Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-04T20:12:34.021Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  20 January 2017

M. S. Ahmad-Hamdani ,
Qin Yu ,
Heping Han ,
Gregory R. Cawthray ,
Shao F. Wang  and
Stephen B. Powles
M. S. Ahmad-Hamdani
Affiliation:
Australian Herbicide Resistance Initiative (M086) and School of Plant Biology, the University of Western Australia (UWA), Crawley, WA 6009, Australia
Qin Yu*
Affiliation:
Australian Herbicide Resistance Initiative (M086) and School of Plant Biology, the University of Western Australia (UWA), Crawley, WA 6009, Australia
Heping Han
Affiliation:
Australian Herbicide Resistance Initiative (M086) and School of Plant Biology, the University of Western Australia (UWA), Crawley, WA 6009, Australia
Gregory R. Cawthray
Affiliation:
Australian Herbicide Resistance Initiative (M086) and School of Plant Biology, the University of Western Australia (UWA), Crawley, WA 6009, Australia
Shao F. Wang
Affiliation:
ChemCentre, Resources and Chemistry Precinct, Curtin University, Bentley, WA 6102, Australia, and Centre for Legumes in Mediterranean Agriculture UWA
Stephen B. Powles
Affiliation:
Australian Herbicide Resistance Initiative (M086) and School of Plant Biology, the University of Western Australia (UWA), Crawley, WA 6009, Australia
*
Corresponding author's E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Diclofop-methylwild oat, Avena fatua L. AVEFAHerbicide uptake and translocationmultiple resistance mechanismsnon-target-site based resistance
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 61 , Issue 1 , March 2013 , pp. 55 - 62
Copyright
Copyright © 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.)

Footnotes

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

References

Literature Cited

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: 130–136.Google Scholar
Beckie, H. J. and Tardif, F. J. 2012. Herbicide cross resistance in weeds. Crop Prot. 35: 15–28.Google Scholar
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: 10–18.Google Scholar
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: 474–477.Google Scholar
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: 323–334.Google Scholar
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: 248–254.Google Scholar
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: 169–180.Google Scholar
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: 587–597.Google Scholar
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: 7261–7267.Google Scholar
Délye, C. 2005. Weed resistance to acetyl coenzyme A carboxylase inhibitors: an update. Weed Sci. 53: 728–746.Google Scholar
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: 433–437.Google Scholar
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: 95–105.Google Scholar
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: 2185–2191.Google Scholar
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: 311–318.Google Scholar
Devine, M. D. and Shimabukuro, R. H. 1994. Resistance to acetyl coenzyme A carboxylase inhibiting herbicides. Pages 141–169 in Powles, S. B. and Holtum, J. A. M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: Lewis Publishers, CRC.Google Scholar
Donald, W. W. and Shimabukuro, R. H. 1980. Selectivity of diclofop-methyl between wheat and wild oat: growth and herbicide metabolism. Physiol. Plantarum 49: 459–464.Google Scholar
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: 126–139.Google Scholar
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: 87–98.Google Scholar
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: 137–146.Google Scholar
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: 1026–1034.Google Scholar
Jacobson, A. and Shimabukuro, R. H. 1984. Metabolism of diclofop-methyl in root-treated wheat and oat seedlings. J. Agric. Food Chem. 32: 742–746.Google Scholar
Letouzé, A. and Gasquez, J. 2001. Inheritance of fenoxaprop-P-ethyl resistance in a blackgrass (Alopecurus myosuroides Huds.) population. Theor. Appl. Genet. 103: 288–296.Google Scholar
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: 627–635.Google Scholar
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: 105–114.Google Scholar
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: 7–14.Google Scholar
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: 441–447.Google Scholar
Nandula, V. K. and Messersmith, C. G. 2003. Imazamethabenz-resistant wild oat (Avena fatua L.) is resistant to diclofop-methyl. Pest. Biochem. Physiol. 74: 53–61.Google Scholar
Nelson, D. and Werck-Reichhart, D. 2011. A P450-centric view of plant evolution. Plant J. 66: 194–211.Google Scholar
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: 711–718.Google Scholar
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: 25–31.Google Scholar
Powles, S. B. and Yu, Q. 2010. Evolution in action: plants resistant to herbicides. Annu. Rev. Plant Biol. 61: 317–347.Google Scholar
Preston, C. 2004. Herbicide resistance in weeds endowed by enhanced detoxification: complications for management. Weed Sci. 52: 448–453.Google Scholar
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: 179–189.Google Scholar
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: 123–134.Google Scholar
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: 181–189.Google Scholar
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: 932–941.Google Scholar
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: 776–781.Google Scholar
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: 615–623.Google Scholar
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: 393–397.Google Scholar
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: 147–155.Google Scholar
Siminszky, B. 2006. Plant cytochrome P450-mediated herbicide metabolism. Phytochem. Rev. 5: 445–458.Google Scholar
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: 559–565.Google Scholar
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: 488–494.Google Scholar
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.Google Scholar
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: 21–30.Google Scholar
Zimmerlin, A. and Durst, F. 1990. Xenobiotic metabolism in plants—aryl hydroxylation of diclofop by a cytochrome-P-450 enzyme from wheat. Phytochemistry 29: 1729–1732.Google Scholar
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: 868–873.Google Scholar