Hostname: page-component-7b7567c8c-fvjsw Total loading time: 0 Render date: 2026-11-15T10:47:38.841Z Has data issue: false hasContentIssue false
  • English
  • Français

Protoporphyrinogen Oxidase-Inhibiting Herbicides

Published online by Cambridge University Press:  12 June 2017

Stephen O. Duke,
John Lydon,
José M. Becerril,
Timothy D. Sherman,
Larry P. Lehnen Jr. and
Hiroshi Matsumoto
Stephen O. Duke
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
John Lydon
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
José M. Becerril
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
Timothy D. Sherman
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
Larry P. Lehnen Jr.
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
Hiroshi Matsumoto
Affiliation:
USDA, Agric. Res. Serv., Southern Weed Sci. Lab., P.O. Box 350, Stoneville, MS 38776
Get accessRights & Permissions [Opens in a new window]

Abstract

Several commercial and experimental herbicides such as p-nitrodiphenyl ethers, oxadiazoles, and cyclic imides inhibit protoporphyrinogen IX oxidase (Protox), the enzyme that converts protoporphyrinogen IX to protoporphyrin IX (Proto). This leads to uncontrolled autooxidation of the substrate and results in accumulation of Proto. Blockage of the porphyrin pathway at this site inhibits synthesis of both chlorophylls and heme. Heme is a feedback regulator of the porphyrin pathway. Thus, inhibition of Protox also deregulates the pathway, causing increased carbon flow to the accumulating pool of Proto. Proto is a potent photosensitizer that generates high levels of singlet oxygen in the presence of molecular oxygen and light. In plants treated with these herbicides, damage is light dependent and closely correlated with the level of Proto that accumulates. Proto accumulation is apparently largely extraplastidic, resulting in rapid photodynamic damage to the plasmalemma and tonoplast. After high levels of Proto accumulate in response to these herbicides, protochlorophyllide (PChlide) levels can increase also; however, Proto appears to be the primary photodynamic pigment responsible for the herbicidal activity.

Keywords

Acifluorfenchlorophyll synthesisoxadiazonperoxidizing herbicidesphotobleaching herbicidesporphyrin synthesisprotoporphyrin IX

Information

Type
Special Topics
Information
Weed Science , Volume 39 , Issue 3 , September 1991, pp. 465 - 473
Copyright
Copyright © 1991 by the Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Literature Cited

1. Becerril, J. M. and Duke, S. O. 1989. Protoporphyrin DC content correlates with activity of photobleaching herbicides. Plant Physiol. 90:1175–1181.CrossRefGoogle Scholar
2. Becerril, J. M. and Duke, S. O. 1989. Acifluorfen effects on intermediates of chlorophyll synthesis in green cucumber cotyledon tissues. Pestic. Biochem. Physiol. 35:119–126.Google Scholar
3. Böger, P. 1984. Multiple modes of action of diphenyl ethers. Z. Naturforsch. 39C:468–475.Google Scholar
4. Bowyer, J. R., Hallahan, B. J., Camilleri, P., and Howard, J. 1989. Mode of action studies on nitrodiphenyl ether herbicides, II. The role of photosynthetic electron transport in Scenedesmus obliquus . Plant Physiol. 89:674–680.CrossRefGoogle ScholarPubMed
5. Brenner, D. A. and Bloomer, J. R. 1980. Enzymatic defect in variegate porphyria — studies with human cultured skin fibroblasts. N. Engl. J. Med. 302:765–769.CrossRefGoogle ScholarPubMed
6. Camadro, J. M., Urban-Grimal, D., and Labbe, P. 1982. A new assay of protoporphyrinogen oxidase: Evidence for a total deficiency in that activity in a heme-less mutant of Saccharomyces cerevisiae . Biochem. Biophys. Res. Commun. 106:724–730.CrossRefGoogle Scholar
7. Castelfranco, P. A. and Beale, S. I. 1983. Chlorophyll biosynthesis: Recent advances and areas of interest. Annu. Rev. Plant Physiol. 34:241–278.CrossRefGoogle Scholar
8. Derrick, P. M., Cobb, A. H., and Pallett, K. E. 1988. Ultrastructural effects of the diphenyl ether herbicide acifluorfen and the experimental herbicide M&B 39279. Pestic. Biochem. Physiol. 32:153–163.Google Scholar
9. Deybach, J. C., de Verneuil, H., and Nordmann, Y. 1981. The inherited enzymatic defect in porphyria variegate. Hum. Genet. 58:425–428.Google Scholar
10. Duke, S. O., Becerril, J. M., Matsumoto, H., and Sherman, T. D. 1991. Photosensitizing porphyrins as herbicides. Am. Chem. Soc. Symp. Ser. 449:371–386.Google Scholar
11. Duke, S. O. and Kenyon, W. H. 1986. Photosynthesis is not involved in the mechanism of action of acifluorfen in cucumber (Cucumis sativus L.). Plant Physiol. 81:882–888.Google Scholar
12. Duke, S. O. and Kenyon, W. H. 1987. A non-metabolic model of acifluorfen activity. Z. Naturforsch. 42C:813–818.CrossRefGoogle Scholar
13. Duke, S. O., Lydon, J., Paul, R. N. 1989. Oxadiazon activity is similar to that of p-nitro-diphenyl ether herbicides. Weed Sci. 37:152–160.Google Scholar
14. Duke, S. O., Vaughn, K. C., and Meeusen, R. L. 1984. Mitochondrial involvement in the mode of action of acifluorfen. Pestic. Biochem. Physiol. 21:368–376.Google Scholar
15. Ensminger, M. P. and Hess, F. D. 1985. Action spectrum of the activity of acifluorfen-methyl, a diphenyl ether herbicide, in Chlamydomonas eugametos . Plant Physiol. 77:503–505.Google Scholar
16. Ensminger, M. P. and Hess, F. D. 1985. Photosynthesis involvement in the mechanism of action of diphenyl ether herbicides. Plant Physiol. 78:46–50.CrossRefGoogle ScholarPubMed
17. Ensminger, M. P., Hess, F. D., and Bahr, J. T. 1985. Nitro free radical formation of diphenyl ether herbicides is not necessary for their toxic action. Pestic. Biochem. Physiol. 23:163–170.Google Scholar
18. Fadayomi, O. and Warren, G. F. 1976. The light requirement for herbicidal activity of diphenyl ethers. Weed Sci. 24:598–600.CrossRefGoogle Scholar
19. Ferreira, G. C., Andrew, T. L., Karr, S. W., and Dailey, H. A. 1988. Organization of the terminal enzymes of the heme biosynthetic pathway. J. Biol. Chem. 263:3835–3839.CrossRefGoogle ScholarPubMed
20. Finckh, B. F. and Kunert, K. J. 1985. Vitamins C and E: An antioxidative system against herbicide-induced lipid peroxidation in higher plants. J. Agric. Food Sci. 33:574–577.Google Scholar
21. Rear, D. S., Swanson, H. R., and Mansager, E. R. 1983. Acifluorfen metabolism in soybean: diphenylether bond cleavage and the formation of homoglutathione, cysteine, and glucose conjugates. Pestic. Biochem. Physiol. 20:299–310.Google Scholar
22. Gaba, V., Cohen, N., Shaaltiel, Y., Ben-Amotz, A., and Gressel, J. 1988. Light-requiring acifluorfen action in the absence of bulk photosynthetic pigments. Pestic. Biochem. Physiol. 31:1–12.Google Scholar
23. Gassman, M. A. 1973. The conversion of photoinactive protochlorophyllide663 to phototransformable protochlorophyllide650 in etiolated bean leaves treated with δ-aminolevulinic acid. Plant Physiol. 52:590–594.Google Scholar
24. Halling, B. P. and Peters, G. R. 1987. Influence of chloroplast development on the activation of the diphenyl ether herbicide acifluorfen-methyl. Plant Physiol. 84:1114–1120.CrossRefGoogle ScholarPubMed
25. Haworth, P. and Hess, F. D. 1988. The generation of singlet oxygen (IO2) by the nitro-diphenyl ether herbicide oxyfluorfen is independent of photosynthesis. Plant Physiol. 86:672–676.CrossRefGoogle Scholar
26. Jacobs, J. M. and Jacobs, N. J. 1987. Oxidation of protoporphyrinogen to protoporphyrin, a step in chlorophyll and haem biosynthesis. Purification and partial characterization of the enzyme from barley organelles. Biochem. J. 244:219–224.Google Scholar
27. Kenyon, W. H. and Duke, S. O. 1985. Effects of acifluorfen on endogenous antioxidants and protective enzymes in cucumber (Cucumis sativus L.) cotyledons. Plant Physiol. 79:862–866.Google Scholar
28. Kenyon, W. H., Duke, S. O., and Paul, R. N. 1988. Effects of temperature on the activity of the p-nitrosubstituted diphenyl ether herbicide acifluorfen in cucumber (Cucumis sativus L.). Pestic. Biochem. Physiol. 30:57–66.Google Scholar
29. Kenyon, W. H., Duke, S. O., and Vaughn, K. C. 1985. Sequence of herbicidal effects of acifluorfen on ultrastructure and physiology of cucumber cotyledons. Pestic. Biochem. Physiol. 24:240–250.Google Scholar
30. Kouji, H., Masuda, T., and Matsunaka, S. 1988. Action mechanism of diphenyl ether herbicides: Light-dependent O2 consumption in diphenyl ether-treated tobacco cell homogenate. J. Pestic. Sci. 13:495–499.Google Scholar
31. Kouji, H., Masuda, T., and Matsunaka, S. 1989. Action mechanism of diphenyl ether herbicides: Stimulation of ALA synthesizing activities. Pestic. Biochem. Physiol. 33:230–238.CrossRefGoogle Scholar
32. Kunert, K. J., Sandmann, G., and Böger, P. 1987. Modes of action of diphenyl ethers. Rev. Weed Sci. 3:35–55.Google Scholar
33. Lehnen, L. P., Sherman, T. D., Becerril, J. M., and Duke, S. O. 1990. Tissue and cell localization of acifluorfen-induced porphyrins in cucumber cotyledons. Pestic. Biochem. Physiol. 37:239–298.CrossRefGoogle Scholar
34. Lydon, J. and Duke, S. O. 1988. Porphyrin synthesis is required for photobleaching activity of the p-nitrosubstituted diphenyl ether herbicides. Pestic. Biochem. Physiol. 31:74–83.Google Scholar
35. Mascia, P. N. and Robertson, D. S. 1978. Studies of chloroplast development in four maize mutants defective in chlorophyll biosynthesis. Planta 143:207–211.CrossRefGoogle ScholarPubMed
36. Masuda, T., Kouji, H., and Matsunaka, S. 1990. Diphenyl ether herbicide-decreased heme contents stimulate 5-aminolevulinic acid synthesis. Pestic. Biochem. Physiol. 36:106–114.CrossRefGoogle Scholar
37. Matringe, M. and Scalla, R. 1987. Photoreceptors and respiratory electron flow involvement in the activity of acifluorfen-methyl and LS 82–556 on nonchlorophyllous soybean cells. Pestic. Biochem. Physiol. 27:267–274.Google Scholar
38. Matringe, M. and Scalla, R. 1987. Induction of tetrapyrroles by diphenylether-type herbicides. Proc. Br. Crop Prot. Conf. 9B:981–988.Google Scholar
39. Matringe, M. and Scalla, R. 1988. Studies on the mode of action of acifluorfen-methyl in non-chlorophyllous soybean cells: Accumulation of tetrapyrroles. Plant Physiol. 86:619–622.CrossRefGoogle Scholar
40. Matringe, M. and Scalla, R. 1988. Effects of acifluorfen-methyl on cucumber cotyledons: Protoporhyrin accumulation. Pestic. Biochem. Physiol. 32:164–172.Google Scholar
41. Matringe, M., Camadro, J.-M., Labbe, P., and Scalla, R. 1989. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem. J. 260:231–235.Google Scholar
42. Matringe, M., Camadro, J.-M., Labbe, P., and Scalla, P. 1989. Protoporphyrinogen oxidase inhibition by three peroxidizing herbicides: oxadiazon, LS 82–556 and M&B 39279. FEBS Lett. 245:35–38.Google Scholar
43. Matsunaka, S. 1969. Acceptor of light energy in photoactivation of diphenylether herbicides. J. Agric. Food Sci. 17:171–5.Google Scholar
44. Matsunaka, S. 1976. Diphenyl ethers. Pages 709–739 in Kearney, P. C. and Kaufman, D. D., eds. Herbicides: Chemistry, Degradation, and Mode of Action. Vol. 2. Marcel-Dekker, New York.Google Scholar
45. Méallier, P., Emmelin, C., Périchet, G., and Tissut, M. 1989. Photodependent generation of reactive oxygen species by a phytotoxic pyridine derivative. Chemosphere 19:1427–1434.CrossRefGoogle Scholar
46. Nicolaus, B., Sandmann, G., Watanabe, G., Wakabayashi, K., and Böger, P. 1989. Herbicide-induced peroxidation: Influence of light and diuron on protoporphyrin DC formation. Pestic. Biochem. Physiol. 35:192–210.CrossRefGoogle Scholar
47. Nurit, F., Ravanel, P., and Tissut, M. 1988. The photodependent effect of LS 82556 and acifluorfen in cucumber cotyledon pieces: The possible indirect involvement of photosynthesis. Pestic. Biochem. Physiol. 31:67–73.Google Scholar
48. Orr, G. L., Elliott, C. M., and Hogan, M. E. 1983. Activity in vivo and redox sites in vitro of nitro- and chlorodiphenyl ether herbicide analogs. Plant Physiol. 73:939–944.CrossRefGoogle Scholar
49. Orr, G. L. and Hess, F. D. 1982. Mechanism of action of the diphenyl ether herbicide acifluorfen-methyl in excised cucumber (Cucumis sativus L.) cotyledons. Plant Physiol 69:502–507.Google Scholar
50. Rao, D.N.R. and Mason, R. P. 1988. Photoreduction of some nitrobiphenyl ether herbicides to nitro radical anions by δ-carotene and related compounds. Photochem. Photobiol. 47:791–795.Google Scholar
51. Rebeiz, C. A., Montazer-Zouhoor, A., Hopen, H. J., and Wu, S. -M. 1984. Photodynamic herbicides: 1. Concept and phenomenology. Enzyme Microb. Technol. 5:390–401.Google Scholar
52. Rebeiz, C. A., Montazer-Zouhoor, A., Mayasich, J. M., Tripathy, B. C., Wu, S.-M., and Rebeiz, C. C. 1987. Photodynamic herbicides and chlorophyll biosynthesis modulators. Am. Chem. Soc. Symp. Ser. 339:295–328.Google Scholar
53. Rebeiz, C. A., Montazer-Zouhoor, A., Mayasich, J. M., Tripathy, B. C., Wu, S. -M., and Rebeiz, C. C. 1988. Phytodynamic herbicides. Recent developments and molecular basis of selectivity. CRC Crit. Rev. Plant Sci. 6:385–436.Google Scholar
54. Sandmann, G. and Böger, P. 1988. Accumulation of protoporphyrin DC in the presence of peroxidizing herbicides. Z. Naturforsch. 43C:699–704.Google Scholar
55. Sandmann, G. and Böger, P. 1990. Peroxidizing herbicides. Some aspects of tolerance. Am. Chem. Soc. Symp. Ser. 421:407–418.Google Scholar
56. Sandmann, G., Reck, H., and Böger, P. 1984. Herbicidal mode of action on chlorophyll formation. J. Agric. Food Chem. 32:868–872.Google Scholar
57. Sato, R., Nagano, E., Oshio, H., Kamoshita, K., and Furuya, M. 1987. Wavelength effect on the action of a N-phenylimide S-23142 and a diphenylether acifluorfen-ethyl in cotyledons of cucumber (Cucumis sativus L.) seedlings. Plant Physiol. 85:1146–1150.Google Scholar
58. Sato, R., Nagano, E., Oshio, H., and Kamoshita, K. 1988. Activities of the N-phenyl imide S-23142 in carotenoid-deficient seedlings of rice and cucumber. Pestic. Biochem. Physiol. 31:213–220.Google Scholar
59. Shaaltiel, Y., Glazer, A., Bocion, P. F., and Gressel, J. 1988. Cross tolerance to herbicidal and environmental oxidants of plant biotypes tolerant to paraquat, sulfur dioxide, and ozone. Pestic. Biochem. Physiol. 31:13–23.Google Scholar
60. Tanielian, C. and Wolff, C. 1988. Mechanism of physical quenching of singlet molecular oxygen by chlorophylls and related compounds of biological interest. Photochem. Photobiol. 48:277–280.Google Scholar
61. Teraoka, T., Sandmann, G., Böger, P., and Wakabayashi, K. 1987. Effect of cyclic imide herbicides on pigment formation in plants. J. Pestic. Sci. 12:499–504.CrossRefGoogle Scholar
62. Towers, G.H.N. and Arnason, J. T., Arnason, J. T. 1988. Photodynamic herbicides. Weed Technol. 2:545–549.Google Scholar
63. Wakabayashi, K., Matsuya, K., Teraoka, T., Sandmann, G., and Böger, P. 1986. Effect of cyclic imide herbicides on chlorophyll formation in higher plants. J. Pestic. Sci. 11:635–640.Google Scholar
64. Wakabayashi, K., Sandmann, G., Ohta, H., and Böger, P. 1988. Peroxidizing herbicides: Comparison of dark and light effect. J. Pestic. Sci. 13:461–471.Google Scholar
65. Wickliff, J. L., Duke, S. O., and Vaughn, K. C. 1982. Involvement of photobleaching and inhibition of protochlorophyll(ide) accumulation in tentoxin effects on greening mung bean seedlings. Physiol. Plant. 56:399–406.Google Scholar
66. Witkowski, D. A. and Hailing, B. P. 1988. Accumulation of photodynamic tetrapyrroles induced by acifluorfen-methyl. Plant Physiol. 87:632–637.Google Scholar
67. Witkowski, D. A. and Hailing, B. P. 1989. Inhibition of plant protoporphyrinogen oxidase by the herbicide acifluorfen-methyl. Plant Physiol. 90:1239–1242.Google Scholar
68. Yanase, D. and Andoh, A. 1989. Porphyrin synthesis involvement in diphenyl ether-like mode of action of TNPP-ethyl, a novel phenylpyrazole herbicide. Pestic. Biochem. Physiol. 35:70–80.Google Scholar