Skip to main content Accessibility help
×
Home

Herbicide Resistance Endowed by Enhanced Rates of Herbicide Metabolism in Wild Oat (Avena spp.)

  • M. S. Ahmad-Hamdani (a1), Qin Yu (a1), Heping Han (a1), Gregory R. Cawthray (a1), Shao F. Wang (a2) and Stephen B. Powles (a1)...

Abstract

The biochemical basis of resistance to the acetyl-coenzyme A carboxylase (ACCase)-inhibiting herbicide diclofop-methyl was investigated in a resistant wild oat population (R1), which does not exhibit a resistant ACCase. Rates of foliar uptake and translocation of [14C]-diclofop were the same in the R1 vs. susceptible (S) populations. However, the level of phytotoxic diclofop acid was always found to be lower in the R1 vs. S plants, with a concomitant higher level (up to 1.7-fold) of nontoxic polar diclofop metabolites in R1 relative to the S plants. These results indicate that a non–target-site-based mechanism of enhanced rate of diclofop acid metabolism confers resistance in population R1. Moreover, the high-performance liquid chromotography elution profile of the major diclofop metabolites in R1 is similar to that of wheat, suggesting resistance in individuals of population R1 involves a wheat-like detoxification system mediated by cytochrome P450 monooxygenases. In addition, lower level of tissue diclofop acid was also observed using nonradioactive ultra-performance liquid chromatography–mass spectrometry analysis in resistant individuals of three other resistant wild oat populations (R2, R3, and R4) known to posses ACCase gene resistance mutations. These results establish that either one or at least two independent resistance mechanisms (target-site ACCase resistance mutations and non–target-site enhanced rates of herbicide metabolism) can be present in individual wild oat plants.

Copyright

Corresponding author

Corresponding author's E-mail: qin.yu@uwa.edu.au

Footnotes

Hide All

Current address: Department of Crop Science, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia.

Footnotes

References

Hide All
Ahmad-Hamdani, M. S., Owen, M. J., Yu, Q., and Powles, S. B. 2012. ACCase-inhibiting herbicide resistant wild oat (Avena fatua L.) populations from the Western Australian grain belt. Weed Technol. 26: 130136.
Beckie, H. J. and Tardif, F. J. 2012. Herbicide cross resistance in weeds. Crop Prot. 35: 1528.
Beckie, H. J., Warwick, S. I., and Sauder, C. A. 2012. Basis for herbicide resistance in Canadian populations of wild oat (Avene fatua). Weed Sci. 60: 1018.
Boldt, P. F. and Putnam, A. R. 1980. Selectivity mechanisms for foliar applications of diclofop-methyl. I. Retention, absorption, translocation, and volatility. Weed Sci. 28: 474477.
Cocker, K. M., Coleman, J. O. D., Blair, A. M., Clarke, J. H., and Moss, S. R. 2000. Biochemical mechanisms of cross-resistance to aryloxyphenoxypropionate and cyclohexanedione herbicides in populations of Avena spp. Weed Res. 40: 323334.
Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilising the principle of protein binding. Anal Biochem. 72: 248254.
Cocker, K. M., Moss, S. R., and Coleman, J. O. D. 1999. Multiple mechanisms of resistance to fenoxaprop-P-ethyl in United Kingdom and other European populations of herbicide-resistant Alopecurus myosuroides (black-grass). Pest. Biochem. Physiol. 65: 169180.
Cocker, K. M., Northcroft, D. S., Coleman, J. O. D., and Moss, S. R. 2001. Resistance to ACCase-inhibiting herbicides and isoproturon in UK populations of Lolium multiflorum: mechanisms of resistance and implications for control. Pest Manag. Sci. 57: 587597.
Cruz-Hipolito, H., Osuna, M. D., Domínguez-Valenzuela, J. A., Espinoza, N., and De Prado, R. 2011. Mechanism of resistance to ACCase-inhibiting herbicides in wild oat (Avena fatua) from Latin America. J. Agric. Food Chem. 59: 72617267.
Délye, C. 2005. Weed resistance to acetyl coenzyme A carboxylase inhibitors: an update. Weed Sci. 53: 728746.
Délye, C., Gardin, J. A. C., Boucansaud, K., Chauvel, B., and Petit, C. 2011. Non-target-site-based resistance should be the centre of attention for herbicide resistance research: Alopecurus myosuroides as an illustration. Weed Res. 51: 433437.
Délye, C., Menchari, Y., Guillemin, J. P., Matejicek, A., Michel, S., Camilleri, C., and Chauvel, B. 2007. Status of black grass (Alopecurus myosuroides) resistance to acetyl-coenzyme A carboxylase inhibitors in France. Weed Res. 47: 95105.
De Prado, J. L., Osuna, M. D., Heredia, A., and De Prado, R. 2005. Lolium rigidum, a pool of resistance mechanisms to ACCase inhibitor herbicides. J. Agric. Food Chem. 53: 21852191.
De Prado, R., Gonzalez-Gutierrez, J., Menendez, J., Gasquez, J., Gronwald, J. W., and Gimenez-Espinosa, R. 2000. Resistance to acetyl CoA carboxylase-inhibiting herbicides in Lolium multiflorum . Weed Sci. 48: 311318.
Devine, M. D. and Shimabukuro, R. H. 1994. Resistance to acetyl coenzyme A carboxylase inhibiting herbicides. Pages 141169 in Powles, S. B. and Holtum, J. A. M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: Lewis Publishers, CRC.
Donald, W. W. and Shimabukuro, R. H. 1980. Selectivity of diclofop-methyl between wheat and wild oat: growth and herbicide metabolism. Physiol. Plantarum 49: 459464.
Gronwald, J. W., Eberlein, C. V., Betts, K. J., Baerg, R. J., Ehlke, N. J., and Wyse, D. L. 1992. Mechanism of diclofop resistance in an Italian ryegrass (Lolium multiflorum Lam.) biotype. Pest. Biochem. Physiol. 44: 126139.
Hall, L. M., Moss, S. R., and Powles, S. B. 1997. Mechanisms of resistance to aryloxyphenoxypropionate herbicides in two resistant biotypes of Alopecurus myosuroides (blackgrass): herbicide metabolism as a cross-resistance mechanism. Pest. Biochem. Physiol. 57: 8798.
Hidayat, I. and Preston, C. 1997. Enhanced metabolism of fluazifop acid in a biotype of Digitaria sanguinalis resistant to the herbicide fluazifop-P-butyl. Pest. Biochem. Physiol. 57: 137146.
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.
Jacobson, A. and Shimabukuro, R. H. 1984. Metabolism of diclofop-methyl in root-treated wheat and oat seedlings. J. Agric. Food Chem. 32: 742746.
Letouzé, A. and Gasquez, J. 2001. Inheritance of fenoxaprop-P-ethyl resistance in a blackgrass (Alopecurus myosuroides Huds.) population. Theor. Appl. Genet. 103: 288296.
Maneechote, C., Holtum, J. A. M., Preston, C., and Powles, S. B. 1994. Resistant acetyl-coA carboxylase is a mechanism of herbicide resistance in a biotype of Avena-sterilis ssp. ludoviciana . Plant Cell Physiol. 35: 627635.
Maneechote, C., Preston, C., and Powles, S. B. 1997. A diclofop-methyl-resistant Avena sterilis biotype with a herbicide-resistant acetyl-coenzyme A carboxylase and enhanced metabolism of diclofop-methyl. Pestic. Sci. 49: 105114.
Marles, M. A. S., Devine, M. D., and Hall, J. C. 1993. Herbicide resistance in Setaria viridis conferred by a less sensitive form of acetyl coenzyme-A carboxylase. Pest. Biochem. Physiol. 46: 714.
Matthews, N., Powles, S. B., and Preston, C. 2000. Mechanisms of resistance to acetyl-coenzyme A carboxylase-inhibiting herbicides in a Hordeum leporinum population. Pest Manag. Sci. 56: 441447.
Nandula, V. K. and Messersmith, C. G. 2003. Imazamethabenz-resistant wild oat (Avena fatua L.) is resistant to diclofop-methyl. Pest. Biochem. Physiol. 74: 5361.
Nelson, D. and Werck-Reichhart, D. 2011. A P450-centric view of plant evolution. Plant J. 66: 194211.
Owen, M. J., Walsh, M. J., Llewellyn, R. S., and Powles, S. B. 2007. Widespread occurrence of multiple herbicide resistance in Western Australian annual ryegrass (Lolium rigidum) populations. Aust. J. Agric. Res. 58: 711718.
Owen, M. J. and Powles, S. B. 2009. Distribution and frequency of herbicide-resistant wild oat (Avena spp.) across the Western Australian grain belt. Crop Pasture Sci. 60: 2531.
Powles, S. B. and Yu, Q. 2010. Evolution in action: plants resistant to herbicides. Annu. Rev. Plant Biol. 61: 317347.
Preston, C. 2004. Herbicide resistance in weeds endowed by enhanced detoxification: complications for management. Weed Sci. 52: 448453.
Preston, C. and Powles, S. B. 1998. Amitrole inhibits diclofop metabolism and synergises diclofop-methyl in a diclofop-methyl-resistant biotype of Lolium rigidum . Pest. Biochem. Physiol. 62: 179189.
Preston, C., Tardif, F. J., Christopher, J. T., and 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. Pest. Biochem. Physiol. 54: 123134.
Romano, M. L., Stephenson, G. R., Tal, A., and Hall, J. C. 1993. The effect of monooxygenase and glutathione-S-transferase inhibitors on the metabolism of diclofop-methyl and fenoxaprop-ethyl in barley and wheat. Pest. Biochem. Physiol. 46: 181189.
Scarabel, L., Silvia, P., Serena, V., and Sattin, M. 2011. Allelic variation of the ACCase gene and response to ACCase-inhibiting herbicides in pinoxaden-resistant Lolium spp. Pest Manag. Sci. 67: 932941.
Seefeldt, S. S., Fuerst, E. P., Gealy, D. R., Shukla, A., Irzyk, G. P., and Devine, M. D. 1996. Mechanisms of resistance to diclofop of two wild oat (Avena fatua) biotypes from the Willamette Valley of Oregon. Weed Sci. 44: 776781.
Shimabukuro, R. H., Walsh, W. C., and Hoerauf, R. A. 1979. Metabolism and selectivity of diclofop-methyl in wild oat and wheat. J. Agric. Food Chem. 27: 615623.
Shimabukuro, R. H., Walsh, W. C., and Jacobson, A. 1987. Aryl-O-glucoside of diclofop—a detoxification product in wheat shoots and wild oat-cell suspension-culture. J. Agric. Food Chem. 35: 393397.
Shukla, A., Dupont, S., and Devine, M. D. 1997. Resistance to ACCase-inhibitor herbicides in wild oat: evidence for target site-based resistance in two biotypes from Canada. Pest. Biochem. Physiol. 57: 147155.
Siminszky, B. 2006. Plant cytochrome P450-mediated herbicide metabolism. Phytochem. Rev. 5: 445458.
Tanaka, F. S., Hoffer, B. L., Shimabukuro, R. H., Wien, R. G., and Walsh, W. C. 1990. Identification of the isomeric hydroxylated metabolites of methyl 2-4-(2,4-dichlorophenoxy)-phenoxy propanoate (diclofop-methyl) in wheat. J. Agric. Food Chem. 38: 559565.
Tardif, F. J. and Powles, S. B. 1994. Herbicide multiple-resistance in a Lolium rigidum biotype is endowed by multiple mechanisms—isolation of a subset with resistant acetyl-coA carboxylase. Physiol. Plantarum 91: 488494.
Yu, Q., Ahmad-Hamdani, M. S., Han, H. P., Christoffers, M. J., and Powles, S. B. 2012. Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity. DOI:10.1038/hdy.2012.69.
Yu, Q., Friesen, L. J. S., Zhang, X. Q., and Powles, S. B. 2004. Tolerance to acetolactate synthase and acetyl-coenzyme A carboxylase inhibiting herbicides in Vulpia bromoides is conferred by two co-existing resistance mechanisms. Pest. Biochem. Physiol. 78: 2130.
Zimmerlin, A. and Durst, F. 1990. Xenobiotic metabolism in plants—aryl hydroxylation of diclofop by a cytochrome-P-450 enzyme from wheat. Phytochemistry 29: 17291732.
Zimmerlin, A., Salaün, J-P., Durst, F., and 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: 868873.

Keywords

Herbicide Resistance Endowed by Enhanced Rates of Herbicide Metabolism in Wild Oat (Avena spp.)

  • M. S. Ahmad-Hamdani (a1), Qin Yu (a1), Heping Han (a1), Gregory R. Cawthray (a1), Shao F. Wang (a2) and Stephen B. Powles (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed