Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-28T03:10:35.919Z Has data issue: false hasContentIssue false

Recovery of Transmembrane Potentials in Plants Resistant to Aryloxyphenoxypropanoate Herbicides: A Phenomenon Awaiting Explanation

Published online by Cambridge University Press:  12 June 2017

Joseph A. M. Holtum
Affiliation:
Dep. Bot., James Cook Univ., Townsville 4811, Qld. Australia
Rainer E. Häusler
Affiliation:
Univ. Sheffield, U.K.
Malcolm D. Devine
Affiliation:
Dep. Crop Sci. & Plant Ecol., Univ. Sasketchewan, Saskatoon, S7N 0W0 Canada
Stephen B. Powles
Affiliation:
Dep. Crop Prot., Waite Campus, Adelaide 5064, S.A. Australia

Abstract

Aryloxyphenoxypropanoate (APP) herbicides, such as diclofop, depolarize membranes in parenchyma cells of coleoptiles and root tips, and isolated tonoplast or plasma membrane vesicles from a variety of plant species. Some APP-resistant biotypes of rigid ryegrass and wild oat repolarize membranes after removal of herbicide from a bathing medium. The repolarization ability does not require presence of either APP-insensitive acetyl coenzyme A carboxylase or an increased capacity for herbicide detoxification. The kinetics of depolarization and repolarization depend upon the herbicide, the herbicide concentration, the biotype, and the pH of the bathing solution. For rigid ryegrass, depolarization in the presence of diclofop acid is more rapid than in the presence of diclofop-methyl, and 50% depolarization required about 4 μM diclofop acid. Both the nonherbicidal S(–) and the herbicidal R(+) enantiomers of diclofop acid depolarized membranes in susceptible and resistant ryegrass. Susceptible biotypes regenerated transmembrane potentials following removal of the S(–) but not the R(+) enantiomer, whereas resistant biotypes repolarized following exposure to either enantiomer or a mixture of the two. The herbicide 2,4-D affected, in a complex manner, the ability of both susceptible and resistant ryegrass biotypes to depolarize and repolarize. It is postulated that the intracellular concentration of diclofop acid in susceptible and resistant plants is not the same due to differences in the partitioning of diclofop acid between the extracellular spaces and the cytoplasm. The mechanism producing the postulated difference is unknown, but observations on the proton extrusion capacity of both ryegrass and wild oats, the responses of ryegrass to [K+] and PCMBS, and the single-gene inheritance pattern of resistance in wild oats indicate that changes in the diclofop sensitivity of a plasma membrane protein involved in the generation of proton or ion gradients may be involved.

Type
Special Topics
Copyright
Copyright © 1994 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.)

References

Literature Cited

1. Banas, A., Johansson, J., Stenlid, C. T., and Stymne, S. 1990. Flavonoids, pyridazinones and salicylic acid counteract the effects of haloxyfop and alloxydim. Pages 407409 in Proc. Int. Symp. Plant Lipids (9th), Plant Lipid Biochem., Struct. Util. Quinn, P. J. and Harwood, J. L., eds. Portland Press, London, UK.Google Scholar
2. Burnet, M. W. M., Hildebrand, O. B., Holtum, J. A. M., and Powles, S. B. 1991. Amitrole, triazine, substituted urea and metribuzin resistance in a biotype of rigid ryegrass. Weed Sci. 39:317323.Google Scholar
3. Burnet, M. W. M. 1992. Mechanisms of herbicide resistance in Lolium rigidum. Ph.D. Diss., Univ. Adelaide.Google Scholar
4. Burton, J. D., Gronwald, J. W., Somers, D. A., Connelly, J. A., Gengenbach, B. G., and Wyse, D. L., 1987. Inhibition of plant acetyl-coenzyme A carboxylase by the herbicides sethoxydim and haloxyfop. Biochem. Biophys. Res. Commun. 148:10391044.Google Scholar
5. Cho, H.-Y., Widholme, J. M., and Slife, F. W. 1988. Haloxyfop inhibition of the pyruvate and α-ketoglutarate dehydrogenase complexes of corn (Zea mays L.) and soybean (Glycine max [L.] Merr.). Plant Physiol. 87:334340.Google Scholar
6. Christopher, J. T., Powles, S. B., and Holtum, J. A. M. 1992. Resistance to acetolactate synthase herbicides in annual ryegrass (Lolium rigidum) involves at least two mechanisms. Plant Physiol. 100:10901913.Google Scholar
7. Conte-Camarino, D., Mambrini, M., DeLuca, A., Tricarico, D., Bryant, S. H., Tortorella, V., and Bettoni, G. 1988. Enantiomers of clofibric acid and analogs have opposite actions on rat skeletal muscle chloride channels. Pflüegers Arch. 413:105107.Google Scholar
8. Devine, M. D., Hall, J. C., Romano, M. L., Maries, M. A. S., Thomson, L. W., and Shimabukuro, R. H. 1993. Diclofop and fenoxaprop resistance in wild oat is associated with an altered effect on the plasma membrane electrogenic potential. Pestic. Biochem. Physiol. 45:167177.Google Scholar
9. Devine, M. D., MacIsaac, S. A., Romano, M. L., and Hall, J. C. 1992. Investigation of the mechanism of diclofop resistance in two biotypes of Avena fatua . Pestic. Biochem. Physiol. 42:8896.Google Scholar
10. Devine, M. D., Sasata, R., and Renault, S. 1993. An analysis on the effect of diclofop on “resistant” membranes. Abstr. Weed Sci. Soc. Am. 33:63.Google Scholar
10. DiTomaso, J. M. 1993. Evidence against a direct membrane effect in the mechanism of action of graminicides. Weed Sci. 41:(this issue).Google Scholar
11. DiTomaso, J. M., Brown, P. H., Stowe, A. E., Linscott, D. L., and Kochian, L. V. 1991. Effects of diclofop and diclofop-methyl on membrane potentials in roots of intact oat, maize, and pea seedlings. Plant Physiol. 95:10631069.Google Scholar
12. Gronwald, J. W. 1991. Lipid biosynthesis inhibitors. Weed Sci. 39:435449.Google Scholar
13. Hausler, R. E., Holtum, J. A. M., and Powles, S. B. 1991. Cross-resistance to herbicides in annual ryegrass (Lolium rigidum). IV. Correlation between membrane effects and resistance to graminicides. Plant Physiol. 97:10341043.Google Scholar
14. Heap, I. M. and Knight, R. 1986. The occurrence of herbicide cross-resistance in a population of annual ryegrass, Lolium rigidum, resistant to diclofop-methyl. Aust. J. Agric. Res. 37:149156.Google Scholar
15. Heap, I. M., Murray, B. G., Loeppky, H. A., and Morrison, I. N. 1993. Resistance to aryloxyphenoxypropionate and cyclohexanedione herbicides in wild oat (Avena fatua). Weed Sci. 41:232238.Google Scholar
16. Heap, J. and Knight, R. 1982. A population of ryegrass tolerant to the herbicide diclofop-methyl. J. Aust. Inst. Agric. Sci. 48:156157.Google Scholar
17. Holtum, J. A. M., Matthews, J. M., Häusler, R. E., Liljegren, D. R., and Powles, S. B. 1991. Cross-resistance to herbicides in annual ryegrass (Lolium rigidum. III. On the mechanism of resistance to diclofop-methyl. Plant Physiol. 97:10261034.Google Scholar
18. Lucas, W. J., Wilson, C., and Wright, J. P. 1984. Perturbation off Chara plasmalemma transport function by 2[4(2′,4′-dichlorophenoxy)phenoxy]propionic acid. Plant Physiol. 74:6166.Google Scholar
19. Mansooji, A. M., Holtum, J. A. M., Boutsalis, P., Matthews, J. M., and Powles, S. B. 1992. Resistance to aryloxyphenoxypropionate herbicides in two wild oat species (Avena fatua and Avena sterilis ssp. ludoviciana). Weed Sci. 40:599605.Google Scholar
20. Matthews, J. M., Holtum, J. A. M., Liljegren, D. R., Furness, B., and Powles, S. B. 1990. Cross-resistance to herbicides in annual ryegrass (Lolium rigidum). l. Properties of the herbicide target enzymes acetyl-co-enzyme a carboxylase and acetolactate synthase. Plant Physiol. 94:11801186.Google Scholar
21. Morrison, I. N., Heap, I. M., and Murray, B. 1992. Herbicide resistance in wild oat—the Canadian perspective. In Proc. Fourth Int. Oat Conf. Adelaide, Australia.Google Scholar
22. Ratterman, D. M. and Balke, N. E. 1989. Diclofop-methyl increases the proton permeability of isolated oat root tonoplast. Plant Physiol. 91:756765.Google Scholar
23. Ratterman, D. M. and Balke, N. E. 1988. Herbicide disruption of proton gradient development and maintenance in plasmalemma and tonoplast vesicles from oat root. Pestic. Biochem. Physiol. 31:221236.Google Scholar
24. Secor, J. and Cséke, C. 1988. Inhibition of acetyl-coA carboxylase activity by haloxyfop and tralkoxydim. Plant Physiol. 86:1012.Google Scholar
25. Shimabukuro, M. A., Shimabukuro, R. H., and Walsh, W. C. 1982. The antagonism of IAA-induced hydrogen ion extrusion and coleoptile growth by diclofop-methyl. Physiol. Plant. 56:444452.Google Scholar
26. Shimabukuro, R. H. 1990. Selectivity and mode of action of the postemergence herbicide diclofop-methyl. Plant Growth Reg. Soc. Am. Quart. 18:3754.Google Scholar
27. Shimabukuro, R. H. and Hoffer, B. L. 1992. Effect of diclofop on the membrane potentials of herbicide-resistant and -susceptible annual ryegrass root tips. Plant Physiol. 98:14151422.Google Scholar
28. Shimabukuro, R. H. and Hoffer, B. L. 1991. Metabolism of diclofop-methyl in susceptible and resistant biotypes of Lolium rigidum . Pestic. Biochem. Physiol. 39:251260.Google Scholar
29. Shimabukuro, R. H. and Hoffer, B. L. 1990. Perturbation of transmembrane proton -gradient and inhibition of fatty acid metabolism: their roles in the mechanism of action of diclofop-methyl. Weed Sci. Soc. Am. Abstr. No. 176.Google Scholar
30. Shimabukuro, R. H., Walsh, W. C., and Wright, J. P. 1989. Effect of diclofop-methyl and 2,4-D on transmembrane proton gradients: a mechanism for their antagonistic interaction. Physiol. Plant. 77:107114.Google Scholar
31. Weber, A. and Lüttge, U. 1988. The effects of the herbicide sethoxydim on transport processes in sensitive and tolerant grass species. II. Effects on membrane-bound redox systems in plant cells. Z. Naturforsch. 43c:257263.Google Scholar
32. Weber, A., Fischer, E., von Branitz, H. S., and Lüttge, U. 1988. The effects of the herbicide sethoxydim on transport processes in sensitive and tolerant grass species I. Effects on the electrical membrane potential and alanine uptake. Z. Natürforsch. 43c:249256.Google Scholar
33. Wright, J. P. 1993. Use of membrane potential measurements to study mode of action of diclofop-methyl. Weed Sci. 41:(this issue).Google Scholar
34. Wright, J. P. and Shimabukuro, R. H. 1987. Effects of diclofop and diclofop-methyl on the membrane potentials of wheat and oat coleoptiles. Plant Physiol. 85:188193.Google Scholar