Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-21T14:47:33.603Z Has data issue: false hasContentIssue false
  • English
  • Français

Investigating the mechanism of glyphosate resistance in rigid ryegrass (Lolium ridigum)

Published online by Cambridge University Press:  20 January 2017

Scott R. Baerson ,
Damian J. Rodriguez ,
Nancy A. Biest ,
Minhtien Tran ,
Jinsong You ,
Roger W. Kreuger ,
Gerald M. Dill ,
James E. Pratley  and
Kenneth J. Gruys
Scott R. Baerson
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Damian J. Rodriguez
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Nancy A. Biest
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Minhtien Tran
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Jinsong You
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Roger W. Kreuger
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
Gerald M. Dill
Affiliation:
Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, MO 63167
James E. Pratley
Affiliation:
Farrer Centre, Faculty of Science and Agriculture, Charles Sturt University, Wagga Wagga, NSW 2678, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Glyphosate is a broad-spectrum herbicide that has been used extensively for more than 20 yr. The first glyphosate-resistant weed biotype appeared in 1996; it involved a rigid ryegrass population from Australia that exhibited an LD50 value approximately 10-fold higher than that of sensitive biotypes. We have characterized gene expression levels and glyphosate sensitivity of 5-enolpyruvylshikimate 3-phosphate synthase (EPSPS), the target enzyme for glyphosate inhibition, in sensitive and resistant lines derived from this population. Restriction fragment length polymorphism analyses were also performed to examine the distribution of EPSPS gene variants and the gene copy number. A two- to threefold increase in basal EPSPS messenger RNA (mRNA) and enzyme activity levels was observed in the most resistant lines analyzed; however, differences among lines in the sensitivity of EPSPS to glyphosate were not apparent. Induction of EPSPS was observed within 48 h after application of 1.5 kg ae ha−1 of glyphosate. This was reflected in elevated levels of both EPSPS mRNA and enzyme activity. Similarly, 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase mRNA levels increased after glyphosate treatment; however, basal and induced transcript levels were comparable for sensitive and resistant lines in this case. The restriction fragment length polymorphism analyses showed no evidence for gene amplification or cosegregation of a specific EPSPS gene variant with glyphosate resistance. EPSPS expression in lines exhibiting an intermediate level of resistance was indistinguishable from that in glyphosate-sensitive lines, suggesting that the mechanism could, at least in part, be non–target-based.

Keywords

Glyphosaterigid ryegrass, Lolium rigidum Gaudin LOLRIDAHPS3-deoxy-D-arabino-heptulosonate 7-phosphate synthase5-enolpyruvylshikimate 3-phosphate synthaseEPSPSherbicide resistance
Type
Research Article
Information
Weed Science , Volume 50 , Issue 6 , December 2002 , pp. 721 - 730
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

Present address: USDA, ARS, Natural Products Utilization Research Unit, P.O. Box 8048, University, MS 38677

References

Literature Cited

Baerson, S. R., Rodriguez, D. J., Tran, M., Feng, Y., Biest, N. A., and Dill, G. M. 2002. Glyphosate-resistant Eleusine indica: identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol. 129:1265–1275.Google Scholar
Boerboom, C. M., Wyse, D. L., and Somers, D. A. 1990. Mechanism of glyphosate tolerance in birdsfoot trefoil (Lotus corniculatus). Weed Sci. 38:463–467.CrossRefGoogle Scholar
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. 72:248–254.Google Scholar
Bradshaw, L. D., Padgette, S. R., Kimball, S. L., and Wells, B. H. 1997. Perspectives on glyphosate resistance. Weed Technol. 11:189–198.CrossRefGoogle Scholar
Duncan, C. N. and Weller, S. C. 1987. Heritability of glyphosate susceptibility among biotypes of field bindweed. J. Hered. 78:257–260.CrossRefGoogle Scholar
Dyer, W. E., Henstrand, J. M., Handa, A. K., and Herrmann, K. M. 1989. Wounding induces the first step of the shikimate pathway in Solanaceae . Proc. Natl. Acad. Sci. USA 86:7370–7373.CrossRefGoogle Scholar
Feng, P.C.C., Pratley, J. E., and Bohn, J. A. 1999. Resistance to glyphosate in Lolium rigidum . II. Uptake, translocation, and metabolism. Weed Sci. 47:412–415.Google Scholar
Görlach, J., Raesecke, H. R., Rentsch, D., et al. 1995. Temporally distinct accumulation of transcripts encoding enzymes of the prechorismate pathway in elicitor-treated, cultured tomato cells. Proc. Natl. Acad. Sci. USA 92:3166–3170.Google Scholar
Hall, L. M., Holtum, J.A.M., and Powles, S. B. 1994. Mechanisms responsible for cross resistance and multiple resistance. Pages 243–262 In Powles, S. B. and Holtum, J.A.M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: Lewis Publishers.Google Scholar
Haughn, G. W. and Somerville, C. R. 1986. Sulfonylurea-resistant mutants of Arabidopsis thaliana . Mol. Gen. Genet. 204:430–434.Google Scholar
Haughn, G. W. and Somerville, C. R. 1987. Selection for herbicide resistance at the whole plant level. Pages 98–108 In Lebaron, H., Mumma, R. O., Honeycutt, R. C., and Duesing, J. H., eds. Applications of Biotechnology to Agricultural Chemistry. Washington, DC: Am. Chem. Soc.CrossRefGoogle Scholar
Haughn, G. W. and Somerville, C. R. 1990. A mutation causing imidazolinone resistance maps to the csr1 locus of Arabidopsis thaliana . Plant Physiol. 92:1081–1085.Google Scholar
Herrmann, K. M. 1995. The shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7:907–919.CrossRefGoogle ScholarPubMed
Höllander-Czytko, H. and Amrhein, N. 1983. Subcellular compartmentation of shikimic acid and phenylalanine in buckwheat cell suspension cultures grown in the presence of shikimate pathway inhibitors. Plant Sci. Lett. 29:89–96.Google Scholar
Holtum, J.A.M. and Powles, S. B. 1991. Annual ryegrass: an abundance of resistance, a plethora of mechanisms. Brighton Crop Protection Conf.—Weeds. Surrey, U.K. pp. 1071–1078.Google Scholar
Jones, J. D., Goldsbrough, P. B., and Weller, S. C. 1996. Stability and expression of amplified EPSPS genes in glyphosate resistant tobacco cells and plantlets. Plant Cell Rep. 15:431–436.Google Scholar
Lee, L. J. and Ngim, J. 2000. A first report of glyphosate-resistant goosegrass (Eleusine indica (L) Gaertn) in Malaysia. Pest. Manag. Sci. 56:336–339.3.0.CO;2-8>CrossRefGoogle Scholar
Marzabadi, M. R., Gruys, K. J., Pansegrau, P. D., Walker, M. C., Yuen, H. K., and Sikorski, J. A. 1996. An EPSP synthase inhibitor joining shikimate 3-phosphate with glyphosate: synthesis and ligand binding studies. Biochemistry 35:4199–4210.Google Scholar
Naylor, B. 1960. Species differentiation in the genus Lolium . Heredity 15:219–233.CrossRefGoogle Scholar
Padgette, S. R., Huynh, Q. K., Aykent, S., Sammons, R. D., Sikorski, J. A., and Kishore, G. M. 1988. Identification of the reactive cysteines of Escherichia coli 5-enolpyruvylshikimate-3-phosphate synthase and their nonessentiality for enzymatic catalysis. J. Biol. Chem. 263:1798–1802.CrossRefGoogle ScholarPubMed
Padgette, S. R., Re, D. B., Gasser, C. S., et al. 1991. Site-directed mutagenesis of a conserved region of the 5-enolpyruvylshikimate-3-phosphate synthase active site. J. Biol. Chem. 266:22 364–22 369.Google Scholar
Peschke, V. M. and Phillips, R. L. 1992. Genetic implications of somaclonal variation in plants. Adv. Genet. 30:41–75.CrossRefGoogle Scholar
Pinto, J.E.B.P., Dyer, W. E., Weller, S. C., and Herrmann, K. M. 1988. Glyphosate induces 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase in potato (Solanum tuberosum L.) cells grown in suspension culture. Plant Physiol. 87:891–893.CrossRefGoogle Scholar
Powles, S. B., Holtum, J.A.M., Matthews, J. M., and Liljegren, D. R. 1990. Herbicide cross-resistance in annual ryegrass (Lolium rigidum Gaud). ACS Symposium Series 421. Washington, DC: Am. Chem. Soc. pp. 394–406.Google Scholar
Powles, S. B., Lorraine-Colwill, D. F., Dellow, J. J., and Preston, C. 1998. Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed Sci. 46:604–607.Google Scholar
Powles, S. B. and Matthews, J. M. 1992. Multiple herbicide resistance in annual ryegrass (Lolium rigidum), the driving force for the adoption of integrated weed management. Pages 75–87 In Denholm, I., Devonshire, A., and Holloman, D., eds. Achievements and Developments in Combating Pest Resistance. London: Elsevier.Google Scholar
Pratley, J., Baines, P., Eberbach, P., Incerti, M., and Broster, J. 1996. Glyphosate resistance in annual ryegrass. Proc. 11th Annual Conf. Grasslands Society of New South Wales. 122 p.Google Scholar
Pratley, J. E., Urwin, N.A.R., Stanton, R. A., Baines, P. R., Broster, J. C., Cullis, K., Schafer, D. E., Bohn, J. A., and Krueger, R. W. 1999. Resistance to glyphosate in Lolium rigidum . I. Bioevaluation. Weed Sci. 47:405–411.Google Scholar
Preston, C., Tardif, F. J., and Powles, S. B. 1996. Multiple mechanisms and multiple herbicide resistance in Lolium rigidum . Pages 117–129 In Brown, T., ed. Molecular Genetics and Evolution of Pesticide Resistance. Washington, DC: Am. Chem. Soc.CrossRefGoogle Scholar
Saghai-Maroof, M. A., Soliman, K. M., Jorgensen, R. A., and Allard, R. W. 1984. Ribosomal DNA spacer-length polymorphisms in barley: Men-delian inheritance, chromosomal location, and population dynamics. Proc. Natl. Acad. Sci. USA 81:8014–8018.Google Scholar
Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 7.3–9.59.Google Scholar
Shah, D. M., Gasser, C. S., Della-Cioppa, G., and Kishore, G. M. 1988. Genetic engineering of herbicide resistance genes. Pages 297–309 In Verma, D. and Goldberg, R., eds. Plant Gene Research: Temporal and Spatial Regulation of Plant Genes. Volume 5. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Shah, D. M., Horsch, R. B., Klee, H. J., et al. 1986. Engineering herbicide tolerance in transgenic plants. Science 233:478–481.Google Scholar
Singh, B. K., and Shaner, D. L. 1998. Rapid determination of glyphosate injury to plants and identification of glyphosate-resistant plants. Weed Technol. 12:527–530.Google Scholar
Smith, K. A., Agarwal, M. L., Chernov, M. V., Chernova, O. B., Deguchi, Y., Ishizaka, Y., Patterson, T. E., Poupon, M. F., and Stark, G. R. 1995. Regulation and mechanisms of gene amplification. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 347:49–56.Google ScholarPubMed
Suh, H., Hepburn, A. G., Kriz, A. L., and Widholm, J. M. 1993. Structure of the amplified 5-enolpyruvylshikimate-3-phosphate synthase gene in glyphosate-resistant carrot cells. Plant Mol. Biol. 22:195–205.Google Scholar
Tran, M., Baerson, S. R., Brinker, R., et al. 1999. Characterization of glyphosate resistant Eleusine indica biotypes from Malaysia. Proc. 1 (B) 17th Asian-Pacific Weed Soc. Conf. pp. 527–536.Google Scholar
Westwood, J. H. and Weller, S. C. 1997. Cellular mechanisms influence differential glyphosate sensitivity in field bindweed (Convolvulus arvensis) biotypes. Weed Sci. 45:2–11.Google Scholar