Physiological mechanisms of glyphosate resistance

Weed Technology

Volumn 20, Issue 2, 2006, Pages 290-300

  Pline Srnic, Wendy ^a  

^a JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

Author keywords

EPSPS; Gene amplification; Glyphosate; Glyphosate N acetyl transferase; Glyphosate oxidoreductase; Herbicide metabolism; Herbicide resistance; Shikimate pathway

Indexed keywords

ADAPTATION; AMINO ACID; CROP; ENZYME; GENE; GLYPHOSATE; PESTICIDE RESISTANCE; PHYSIOLOGICAL RESPONSE;

AGROBACTERIUM; CONVOLVULUS; RHIZOBIUM;

EID: 33750295886     PISSN: 0890037X     EISSN: None     Source Type: Journal    
DOI: 10.1614/WT-04-131R.1     Document Type: Article

References (86)

1. Amrhein, N., D. Johanning, J. Schab, and A. Schulz. 1983. Biochemical basis for glyphosate tolerance in a bacterium and a plant tissue culture. FEBS Lett. 157:191-196.
2. Anonymous. 2003a. January 16. Summary Information Format. Roundup Ready Sugar Beet. According to Council Regulation 2002/812/EC: Web page: http://gmoinfo.jrc.it/csnifs/C-BE-99-01.pdf. Accessed: January 23, 2004.
3. Anonymous. 2003b. June 30. Acreage-Biotechnology Varieties. National Agricultural Statistics Service, Cr. Pr. 2-5: Web page: http://usda.mannlib. cornell.edu/reports/nassr/field/pcp-bba/acrg0603.pdf. Accessed: January 21, 2004.
4. Baerson, S. R., D. J. Rodriguez, M. Tran, Y. Feng, N. A. Best, and G. M. Dill. 2002. Glyphosate resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol. 129:1265-1275.
5. Barry, G., G. Kishore, M. Padgette, K. Kolacz, M. Weldon, D. Re, D. Eichholtz, K. Fincher, and L. Hallas. 1992. Inhibitors of amino acid biosynthesis: strategies for imparting glyphosate tolerance to crop plants. In B. K. Singh, H. E. Flores, and J. C. Shannon, eds. Biosynthesis and Molecular Regulation of Amino Acids in Plants. Rockville, MD: American Society of Plant Physiologists. Pp. 139-145.
6. Bradshaw, L. D., S. R. Padgette, S. L. Kimball, and B. H. Wells. 1997. Perspectives on glyphosate resistance. Weed Technol. 11:189-198.
7. Castle, L. A., D. Siehl, L. J. Giver, J. Minshull, C. Ivy, Y. H. Chen, and N. B. Duck, inventors; Maxygen, Inc. and Pioneer Hi-Bred International, Inc., assignees. 2002. Novel glyphosate N-acetyltransferase (GAT) genes. WO 02/36782. May 10, 2002.
8. Castle, L. A., D. L. Siehl, R. Gorton, et al. 2004. Discovery and directed evolution of a glyphosate tolerance gene. Science 304:1151-1154.
9. Comai, L., L. Sen, and D. M. Stalker. 1983. An altered aroA gene product confers resistance to the herbicide glyphosate. Science 221:370-371.
10. Comai, L., D. D. Facciotti, W. R. Hiatt, G. Thompson, R. E. Rose, and D. M. Stalker. 1985. Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature 317:741-744.
11. Cresswell, R. C., M. W. Fowler, and A. H. Scragg. 1988. Glyphosate tolerance in Catharanthus roseus. Plant Sci. 54:55-63.
12. Dams, T. R., P. C. Anderson, R. J. Daines, W. J. Gordon-Kamm, A. P. Kausch, C. J. Mackey, E. M. Orozco, P. M. Orr, and M. A. Stephens, inventors; Dekalb Genetics Corporation, assignee. 1995. Fertile, transgenic maize plants and methods for their production. World patent WO 95/06128. March 2, 1995.
13. Delannay, X., T. T. Bauman, D. H. Beighley, et al. 1995. Yield evaluation of a glyphosate-tolerant soybean line after treatment with glyphosate. Crop Sci. 35:1461-1467.
14. Dröge, W., I. Bröer, and A. Puhler. 1992. Transgenic plants containing the phosphinothricin-N-acetyltransferase gene metabolize the herbicide L-phosphinothricin (glufosinate) differently from untransformed plants. Planta 187:142-151.
15. Duke, S. O., A. M. Rimando, P. F. Pace, K. N. Reddy, and R. J. Smeda. 2003. Isoflavone, glyphosate, and aminomethylphosphonic acid levels in seeds of glyphosate-treated, glyphosate-resistant soybean. J. Agric. Food Chem. 51:340-344.
16. Dyer, W. E., S. C. Weller, R. A. Bressan, and K. M. Herrmann. 1988. Glyphosate tolerance in tobacco (Nicotiana tabacum L.). Plant Physiol. 88:661-666.
17. Elmore, R. W., F. W. Roeth, R. N. Klein, S. Z. Knezevic, A. Martin, L. A. Nelson, and C. A. Shapiro. 2001. Glyphosate-resistant soybean cultivar response to glyphosate. Agron. J. 93:404-407.
18. Fillatti, J. J., J. Kiser, R. Rose, and L. Comai. 1987. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Biotechnology 5:726-730.
19. Forlani, G., B. Nielsen, and M. L. Racchi. 1992. A glyphosate-resistant 5-enol-pyruvyl-shikimate-3-phosphate synthase confers tolerance to a maize cell line. Plant Sci. 85:9-15.
20. Franz, J. E., M. K. Mao, J. A. Sikorski. 1997. Uptake, transport and metabolism of glyphosate in plants. In Franz, J. E., M. K. Mao, and J. A. Sikorski, eds. Glyphosate: A Unique Global Herbicide. ACS Monogr. 189:143-181.
21. Gasser, C. S., J. A. Winter, C. M. Hironaka, and D. M. Shah. 1988. Structure, expression, and evolution of the 5-enolpyruvylshikimate-3-phosphate synthase genes of petunia and tomato. J. Biol. Chem. 263:4280-4289.
22. Geiger, D. R. and H. D. Bestman. 1990. Self-limitation of herbicide mobility by phytotoxic action. Weed Sci. 38:324-329.
23. Goldsbrough, P. B., E. M. Hatch, B. Huang, W. G. Kosinsky, W. E. Dyer, K. M. Herrmann, and S. C. Weller. 1990. Gene amplification in glyphosate tolerant tobacco cells. Plant Sci. 72:53-62.
24. Gorlach, J., J. Schmid, and N. Amrhein. 1994. Abundance of transcripts specific for genes encoding enzymes of the prechorismate pathway in different organs of tomato (Lycopersion esculentum L.) plants. Planta 193:216-223.
25. Gougler, J. A. and D. R. Geiger. 1981. Uptake and distribution of N-phosphonomethylglycine in sugarbeet plants. Plant Physiol. 68:668-672.
26. Gower, S. A., M. M. Loux, J. Cardina, and S. K. Harrison. 2002. Effect of planting date, residual herbicide, and postemergence application timing on weed control and grain yield in glyphosate-tolerant corn (Zea mays). Weed Technol. 16:488-494.
27. Gower, S. A., M. M. Loux, J. Cardina, et al. 2003. Effect of postemergence glyphosate application timing on weed control and grain yield in glyphosate-resistant corn: results of a 2-yr multistate study. Weed Technol. 17:821-828.
28. Hauptman, P. M., G. della-Cioppa, A. G. Smith, G. M. Kishore, J. M. Widholm. 1988. Expression of glyphosate resistance in carrot somatic hybrid cells through the transfer of an amplified 5-enolpyruvylshikimate-3-phosphate synthase gene. Mol. Gen. Genet. 211:357-363.
29. He, M., Y. F. Nie, and P. Xu. 2003. A T42M substitution in bacterial 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) generates enzymes with increased resistance to glyphosate. Biosci. Biotechnol. Biochem. 67:1405-1409.
30. He, M., Z. Y. Yang, Y. F. Nie, J. Wang, and P. Xu. 2001. A new type of class 1 bacterial 5-enopyruvylshikimate-3-phosphate synthase mutants with enhanced tolerance to glyphosate. Biochim. Biophys. Acta 1568:1-6.
31. Hoagland, R. E. 1980. Effects of glyphosate on metabolism of phenolic compounds: VI. Effects of glyphosine and glyphosate metabolites on phenylalanine ammonia-lyase activity, growth, and protein, chlorophyll, and anthocyanin levels in soybean (Glycine max) seedlings. Weed Sci. 28:393-400.
32. Holländer-Czytko, H., D. Johanning, H. E. Meyer, and N. Amrhein. 1988. Molecular basis for the overproduction of 5-enolpyruvylshikimate-3- phosphate synthase in a glyphosate-tolerant cell suspension culture of Corydalis sempervirens. Plant Mol. Biol. 11:215-220.
33. Holländer-Czytko, H., I. Sommer, and N. Amrhein. 1992. Glyphosate tolerance of cultured Corydalis sempervirens cells is acquired by an increased rate of transcription of 5-enolpyruvylshikimate 3-phosphate synthase as well as a reduced turnover of the enzyme. Plant Mol. Biol. 20:1029-1036.
34. Jones, M. A. and C. E. Snipes. 1999. Tolerance of transgenic cotton to topical application of glyphosate. J. Cotton Sci. 3:19-26.
35. Kishore, G. M., L. Brundage, K. Kolk, S. R. Padgette, D. Rochester, K. Huynh, and G. della-Cioppa. 1986. Isolation, purification and characterization of a glyphosate tolerant mutant E. coli EPSP synthase. Fed. Proc. 45:1506.
36. Kishore, G. M. and G. S. Jacob. 1987. Degradation of glyphosate by Pseudomonas sp. PG2982 via a sarcosine intermediate. J. Biol. Chem. 262:12164-12168.
37. Klee, H. J., Y. M. Muskopf, and C. S. Gasser. 1987. Cloning of an Arabidopsis thaliana gene encoding 5-enolpyruvylshikimate-3-phosphate synthase: sequence analysis and manipulation to obtain glyphosate-tolerant plants. Mol. Gen. Genet. 210:437-442.
38. Komossa, D., I. Gennity, and H. Sandermann. 1992. Plant metabolism of herbicides with C-P bonds: glyphosate. Pestic. Biochem. Physiol. 43:85-94.
39. Lebrun, M., A. Sailland, and G. Freyssinet, inventors: Rhone-Poulenc Agrochimie, assignee. 1997. Mutated 5-enol pyruvylshikimate-3-phosphate synthase, gene coding for said protein and transformed plants containing said gene. World patent application WO9704103. February 6, 1997.
40. Lebrun, M., A. Sailland, G. Freyssinet, E. Degryse, inventors; Bayer Crop Science S.A., assignee. 2003. Mutated 5-enolpyruvylshikimate-3-phosphate synthase, gene coding for said protein and transformed plants containing said gene. U.S. patent 6,566,587. May 20, 2003.
41. Light, G. G., T. A. Bauman, P. A. Dotray, J. W. Keeling, and D. B. Wester. 2003. Yield of glyphosate-tolerant cotton as affected by topical glyphosate applications on the Texas High Plains and Rolling Plains. J. Cotton Sci. 7:231-235.
42. Malik, J., G. Barry, and G. Kishore. 1989. The herbicide glyphosate. Biofactors 2:17-25.
43. Mannerlöf, M., S. Tuvesson, P. Steen, and P. Tenning. 1997. Transgenic sugar beet tolerant to glyphosate. Euphytica. 94:83-91.
44. 2-labeled photoassimilates in Canada thistle (Cirsium arvense). Weed Sci. 33:153-159.
45. Moore, J. K., H. D. Braymer, and A. D. Larson. 1983. Isolation of a Pseudomonas sp. which utilizes the phosphonate herbicide glyphosate. Appl. Environ. Microbiol. 46:316-320.
46. Murata, M., J.-H. Ryu, S. Caretto, D. Rao, H.-S. Song, J. M. Widholm. 1998. Stability and culture limitations of gene amplification in glyphosate resistant carrot cell lines. J. Plant Physiol. 152:112-117.
47. Nafziger, E. D., J. M. Widholm, H. C. Steinrucken, and J. L. Killmer. 1984. Selection and characterization of a carrot cell line tolerant to glyphosate. Plant Physiol. 76:571-574.
48. Nap, J. P., P.L.J. Metz, M. Escaler, and A. J. Conner. 2003. The release of genetically modified crops into the environment. Part I. Overview of current status and regulations. Plant J. 33:1-18.
49. Nida, D. L., K. H. Kolacz, R. E. Buehler, et al. 1996. Glyphosate-tolerant cotton: genetic characterization and protein expression. J. Agric. Food Chem. 44:1960-1966.
50. Odell, J. T., F. Nagy, and N.-H. Chua. 1985. Identification of DNA sequences required for activity of the Cauliflower Mosaic Virus 35S promoter. Nature 313:810-812.
51. Padgette, S. R., K. H. Kolacz, X. Delannay, et al. 1995. Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci. 35:1451-1461.
52. Padgette, S. R., D. B. Re, G. F. Barry, D. E. Eichholtz, X. Delannay, R. L. Fuchs, G. M. Kishore, and R. T. Fraley. 1996. New weed control opportunities: development of soybeans with a Roundup Ready gene. In S. O. Duke, ed. Herbicide-Resistant Crops: Agricultural, Economic, Environmental, Regulatory, and Technological Aspects. Boca RaUm, FL: CRC. Pp. 53-84.
53. Padgette, S. R., D. B. Re, C. S. Gasser, et al. 1991. Site-directed mutagenesis of a conserved region of the 5-enolpyruvylshikimate-3-phosphate synthase active site. J. Biol. Chem. 266:22364-22369.
54. Papanikou, E., J. E. Brotherton, and J. M. Widholm. 2004. Length of time in tissue culture can affect the selected glyphosate resistance mechanism. Planta 218:589-598.
55. Pline, W. A., A. J. Price, J. W. Wilcut, K. L. Edmisten, and R. Wells. 2001. Absorption and translocation of glyphosate in glyphosate-resistant cotton as influenced by application method and growth stage. Weed Sci. 49:460-467.
56. Pline, W. A., R. Viator, J. W. Wilcut, K. L. Edmisten, J. Thomas, R. Wells. 2002. Reproductive abnormalities in glyphosate-resistant cotton caused by lower CP4-EPSPS levels in the male reproductive tissue. Weed Sci. 50:438-447.
57. Reddy, K. N., A. M. Rimando, and S. O. Duke. 2004. Is aminomethylphosphonic acid, a metabolite of glyphosate, causing injury in glyphosate-treated glyphosate-resistant soybean? WSSA Abstr. 44:116.
58. Reinbothe, S., A. Nelles, and B. Partbier. 1991. N-(phosphonomethyl) glycine (glyphosate) tolerance in Euglena gracilis acquired by either overproduced or resistant 5-enolpyruvyl shikimate-3-phosphate synthase. Eur. J. Biochem. 198:365-373.
59. Rubin, J. L., C. G. Gaines, and R. A. Jensen. 1984. Glyphosate inhibition of 5-enolpyruvylshikimate 3-phosphate synthase from suspension-cultured cells of Nicotiana silvestris. Plant Physiol. 75:839-845.
60. Rueppel, M. L., B. B. Brightwell, J. Schaefer, and J. T. Marvel. 1977. Metabolism and degradation of glyphosate in soil and water. J. Agric. Food Chem. 25:517-528.
61. Ruff, T. D. Eichholtz, D. Re, S. Padgette, and G. Kishore. 1991. Effects of amino acid substitutions on glyphosate tolerance and activity of EPSPS. Plant Physiol. 96(Suppl.):94.
62. 14C-glyphosate in several weed species. Weed Res. 20:195-200.
63. Sellin, C., G. Forlani, J. Dubois, E. Nielsen, and J. Vasseur. 1992. Glyphosate tolerance in Cichorium intybus L. var. Magdebourg. Plant Sci. 85:223-231.
64. Shah, D. M., R. B. Horsch, H. J. Klee, et al. 1986. Engineering herbicide tolerance in transgenic plants. Science 233:478-481.
65. Shyr, Y.Y.J., A. G. Hepburn. and J. M. Widholm. 1992. Glyphosate selected amplification of the 5-enolpyruvylshikimate-3-phosphate synthase gene in cultured carrot cells. Mol. Gen. Genet. 232:377-382.
66. Singer, S. R. and C. N. McDaniel. 1985. Selection of glyphosate-tolerant tobacco calli and the expression of this tolerance in regenerated plants. Plant Physiol. 78:411-416.
67. Smart, C. C., D. Johanning, G. Muller, and N. Amrhein. 1985. Selective over-production of 5-enol-pyruvylshikimic acid 3-phosphate synthase in a plant cell culture which tolerates high doses of the herbicide glyphosate. J. Biol. Chem. 260:16338-16346.
68. Smith, C. M., D. Pratt, and G. A. Thompson. 1986. Increased 5-enolpyruvylshikimic acid 3-phosphate synthase activity in a glyphosate-tolerant variant strain of tomato cells. Plant Cell Rep. 5:298-301.
69. Sost, D. and N. Amrhein. 1990. Substitution of Gly-96 to Ala in the 5-enolpyruvylshikimate-3-phosphate synthase of Klebsiella pneumoniae results in a greatly reduced affinity for the herbicide glyphosate. Arch. Biochem. Biophys. 282:433-436.
70. Sost, D., A. Schulz, and N. Amrhein. 1984. Characterization of a glyphosate-insensitive 5-enolpyruvyl-shikimic acid-3-phosphate synthase. FEBS Lett. 173:238-242.
71. Stalker, D. M., W. R. Hiatt, and L. Comai. 1985. A single amino acid substitution in the enzyme 5-enolpyruvylshikimate-3-phosphate synthase confers resistance to the herbicide glyphosate. J. Biol. Chem. 260:4724-4728.
72. Steinrucken, H. C., A. Schulz, N. Amrhein, C. A. Porter, and R. T. Fraley. 1986. Overproduction of 5-enolpyruvyl-shikimate 3-phosphate synthase in a glyphosate-tolerant Petunia hybrida cell line. Arch. Biochem. Biophys. 244:169-178.
73. Suh, H., A. G. Hepburn, A. L. Kriz, and J. M. Widholm. 1993. Structure of the amplified 5-enolpyruvylshikimate-3-phosphate synthase gene in glyphosate resistant carrot cells. Plant Mol. Biol. 22:195-205.
74. Tharp, B. E. and J. J. Kells. 1999. Influence of herbicide application rate, timing, and interrow cultivation on weed control and corn (Zea mays) yield in glufosinate-resistant and glyphosate-resistant corn. Weed Technol. 13:807-813.
75. Thompson, C. J., R. N. Movva, R. Tizard, R. Crameri, J. E. Davies, M. Lauwereys, and J. Botterman. 1987a. Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J. 9:2519-2523.
76. Thompson, G. A., W. R. Hiatt, D. Gacciotti, D. M. Stalker, and L. Comai. 1987b. Expression in plants of a bacterial gene coding for glyphosate resistance. Weed Sci. 35(Suppl. 1):19-23.
77. Torstensson, L. 1985. Behavior of glyphosate in soils and its degradation. In E. Grossbard and D. Atkinson, eds. The Herbicide Glyphosate. London: Butterworth. Pp. 137-150.
78. Torstensson, N.T.L. and A. Aamisepp. 1977. Detoxification of glyphosate in soil. Weed Res. 17:209-212.
79. Wang, H. Y., Y. F. Li, L. X. Xie, and P. Xu. 2003. Expression of a bacterial aroA mutant, aroA-M1, encoding 5-enolpyruvylshikimate-3-phosphate synthase for the production of glyphosate-resistant tobacco plants. J. Plant Res. 116:455-460.
80. Wang, Y. X., J. D. Jones, S. C. Weller, and P. B. Goldsbrough. 1991. Expression and stability of amplified genes encoding 5-enolpyruvylshikimate-3- phosphate synthase in glyphosate-tolerant tobacco cells. Plant Mol Biol. 17:1127-1138.
81. Warner, S.A.J., T. R. Hawkes, and C. J. Andrews, inventors; Syngenta Limited, assignee. 2002. Herbicide Resistant Plants. WO 02/26995. April 4, 2002.
82. Weaver, L. M. and K. M. Herrmann. 1997. Dynamics of the shikimate pathway in plants. Trends Plant Sci. 2:346-351.
83. Westwood, J. H. and S. C. Weller. 1997. Cellular mechanisms influence differential glyphosate sensitivity in field bindweed (Convolvulus arvensis) biotypes. Weed Sci. 45:2-11.
84. Widholm, J. M., A. R. Chinnala, J. Ryu, H. Song, T. Eggetta, and J. E. Brothertona. 2001. Glyphosate selection of gene amplification in suspension cultures of 3 plant species. Physiol. Plant. 112:540-545.
85. Wyrill, J. B. and O. C. Burnside. 1976. Absorption, translocation, and metabolism of 2,4-D and glyphosate in common milkweed and hemp dogbane. Weed Sci. 24:557-566.
86. Zhou, H., J. W. Arrowsmith, M. E. Fromm, et al. 1995. Glyphosate-tolerant CP4 and GOX genes as a selectable marker in wheat transformation. Plant Cell Rep. 15:159-163.