Hostname: page-component-77c89778f8-swr86 Total loading time: 0 Render date: 2024-07-19T11:06:51.408Z Has data issue: false hasContentIssue false

Acetolactate Synthase (ALS) Target-Site Mutations in ALS Inhibitor-Resistant Russian Thistle (Salsola tragus)

Published online by Cambridge University Press:  20 January 2017

Suzanne I. Warwick*
Affiliation:
Agriculture and Agri-Food Canada [AAFC], Eastern Cereal and Oilseed Research Centre, K. W. Neatby Bldg., Central Experimental Farm, Ottawa, Ontario, Canada K1A 0C6
Connie A. Sauder
Affiliation:
Agriculture and Agri-Food Canada [AAFC], Eastern Cereal and Oilseed Research Centre, K. W. Neatby Bldg., Central Experimental Farm, Ottawa, Ontario, Canada K1A 0C6
Hugh J. Beckie
Affiliation:
AAFC, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan, Canada S7N 0X2
*
Corresponding author's E-mail: Suzanne.Warwick@agr.gc.ca

Abstract

ALS inhibitor-resistant biotypes are the fastest growing class of herbicide-resistant (HR) weeds. A Canadian ALS inhibitor-resistant biotype of Russian thistle was first reported in 1989. The molecular basis for ALS-inhibitor resistance is unknown for Canadian populations of this polyploid weed species, and was determined in this study for one Alberta and two Saskatchewan HR Russian thistle populations. HR plants survived spray application of the ALS-inhibitor mixture thifensulfuron : tribenuron in the greenhouse. All three HR Russian thistle populations were heterogeneous and contained both HR and herbicide-susceptible (HS) individuals. The molecular basis for resistance was determined by sequencing the ALS gene and/or conducting a TaqMan genotyping assay for single nucleotide polymorphism (SNP) for the Trp574Leu mutation. Two target-site mutations were observed: Trp574Leu in all three biotypes (554 individuals) and Pro197Gln in one biotype (one individual), suggesting multiple-founding events for Russian thistle HR populations in western Canada. Segregation patterns among F1 and F2 progeny arrays of HR lines sprayed under greenhouse conditions varied; some segregated (i.e., had HR and HS progeny), whereas other lines were exclusively HR. In contrast, no segregation of molecular types, i.e., Trp574, Trp/Leu574 and Leu574, as would be expected with heterozygosity at a single locus Trp/Leu574, was observed. Such lack of segregation is consistent with the polyploid genome structure of Russian thistle and the presence of two copies of the ALS gene. The presence of more than one ALS gene confounded the ability of the molecular techniques to accurately identify “true” heterozygotes in this study.

Type
Weed Biology and Ecology
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

Bassett, I. J. and Crompton, C. W. 1970. in Löve, A. ed. IOPB Chromosome Number Reports XXVII. Taxon. 19:437442.Google Scholar
Beckie, H. J. 2009. Herbicide-resistant weeds on the march in Alberta. Pages 97106. in. Agronomy Update 2009. Lethbridge, Alberta, Canada: Southern Applied Research Association.Google Scholar
Beckie, H. J. and Francis, A. 2009. The biology of Canadian weeds. 65. Salsola tragus L. (Updated). Can. J. Plant Sci. 89:775789.10.4141/CJPS08181Google Scholar
Beckie, H. J., Hall, L. M., Tardiff, F. J., and Séguin-Swartz, G. 2007. Acetolactate synthase inhibitor-resistant stinkweed (Thlaspi arvense L.) in Alberta. Can. J. Plant Sci. 87:965972.10.4141/CJPS06019Google Scholar
Bernasconi, P., Woodworth, A. R., Rosen, B. A., Subramanian, M. V., and Siehl, D. L. 1995. A naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase. J. Biol. Chem. 270:1738117385.Google Scholar
Boutsalis, P., Karotam, J., and Powles, S. B. 1999. Molecular basis of resistance to acetolactate synthase-inhibiting herbicides in Sisymbrium orientale and Brassica tournefortii . Pestic. Sci. 55:507516.10.1002/(SICI)1096-9063(199905)55:5<507::AID-PS971>3.0.CO;2-G3.0.CO;2-G>Google Scholar
Corbett, C. L. and Tardif, F. J. 2006. Detection of resistance to acetolactate synthase inhibitors in weeds with emphasis on DNA-based techniques: a review. Pest Manag. Sci. 62:584597.Google Scholar
Cui, H. L., Zhang, C. X., Zhang, H. J., Liu, X., Liu, Y., Wang, G. Q., Huang, H. J., and Wei, S. H. 2008. Confirmation of flixweed (Descurainia sophia) resistance to tribenuron in China. Weed Sci. 56:775779.Google Scholar
Devine, M. D. and Eberlein, C. V. 1997. Physiological, biochemical and molecular aspects of herbicide resistance based on altered target sites. Pages 159185. in Roe, R. M., Burton, J. D., and Kuhr, R. J. eds. Herbicide Activity: Toxicology, Biochemistry and Molecular Biology. Amsterdam, The Netherlands: IOS Press.Google Scholar
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
Duggleby, R. G., McCourt, J. A., and Guddat, L. W. 2008. Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Physiol. Biochem. 46:309324.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. 47:2027.10.1017/S0043174500090603Google Scholar
Gaines, T. A., Zhang, W., Wang, D., Bukun, B., et al. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc. Natl. Acad. Sci. U. S. A. 107:10291034.Google Scholar
Guttieri, M. J., Eberlein, C. V., Mallory-Smith, C. A., Thill, D. C., and Hoffman, D. L. 1992. DNA sequence variation in Domain A of the acetolactate synthase genes of herbicide-resistant and -susceptible weed biotypes. Weed Sci. 40:670676.Google Scholar
Hanson, B. D., Park, K. W., Mallory-Smith, C. A., and Thill, D. C. 2004. Resistance of Camelina microcarpa to acetolactate synthase inhibiting herbicides. Weed Res. 44:187194.Google Scholar
Heap, I. 2010. The International Survey of Herbicide Resistant weeds. http://www.weedscience.org. Accessed: November 10, 2009.Google Scholar
Heiser, C. B. Jr. and Whitaker, T. W. 1948. Chromosome number, polyploidy, and growth habit in California weeds. Am. J. Bot. 35:179186.Google Scholar
Kaloumenos, N. S., Dordas, C. A., Diamantidis, G. C., and Eleftherohorinos, I. G. 2009. Multiple Pro197 substitutions in the acetolactate synthase of corn poppy (Papaver rhoeas) confer resistance to tribenuron. Weed Sci. 57:362368.10.1614/WS-08-166.1Google Scholar
Lee, J. M. and Owen, M. D. K. 2000. Comparison of acetolactate synthase enzyme inhibition among resistant and susceptible Xanthium strumarium biotypes. Weed Sci. 48:286290.Google Scholar
Leeson, J. Y., Thomas, A. G., Hall, L. M., Brenzil, C., Andrews, T., Brown, K. R., and Van Acker, R. C. 2005. Prairie Weed Surveys of Cereal, Oilseed and Pulse Crops from the 1970s to the 2000s. Weed Survey Series Publ. 05–1. Saskatoon, Saskatchewan, Canada: Agriculture and Agri-Food Canada. 395.Google Scholar
Liu, W., Harrison, D. K., Chalupska, D., Gornicki, P., O'Donnell, C. C., Adkins, S. W., Haselkorn, R., and Williams, R. R. 2007. Single-site mutations in the carboxyltransferase domain of plastid acetyl-CoA carboxylase confer resistance to grass-specific herbicides. Proc. Natl. Acad. Sci. U. S. A. 104:36273632.Google Scholar
Marshall, R. and Moss, S. R. 2008. Characterisation and molecular basis of ALS inhibitor resistance in the grass weed Alopecurus myosuroides . Weed Res. 48:439447.10.1111/j.1365-3180.2008.00654.xGoogle Scholar
McNaughton, K. E., Letarte, J., Lee, E. A., and Tardif, F. J. 2005. Mutations in ALS confer herbicide resistance in redroot pigweed (Amaranthus retroflexus) and Powell amaranth (Amaranthus powellii). Weed Sci. 53:1722.10.1614/WS-04-109Google Scholar
Morrison, I. N. and Devine, M. D. 1994. Herbicide resistance in the Canadian prairie provinces: five years after the fact. Phytoprotection. 75 (Suppl):516.10.7202/706067arGoogle Scholar
Mosyakin, S. L. 2003. Salsola Linnaeus. Pages 398403. in. Flora of North America north of Mexico. Vol. 4. Magnoliophyta:Caryophyllidae, Part 1. New York, NY and Oxford, UK: Flora of North America Editorial Committee and Oxford University Press.Google Scholar
Mulligan, G. A. 1961. Chromosome numbers of Canadian weeds. III. Can. J. Bot. 39:10571066.10.1139/b61-092Google Scholar
Park, K. W. and Mallory-Smith, C. A. 2004. Physiological and molecular basis for ALS inhibitor resistance in Bromus tectorum biotypes. Weed Res. 44:7177.10.1111/j.1365-3180.2003.00374.xGoogle Scholar
Patzoldt, W. L. and Tranel, P. J. 2007. Multiple ALS mutations confer herbicide resistance in waterhemp (Amaranthus tuberculatus). Weed Sci. 55:421428.Google Scholar
Peterson, D. E. 1999. The impact of herbicide-resistant weeds on Kansas agriculture. Weed Technol. 13:632635.Google Scholar
Rozen, S. and Skaletsky, H. J. 2000. Primer3 on the WWW for general users and for biologist programmers. Pages 365386. in Krawetz, S. and Misener, S. eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press. Source code available at http://fokker.wi.mit.edu/primer3. Accessed: November 15, 2009.Google Scholar
Ryan, J. F., Mosyakin, S. L., and Pitcairn, M. J. 2007. Molecular comparisons of Salsola tragus from California and Ukraine. Can J. Bot. 85:224229.Google Scholar
Saari, L. L., Cotterman, J. C., Smith, W. F., and Primiani, M. M. 1992. Sulfonylurea herbicide resistance in common chickweed, perennial ryegrass and Russian thistle. Pestic. Biochem. Physiol. 42:110118.10.1016/0048-3575(92)90058-8Google Scholar
Sathasivan, K., Haughn, G. W., and Murai, N. 1990. Nucleotide sequence of a mutant acetolactate synthase gene from imidazolinone resistant Arabidopsis thaliana var Columbia. Nucleic Acids Res. 18:2188.Google Scholar
Sibony, M. and Rubin, B. 2003. Molecular basis for multiple resistance to acetolactate synthase-inhibiting herbicides and atrazine in Amaranthus blitoides (prostrate pigweed). Planta (Berl.) 216:10221027.Google Scholar
Stallings, G. P., Thill, D. C., and Mallory-Smith, C. A. 1994. Sulfonylurea-resistant Russian thistle (Salsola iberica) survey in Washington State. Weed Technol. 8:258264.Google Scholar
Stallings, G. P., Thill, D. C., Mallory-Smith, C. A., and Lass, L. W. 1995. Plant movement and seed dispersal of Russian thistle (Salsola iberica). Weed Sci. 43:6369.Google Scholar
Tan, S. Y., 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
Tan, M. K. and Medd, R. W. 2002. Characterisation of the acetolactate synthase (ALS) gene of Raphanus raphanistrum L. and the molecular assay of mutations associated with herbicide resistance. Plant Sci. 163:195205.Google Scholar
Tan, M-K., Preston, C., and Wang, G-X. 2007. Molecular basis of multiple resistance to ACCase-inhibiting and ALS-inhibiting herbicides in Lolium rigidum . Weed Res. 47:534541.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
Tranel, P. J., Wright, T. R., and Heap, I. M. 2010. ALS mutations from herbicide-resistant weeds. http://www.weedscience.org. Accessed: February 10, 2009.Google Scholar
Uchino, A., Ogata, S., Kohara, H., Yoshida, S., Yoshioka, T., and Watanabe, H. 2007. Molecular basis of diverse responses to acetolactate synthase-inhibiting herbicides in sulfonylurea-resistant biotypes of Schoenoplectus juncoides . Weed Biol. Manag. 7:8996.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
Warwick, S. I., Sauder, C., and Beckie, H. J. 2005. Resistance in Canadian biotypes of wild mustard (Sinapis arvensis) to acetolactate synthase inhibiting herbicides. Weed Sci. 53:631639.Google Scholar
Warwick, S. I., Sauder, C., and Beckie, H. J. 2010. ALS-inhibitor resistance on the rise: Russian thistle and wild buckwheat biotypes. Proceedings of the Canadian Weed Science Society National meeting, Charlottetown, PE (in press).Google Scholar
Warwick, S. I., Xu, R., Sauder, C., and Beckie, H. J. 2008. Acetolactate synthase target-site mutations and single nucleotide polymorphism genotyping in ALS-resistant kochia (Kochia scoparia). Weed Sci. 56:797806.Google Scholar
Yu, Q., Abdallah, I., Han, H., Owen, M., and Powles, S. B. 2009. Distinct non-target site mechanisms endow resistance to glyphosate, ACCase and ALS-inhibiting herbicides in multiple herbicide-resistant Lolium rigidum . Planta. 230:713723.Google Scholar
Yu, Q., Heping, H., and Powles, S. B. 2008. Mutations of the ALS gene endowing resistance to ALS-inhibiting herbicides in Lolium rigidum populations. Pest Manag. Sci. 64:12291236.Google Scholar
Yu, Q., Nelson, J. K., Zheng, M. Q., Jackson, M., and Powles, S. B. 2007. Molecular characterisation of resistance to ALS-inhibiting herbicides in Hordeum leporinum biotypes. Pest Manag. Sci. 63:918927.10.1002/ps.1429Google Scholar
Yu, Q., Zhang, X. Q., Hashem, A., Walsh, M. J., and Powles, S. B. 2003. ALS gene proline (197) mutations confer ALS herbicide resistance in eight separated wild radish (Raphanus raphanistrum) populations. Weed Sci. 51:831883.Google Scholar