Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-14T13:25:39.921Z Has data issue: false hasContentIssue false

Multiple ALS Mutations Confer Herbicide Resistance in Waterhemp (Amaranthus tuberculatus)

Published online by Cambridge University Press:  20 January 2017

William L. Patzoldt
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
Patrick J. Tranel*
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
*
Corresponding author's E-mail: [email protected]

Abstract

In a survey of herbicide responses among Illinois waterhemp half-sib populations, several were observed with differential responses to imazethapyr and thifensulfuron, two acetolactate synthase (ALS)–inhibiting herbicides. Plants from two waterhemp populations were verified resistant to imazethapyr, but susceptible to chlorimuron, using a nondestructive leaf-disc assay. Sequencing of the ALS gene revealed that imazethapyr-resistant waterhemp plants from both populations had inferred amino acid substitutions at position 653 of ALS. Depending on the population, the serine at position 653 of ALS was substituted with either asparagine (S653N) or threonine (S653T). Waterhemp lines were derived from each population to create uniformly imidazolinone-resistant (IR) waterhemp biotypes, designated IR-62 and IR-101. ALS-inhibitor responses of each IR biotype were compared with a previously identified ALS inhibitor–resistant biotype with a tryptophan to leucine substitution at position 574 (W574L) and an herbicide-susceptible control. Whole-plant dose–response experiments with waterhemp biotypes containing W574L, S653N, or S653T mutations indicated that each biotype was resistant to imazethapyr, but only the biotype with a W574L mutation was resistant to thifensulfuron. In vitro ALS-activity assays revealed unique patterns of cross-resistance among protein extracts derived from each biotype in response to imazethapyr, thifensulfuron, cloransulam, and pyrithiobac. In conclusion, three different forms of target-site–based resistance to ALS inhibitors have been identified in waterhemp.

Type
Physiology, Chemistry, and Biochemistry
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.)

References

Literature Cited

Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248254.CrossRefGoogle ScholarPubMed
Chang, A. K. and Duggleby, R. G. 1998. Herbicide-resistant forms of Arabidopsis thaliana acetohydroxyacid synthase: characterization of the catalytic properties and sensitivity to inhibitors of four defined mutants. Biochem. J. 333:765777.Google Scholar
Cho, J. H., Ahn, S. C., Koo, S. J., Joe, K. H., and Oh, H. S. 1997. LGC-40863: A new broad spectrum postemergence herbicide. Pages 3944. in. Proceedings of the Brighton Crop Protection Conference—Weeds. Hampshire, UK British Crop Production Council.Google Scholar
Christopher, J. T., Powles, S. B., and Holtum, J. A. M. 1992. Resistance to acetolactate synthase-inhibiting herbicides in annual ryegrass (Lolium rigidum) involves at least two mechanisms. Plant Physiol. 100:19091913.CrossRefGoogle ScholarPubMed
Diebold, R. S., McNaughton, K. E., Lee, E. A., and Tardif, F. J. 2003. Multiple resistance to imazethapyr and atrazine in Powell amaranth (Amaranthus powellii). Weed Sci. 51:312318.Google Scholar
Doyle, J. J. and Doyle, J. L. 1990. Isolation of plant DNA from fresh tissue. Focus. 12:1315.Google Scholar
Emanuelsson, O., Nielsen, H., Brunak, S., and Heijne, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:10051016.Google Scholar
Feucht, D., Müller, K. H., and Wellmann, A. 1999. BAY MKH 6561—a new selective herbicide for grass control in wheat, rye and triticale. Pages 5358. in. Proceedings of the Brighton Conference—Weeds. Hampshire, UK British Crop Production Council.Google Scholar
Foes, M. J., Liu, L., Tranel, P. J., Wax, L. M., and Stoller, E. W. 1998. A biotype of common waterhemp (Amaranthus rudis) resistant to triazine and ALS herbicides. Weed Sci. 31:514520.Google Scholar
Foes, M. J., Liu, L., Vigue, G., Stoller, E. W., Wax, L. M., and Tranel, P. J. 1999. A kochia (Kochia scoparia) biotype resistant to triazine and ALS-inhibiting herbicides. Weed Sci. 47:2027.Google Scholar
Hacker, E., Bieringer, H., Willms, L., Ort, O., Koecher, H., and Kehne, H. 1999. Iodosulfuron plus mefenpyr-diethyl – a new foliar herbicide for weed control in cereals. Pages 1522. in. Proceedings of the Brighton Conference—Weeds. Hampshire, UK British Crop Production Council.Google Scholar
Hager, A. G. and Sprague, C. L. 2003. Weed control for corn, soybeans, and sorghum. Pages 27114. in. Illinois Agricultural Pest Management Handbook. Urbana, IL University of Illinois Extension, College of Agricultural, Consumer, and Environmental Sciences, University of Illinois.Google Scholar
Heap, I. 2006. International Survey of Herbicide Resistant Weeds. http://www.weedscience.com. Accessed: July 30, 2006.Google Scholar
Hidayat, I. and Preston, C. 2001. Cross-resistance to imazethapyr in a fluazifop-P-butyl-resistant population of Digitaria sanguinalis . Pestic. Biochem. Physiol. 71:190195.Google Scholar
Jasieniuk, M., Brûlé-Babel, A. L., and Morrison, I. N. 1996. The evolution and genetics of herbicide resistance in weeds. Weed Sci. 44:176193.CrossRefGoogle Scholar
Kim, J., Liu, K., Kang, S., Koo, S., and Kim, J. 2003. Degradation of the sulfonylurea herbicide LGC-42153 in flooded soil. Pest. Manag. Sci. 59:10371042.Google Scholar
Koo, S. J., Ahn, S., Lim, J. S., Chae, S. H., Kim, J. S., Lee, J. H., and Cho, J. H. 1997. Biological activity of the new herbicide LGC-40863 benzophenone O-[2,6-bis[(4,6-dimethoxy-2-pyrimidinyl)oxy]benzoyl]oxime. Pestic. Sci. 51:109114.Google Scholar
Larelle, D., Mann, R., Cavanna, S., Bernes, R., Duriatti, A., and Mavrotas, C. 2003. Penoxsulam, a new broad spectrum rice herbicide for weed control in European Union paddies. Pages 7580. in. Proceedings of the Brighton Conference—Crop Science and Technology. Hampshire, UK British Crop Production Council.Google Scholar
Lee, Y., Chang, A. K., and Duggleby, R. G. 1999. Effect of mutagenesis at serine 653 of Arabidopsis thaliana acetohydroxyacid synthase on the sensitivity to imidazolinone and sulfonylurea herbicides. FEBS Lett. 452:341345.Google Scholar
Lüthy, C., Zondler, H., Rapold, T., Seifert, G., Urwyler, B., Heinis, T., Steinrücken, H. C., and Allen, J. 2001. 7-(4,6-Dimethoxypyrimidinyl)oxy- and –thiophthalides as novel herbicides, part 1: CGA 279 233: a new grass-killer for rice. Pest Manag. Sci. 57:205224.Google Scholar
Martz, E. 2002. Protein explorer: easy yet powerful macromolecular visualization. Trends Biochem. Sci. 27:107109. http://www.proteinexplorer.org.Google Scholar
McCourt, J. A., Pang, S. S., King-Scott, J., Guddat, L. W., and Duggleby, R. G. 2006. Herbicide-binding sites revealed in the structure of plant acetohydroxyacid synthase. Proc. Natl. Acad. Sci. U. S. A. 103:569573.CrossRefGoogle ScholarPubMed
McNaughton, K. E., Letarte, J., Lee, E. A., and Tardif, F. 2005. Mutations in ALS confer herbicide resistance in redroot pigweed (Amaranthus retroflexus) and Powell amaranth (Amaranthus powellii). Weed Sci. 53:1722.CrossRefGoogle Scholar
Morrica, P., Giordano, A., Seccia, S., Ungaro, F., and Ventriglia, M. 2001. Degradation of imazosulfuron in soil. Pest Manag. Sci. 57:360365.Google Scholar
Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant. 15:473497.Google Scholar
Nandula, V. K. and Messersmith, C. G. 2001. Resistance to BAY MKH 6562 in wild oat (Avena fatua). Weed Technol. 15:343347.Google Scholar
Patzoldt, W. L., Hager, A. G., McCormick, J. S., and Tranel, P. J. 2006. A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc. Natl. Acad. Sci. U. S. A. 103:1232912334.Google Scholar
Patzoldt, W. L., Tranel, P. J., Alexander, A. L., and Schmitzer, P. R. 2001. A common ragweed population resistant to cloransulam-methyl. Weed Sci. 49:485490.Google Scholar
Patzoldt, W. L., Tranel, P. J., and Hager, A. G. 2002. Variable herbicide responses among Illinois waterhemp (Amaranthus rudis and A. tuberculatus) populations. Crop Prot. 21:707712.Google Scholar
Patzoldt, W. L., Tranel, P. J., and Hager, A. G. 2005. A waterhemp (Amaranthus tuberculatus) biotype with multiple resistance across three herbicide sites of action. Weed Sci. 53:3036.Google Scholar
Roux, F., Gasquez, J., and Reboud, X. 2004. The dominance of herbicide resistance cost in several Arabidopsis thaliana mutant lines. Genetics. 166:449460.Google Scholar
Santel, H. J., Bowden, B. A., Sorensen, V. M., and Mueller, K. H. 1999. Flucarbazone-sodium—a new herbicide for the selective control of wild oat and green foxtail in wheat. Pages 2328. in. Proceedings of the Brighton Conference—Weeds. Hampshire, UK British Crop Production Council.Google Scholar
Sathasivan, K., Haughn, G. W., and Murai, N. 1990. Nucleotide sequence of a mutant acetolactate synthase gene from an imidazolinone-resistant Arabidopsis thaliana var. Columbia. Nucleic Acids Res. 18:2188.Google Scholar
Saunders, J. W., Acquaah, G., Renner, K. A., and Doley, W. P. 1992. Monogenic dominant sulfonylurea resistance in sugarbeet from somatic cell selection. Crop Sci. 32:13571360.Google Scholar
Schmitzer, P. R., Eilers, R. J., and Cséke, C. 1993. Lack of cross-resistance of imazaquin-resistant Xanthium strumarium acetolactate synthase to flumetsulam and chlorimuron. Plant Physiol. 103:281283.Google Scholar
Sebastian, S. A., Fader, G. M., Ulrich, J. F., Forney, D. R., and Chaleff, R. S. 1989. Semidominant soybean mutation for resistance to sulfonylurea herbicides. Crop Sci. 29:14031408.Google Scholar
Seefeldt, S. S., Jensen, J. E., and Fuerst, E. P. 1995. Log-logistic analysis of herbicide dose-response relationships. Weed Technol. 9:218227.CrossRefGoogle Scholar
Sprague, C. L., Stoller, E. W., and Wax, L. M. 1997. Response of an acetolactate synthase (ALS)-resistant biotype of Amaranthus rudis to selected ALS-inhibiting and alternative herbicides. Weed Res. 37:93101.Google Scholar
Tan, S., Evans, R. R., Dahmer, M. L., Singh, B. K., and Shaner, D. L. 2005. Imidazolinone-tolerant crops: history, current status and future. Pest Manag. Sci. 61:246257.Google Scholar
Tranel, P. J. and Wright, T. R. 2002. Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci. 50:700712.Google Scholar
[USDA] U.S. Department of Agriculture 2004. National Agricultural Statistical Service. Agricultural Chemical Usage (PCU-BB). http://www.usda.mannlib.cornell.edu/reports/nassr/other/pcu-bb/. Accessed: July 14, 2004.Google Scholar
Veldhuis, L. J., Hall, L. M., O'Donovan, J. T., Dyer, W., and Hall, J. C. 2000. Metabolism-based resistance of a wild mustard (Sinapis arvensis L.) biotype to ethametsulfuron-methyl. J. Agric. Food Chem. 48:29862990.Google Scholar
Whaley, C. M., Wilson, H. P., and Westwood, J. H. 2004. Characterization of a new ALS-inhibitor resistance mutation from the ALS gene of smooth pigweed (Amaranthus hybridus). Weed Sci. Soc. Am. 44:161. [Abstract].Google Scholar
Whaley, C. M., Wilson, H. P., and Westwood, J. H. 2006. ALS resistance in several smooth pigweed (Amaranthus hybridus) biotypes. Weed Sci. 54:828832.Google Scholar
Westerfeld, W. W. 1945. A colorimetric determination of blood acetoin. J. Biol. Chem. 161:495502.Google Scholar
Wright, T. R. and Penner, D. 1998. Cell selection and inheritance of imidazolinone resistance in sugarbeet (Beta vulgaris). Theor. Appl. Genet. 96:612620.Google Scholar