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. 1992 Nov;100(3):1211–1216. doi: 10.1104/pp.100.3.1211

Mode of Action Studies on a Chiral Diphenyl Ether Peroxidizing Herbicide

Correlation between Differential Inhibition of Protoporphyrinogen IX Oxidase Activity and Induction of Tetrapyrrole Accumulation by the Enantiomers

Beverly J Hallahan 1,2,3,1,2, Patrick Camilleri 1,2,3,3, Alison Smith 1,2,3, John R Bowyer 1,2,3
PMCID: PMC1075768  PMID: 16653107

Abstract

The nitrodiphenyl ether herbicide 5-[2-chloro-4-(trifluoromethyl)phenoxy]-2-nitroacetophenone oxime-O-(acetic acid, methyl ester) (DPEI) induced an abnormal accumulation of protoporphyrin IX in darkness in the green alga Chlamydomonas reinhardtii, as determined by high-performance liquid chromatography and spectrofluorimetry. It also inhibited the increase in cell density of the alga in light-grown cultures with an I50 (concentration required to decrease cell density increase to 50% of the noninhibited control value) of 0.16 μm. The relative ability of four peroxidizing diphenyl ether herbicides to cause tetrapyrrole accumulation in C. reinhardtii correlated qualitatively with their ability to inhibit the increase in cell density in light-grown cultures. The purified S(−) enantiomer of the optically active phthalide DPE 5-[2-chloro-4-(trifluoromethyl)phenoxy]-3-methylphthalide (DPEIII), which has greater herbicidal activity than the R(+) isomer, induces a 4- to 5-fold greater tetrapyrrole accumulation than the R(+) isomer. The I50 for inhibition of increase in cell density in light-grown cultures of C. reinhardtii by the S(−) isomer (0.019 μm) is less than 25% of that for the R(+) isomer. DPEIII inhibits protoporphyrinogen IX oxidase activity in pea (Pisum sativum) etioplast lysates, with the S(−) enantiomer showing considerably greater potency than the R(+) isomer and the racemic mixture showing a potency intermediate between the two. The results indicate that the site at which DPEs inhibit protoporphyrinogen IX oxidase shows chiral discrimination and provide further evidence for the link between inhibition of this enzyme, protoporphyrin IX accumulation, and the phytotoxicity of DPE herbicides.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bowyer J. R., Hallahan B. J., Camilleri P., Howard J. Mode of Action Studies on Nitrodiphenyl Ether Herbicides : II. The Role of Photosynthetic Electron Transport in Scenedesmus obliquus. Plant Physiol. 1989 Feb;89(2):674–680. doi: 10.1104/pp.89.2.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Drayer D. E. Pharmacodynamic and pharmacokinetic differences between drug enantiomers in humans: an overview. Clin Pharmacol Ther. 1986 Aug;40(2):125–133. doi: 10.1038/clpt.1986.150. [DOI] [PubMed] [Google Scholar]
  3. Ensminger M. P., Hess F. D. Action Spectrum of the Activity of Acifluorfen-methyl, a Diphenyl Ether Herbicide, in Chlamydomonas eugametos. Plant Physiol. 1985 Feb;77(2):503–505. doi: 10.1104/pp.77.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fuesler T. P., Hanamoto C. M., Castelfranco P. A. Separation of Mg-Protoporphyrin IX and Mg-Protoporphyrin IX Monomethyl Ester Synthesized de novo by Developing Cucumber Etioplasts. Plant Physiol. 1982 Feb;69(2):421–423. doi: 10.1104/pp.69.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gorman D. S., Levine R. P. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1665–1669. doi: 10.1073/pnas.54.6.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Jacobs J. M., Jacobs N. J., Borotz S. E., Guerinot M. L. Effects of the photobleaching herbicide, acifluorfen-methyl, on protoporphyrinogen oxidation in barley organelles, soybean root mitochondria, soybean root nodules, and bacteria. Arch Biochem Biophys. 1990 Aug 1;280(2):369–375. doi: 10.1016/0003-9861(90)90344-x. [DOI] [PubMed] [Google Scholar]
  7. Jacobs J. M., Jacobs N. J., Sherman T. D., Duke S. O. Effect of diphenyl ether herbicides on oxidation of protoporphyrinogen to protoporphyrin in organellar and plasma membrane enriched fractions of barley. Plant Physiol. 1991 Sep;97(1):197–203. doi: 10.1104/pp.97.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jacobs N. J., Jacobs J. M. Assay for enzymatic protoporphyrinogen oxidation, a late step in heme synthesis. Enzyme. 1982;28(2-3):206–219. doi: 10.1159/000459103. [DOI] [PubMed] [Google Scholar]
  9. Labbe P., Camadro J. M., Chambon H. Fluorometric assays for coproporphyrinogen oxidase and protoporphyrinogen oxidase. Anal Biochem. 1985 Aug 15;149(1):248–260. doi: 10.1016/0003-2697(85)90502-0. [DOI] [PubMed] [Google Scholar]
  10. Matringe M., Camadro J. M., Labbe P., Scalla R. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem J. 1989 May 15;260(1):231–235. doi: 10.1042/bj2600231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Matringe M., Camadro J. M., Labbe P., Scalla R. Protoporphyrinogen oxidase inhibition by three peroxidizing herbicides: oxadiazon, LS 82-556 and M&B 39279. FEBS Lett. 1989 Mar 13;245(1-2):35–38. doi: 10.1016/0014-5793(89)80186-3. [DOI] [PubMed] [Google Scholar]
  12. Matringe M., Scalla R. Studies on the mode of action of acifluorfen-methyl in nonchlorophyllous soybean cells : accumulation of tetrapyrroles. Plant Physiol. 1988 Feb;86(2):619–622. doi: 10.1104/pp.86.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Rebeiz C. A., Mattheis J. R., Smith B. B., Rebeiz C., Dayton D. F. Chloroplast biogenesis. Biosynthesis and accumulation of Mg-protoprophyrin IX monoester and longer wavelength metalloporphyrins by greening cotyledons. Arch Biochem Biophys. 1975 Feb;166(2):446–465. doi: 10.1016/0003-9861(75)90408-7. [DOI] [PubMed] [Google Scholar]
  14. Sherman T. D., Becerril J. M., Matsumoto H., Duke M. V., Jacobs J. M., Jacobs N. J., Duke S. O. Physiological basis for differential sensitivities of plant species to protoporphyrinogen oxidase-inhibiting herbicides. Plant Physiol. 1991 Sep;97(1):280–287. doi: 10.1104/pp.97.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Varsano R., Matringe M., Magnin N., Mornet R., Scalla R. Competitive interaction of three peroxidizing herbicides with the binding of [3H]acifluorfen to corn etioplast membranes. FEBS Lett. 1990 Oct 15;272(1-2):106–108. doi: 10.1016/0014-5793(90)80459-v. [DOI] [PubMed] [Google Scholar]
  16. Walker K. A., Ridley S. M., Harwood J. L. Effects of the selective herbicide fluazifop on fatty acid synthesis in pea (Pisum sativum) and barley (Hordeum vulgare). Biochem J. 1988 Sep 15;254(3):811–817. doi: 10.1042/bj2540811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Witkowski D. A., Halling B. P. Accumulation of photodynamic tetrapyrroles induced by acifluorfen-methyl. Plant Physiol. 1988 Jul;87(3):632–637. doi: 10.1104/pp.87.3.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Witkowski D. A., Halling B. P. Inhibition of plant protoporphyrinogen oxidase by the herbicide acifluorfen-methyl. Plant Physiol. 1989 Aug;90(4):1239–1242. doi: 10.1104/pp.90.4.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]

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