Google Scholar 

  9. Helvig C., Tardif F. J., Seyer A., Powles S. B., Mioskowski C., Durst F., Salaün J. P. (1996): Selective inhibition of a cytochrome P450 enzyme in wheat that oxidizes both the natural substrate lauric acid and the synthetic herbicide diclofop. Pestic. Biochem. Physiol., 54, 161–171.

    Article  CAS  Google Scholar 

  10. Pinot F., Alayrac C., Mioskowski C., Durst F., Salaün J. P. (1994): New cytochrome P450-dependent reactions from wheat-Terminal and sub-terminal hydroxylation of oleic acid by microsomes from naphthalic acid anhydride and phenobarbital-induced wheat seedlings. Biochem. Biophys. Res. Commun., 198, 795–803.

    Article  PubMed  CAS  Google Scholar 

  11. Mougin C., Cabanne F., Canivenc M.-C., Scalla R. (1990): Hydroxylation and N-demethylation of chlortoluron, by wheat microsomal enzymes. Plant Sci., 66, 195–203.

    Article  CAS  Google Scholar 

  12. Baerg R., Barrett M., Polge N. (1996) Insecticide and insecticide metabolite interactions with cytochrome P450 mediated activities in maize. Pestic. Biochem. Physiol., 55, 10–20.

    Article  PubMed  CAS  Google Scholar 

  13. Amet Y., Goasduff T., Salaün J.P., Lebreton L., Menez J. F. (1994): Evidence that cytochrome P450 2E1 is involved in the (omega-1)-hydroxylation of lauric acid in rat liver microsomes. Biochem. Biophys. Res. Commun., 203, 1168–1174.

    Article  PubMed  CAS  Google Scholar 

  14. McGonigle B., Lau S. M. C., O’Keefe D. P. (1997): Endogenous reaction and sustrate specificity of herbicide metabolizing enzymes, in Hatzios K. K. (Ed.). Regulation of Enzymatic Systems Detoxifying Xenobiotics in Plants. London, Kluwer Acad. Publ., 9–18.

    Google Scholar 

  15. Salaün J.-P., Helvig C. (1995): Cytochrome P450-dependent oxidation of fatty acids. Drug Metab. Drug Interact., 12, 261–283.

    Google Scholar 

  16. Pinot F., Salaün J.-P., Bosch H., Lesot A., Mioskowski C., Durst F. (1992): ω-Hydroxylation of Z9-octadecenoic, Z9,10-epoxystearic and 9,10-dihydroxystearic acids by microsomal cytochrome P450 systems from Vicia sativa, Biochem. Biophys. Res. Commun., 184, 183–193.

    Article  PubMed  CAS  Google Scholar 

  17. Schweizer P., Jeanguenat A., Métraux J.-P., Mösinger E. (1996): Induction of resistance in barley against Erysiphe graminis f.sp. hordei by free cutin monomers, Physiol. Mol. Plant Pathol., 49, 103–120.

    Article  CAS  Google Scholar 

  18. Alborn H.T., Turlings T.C., Jones T. H, Stenhagen G., Loughrin J.H., Tumlinson J.H. (1997): An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945–948.

    Article  CAS  Google Scholar 

  19. Farmer E. E. (1997): New fatty acid-based signals: a lesson from plant world. Science, 276, 912–913.

    Article  CAS  Google Scholar 

  20. Reichhart D., Salaün J.-P., Benveniste I., Durst F. (1980): Time course of induction of cytochrome P-450, NADPH-cytochrome c reductase, and cinnamic acid hydroxylase by phenobarbital, ethanol, herbicides, and manganese in higher plant microsomes. Plant Physiol., 66, 600–604.

    Article  PubMed  CAS  Google Scholar 

  21. Moreland D. E., Corbin F. T., McFarland J. E. (1993): Effects of safeners on the oxidation of multiple substrates by grain sorghum microsomes. Pestic. Biochem. Physiol., 45, 43–53.

    Article  CAS  Google Scholar 

  22. Canivenc M.-C., Cagnac B., Cabanne F. (1989): Induced changes of chlortoluron metabolism in wheat cell suspension cultures. Plant Physiol. Biochem., 27, 193–201.

    CAS  Google Scholar 

  23. Kreuz K., Gaudin J., Stingelin J., Ebert E. (1991): Metabolism of the aryloxyphenoxypropanoate herbicide, CGA-184927, in wheat, barley and maize — Differential effects of the safener, CGA-185072. Z. Naturforsch. C., 46, 901–905.

    CAS  Google Scholar 

  24. Anderson, J. J., Swain R. S. (1992): Metabolism of sulfometuron-methyl in wheat and its possible role in wheat intolerance. J. Agric. Food Chem., 40, 2279–2283.

    Article  CAS  Google Scholar 

  25. Durst F., Benveniste I., Salaün J.-P., Werck D. (1994): Function and diversity of plant cytochrome P450. In: Lechner M.C. (Ed.). Cytochrome P450. France, John Libbey Eurotext, 23–30.

    Google Scholar 

  26. Shimabukuro R. H., Hoffer B. L. (1997): Perturbation of the transmembrane proton gradient and resistance to AOPP herbicides. In: De Prado R., Jorrin J., Garcia-Thorres L. (Eds.). Weed and Crop Resistance to Herbicides. London, Kluwer Acad. Publ., 71–79.

    Google Scholar 

  27. Burnet M. W. M., Loveys B. R., Holtum J. A. M., Powles S. B. (1993): A mechanism of chlortoluron resistance in Lolium rigidum. Planta, 190, 182–189.

    Article  CAS  Google Scholar 

  28. Mougin C., Cabanne F., Scalla R. (1992): Additional observations on the chlorotoluron hydroxylase and N-demethylase activities in wheat microsomes. Plant Physiol. Biochem., 30, 769–778.

    CAS  Google Scholar 

  29. Preston C., Tardif F. J., Christopher J. T., Powles S. B. (1996): Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide-degrading enzymes. Pestic. Biochem. Physiol., 54,123–134.

    Article  CAS  Google Scholar 

  30. Johnson E. F., Palmer C. N. A., Griffin K. J., Hsu M. H. (1996): Cytochromes P450. 7. Role of the peroxisome proliferator-activated receptor in cytochrome P450 4A gene regulation. FASEB J., 10, 1241–1248.

    PubMed  CAS  Google Scholar 

  31. Lake B. G. (1995): Mechanisms of hepatocarcinogenicity of peroxisome-proliferating drugs and chemicals. Ann. Rev. Pharmacol. Toxicol., 35, 483–507.

    Article  CAS  Google Scholar 

  32. Cajacob C. A., Ortiz de Montellano P.R. (1986): Mechanism-based in vivo inactivation of lauric acid hydroxylases. Biochemistry, 25, 4705–4711.

    Article  PubMed  CAS  Google Scholar 

  33. Helvig C., Alayrac C., Mioskowski C., Koop D., Poullain D., Durst F., Salaün J.-P. (1997): Suicide inactivation of cytochrome P450 by midchain and terminal acetylenes: a mechanistic study of inactivation of a plant lauric acid omega-hydroxylase. J. Biol. Chem., 272, 414–421.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. CNRS-UPR 406, Département d’Enzymologie Cellulaire et Moléculaire, Institut de Biologie Moléculaire des Plantes, Strasbourg, France

    N. Forthoffer, C. Helvig, I. Benveniste & J. -P. Salaün

  2. Waite Institute, Department of Crop Protection, University of Adelaide, Adelaide, Australia

    N. Dillon

  3. Department of Biotransformation, Novartis Pharma AG., Basel, Switzerland

    A. Zimmerlin

  4. Department of Crop Science, University of Guelph, Guelph, Ontario, Canada

    F. Tardif

Authors
  1. N. Forthoffer
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  2. C. Helvig
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  3. N. Dillon
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  4. I. Benveniste
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  5. A. Zimmerlin
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  6. F. Tardif
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  7. J. -P. Salaün
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Forthoffer, N., Helvig, C., Dillon, N. et al. Induction and inactivation of a cytochrome P450 confering herbicide resistance in wheat seedlings. Eur. J. Drug Metab. Pharmacokinet. 26, 9–16 (2001). https://doi.org/10.1007/BF03190370

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  • DOI: https://doi.org/10.1007/BF03190370

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