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History of Herbicide-Tolerant Crops, Methods of Development and Current State of the Art – Emphasis on Glyphosate Tolerance

Published online by Cambridge University Press:  12 June 2017

Ganesh M. Kishore
Affiliation:
Sr. Res. Spec., Plant Prot. and Improve
Stephen R. Padgette
Affiliation:
Sr. Res. Spec., Plant Prot. and Improve
Robert T. Fraley
Affiliation:
Agricultural Group of Monsanto Company, 700 Chesterfield Village Parkway, St. Louis, MO 63198

Abstract

Weed management is an integral part of agriculture; weeds lower both productivity and quality of agricultural products. A combination of mechanical, chemical, biological, and cultural methods is expected to deliver a sustainable weed management program for the next two decades. While chemical methods offer the most cost effective means of weed management, crop selectivity has hampered the use of the best chemicals for weed management. Recent progress in gene technology has facilitated the introduction and expression of genes to confer a wide range of traits to crop plants. Application of this technology has resulted in the development of crop plant genotypes that are resistant to a specific herbicide. This article describes the progress that has been made by our group toward the introduction of glyphosate tolerance to crop plants. Glyphosate [N-(phosphonomethyl)glycine] kills plants due to inhibition of the biosynthesis of aromatic compounds via the shikimate pathway. Our approach for introduction of glyphosate tolerance is based on insertion and expression in plants of a gene encoding a glyphosate-tolerant 5-enolpyruvylshikimate-3-phosphate (EPSP) synthase, a key enzyme of the shikimate pathway. The wild type enzyme present in plants is susceptible to inhibition glyphosate; variants of EPSP synthase have been produced that are less susceptible to inhibition by glyphosate. Expression of genes encoding these variants has been shown to confer glyphosate tolerance to plants. The degree of glyphosate tolerance is related to the tolerance characteristics of the EPSP synthase variant, its substrate activity, targeting to the plastid, and the level of expression of the variant gene. The tissue specificity of expression of the variant EPSP synthase has also been shown to be critical since glyphosate is a systemic herbicide and is translocated to many growing points within the plant. Our studies on glyphosate tolerance have substantially enhanced our understanding of the mode-of-action of glyphosate, the shikimate pathway, and protein sorting within plant cells, as well as developmental and tissue specific expression of genes in plants. Commercial use of glyphosate tolerance technology is expected to affect positively, the weed management arsenal available to the farmers, the sustainability of farm land and groundwater, and promote the use of a “soft” herbicide.

Type
Symposium
Copyright
Copyright © 1990 by the Weed Science Society of America 

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References

Literature Cited

1. Amrhein, N., Deus, B., Gehrke, P., and Steinrucken, H. 1980. The site of inhibition of the shikimate pathway by glyphosate. Plant Physiol. 66:830834.Google Scholar
2. Anderson, P. and Georgeson, M. 1989. Herbicide-tolerant mutants of corn. Genome 31:994999.Google Scholar
3. Ayotte, R., Harney, P., and Sousa Machado, M. V. 1989. The transfer of triazine resistance from Brassica napus L. to B. oleracea L. IV. Second and third backcrosses to B. oleracea and recovery of an 18-chromosome, triazine resistant BC3 . Euphytica 40:1519.Google Scholar
4. Baird, D., Upchurch, R., Homesley, W., and Franz, J. 1971. Introduction of a new broad spectrum postemergence herbicide class with utility for herbaceous perennial weed control. Proc. North Cent. Weed Control Conf. 26:6468.Google Scholar
5. Barrantine, W., Edwards, C. Jr., and Hartwid, E. 1975. Soybean cultivar response to metribuzin. Abstr. Weed Sci. Soc. Am. p. 8.Google Scholar
6. Bickel, H., Palme, L., and Schultz, G. 1978. Incorporation of shikimate and other precursors into aromatic amino acids and prenylquinones of isolated spinach chloroplasts. Phytochemistry 17:199–124.Google Scholar
7. Böger, P. and Sandmann, G. 1989. Target Sites of Herbicide Action. CRC Press, Boca Raton, FL.Google Scholar
8. Boocock, M. and Coggins, J. 1983. FEBS Lett. 154:127133.Google Scholar
9. Brown, H., Wittenbach, V., Forney, D., and Strachan, S. 1990. Basis for sulfonylurea tolerance to thifensulfuron methyl. Pestic. Biochem. Physiol. 37:303313.CrossRefGoogle Scholar
10. Christou, P., McCabe, D., and Swain, W. 1988. Stable transformation of soybean callus by DNA-coated particles. Plant Physiol. 87:671674.Google Scholar
11. Comai, L., Facciotti, D., Hiatt, W., Thompson, G., Rose, R., and Stalker, D. 1985. Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature (London) 317:741744.Google Scholar
12. Comai, L., Sen, L., and Stalker, D. 1983. An altered aroA gene product confers resistance to the herbicide glyphosate. Science 221:370371.Google Scholar
13. De Block, M, De Brower, D., and Tenning, P. 1988. Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in transgenic plants. Plant Physiol. 9:694701.Google Scholar
14. della-Cioppa, G. and Kishore, G. 1988. Import of a precursor protein into chloroplasts is inhibited by the herbicide glyphosate. EMBO J. 7:12991305.CrossRefGoogle ScholarPubMed
15. della-Cioppa, G., Hauptman, R., Fraley, R., and Kishore, G. 1986. Overproduction of 5-enolpyruvylshikimate 3-phosphate synthase in plastids of Petunia hybrida suspension culture cells confers resistance to the herbicide glyphosate. Curr. Top. Plant Biochem. Physiol. 5:194.Google Scholar
16. della-Cioppa, G., Bauer, S., Klein, B., Shah, D., Fraley, R., and Kishore, G. 1986. Translocation of the precursor of 5-enolpyruvylshikimate 3-phosphate synthase into chloroplasts of higher plants in vitro. Proc. Nat. Acad. Sci. USA 83:68736877.CrossRefGoogle Scholar
17. della-Cioppa, G., Bauer, S., Taylor, M., Rochester, D., Klein, B., Shah, D., Fraley, R., and Kishore, G. 1987. Targeting a herbicide-resistant enzyme from Escherichia coli to chloroplasts of higher plants. Bio/Technology 5:579584.Google Scholar
18. Fromm, M., Morrish, F., Armstrong, C., Williams, R., Thomas, J., and Klein, T. 1990. Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. Bio/Technology 8:833839.Google Scholar
19. Goodman, , Hauptli, R. H., Crossway, A., and Knauf, V. 1987. Gene transfer in crop improvement. Science 236:4854.CrossRefGoogle ScholarPubMed
20. Gordon-Kamm, W., Spencer, T., Mangano, M., Adams, T., Daines, R., Start, W., O'Brien, J., Chambers, S., Adams, W. Jr., Willetts, N., Rice, H., Mackey, C., Krueg, R., Kausch, A., and Lemaux, P. 1990. Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2:603618.CrossRefGoogle ScholarPubMed
21. Harms, C., Montoya, A., Privalle, L., and Briggs, R. 1990. Genetic and biochemical characterization of corn inbred lines tolerant to the sulfonylurea herbicide primisulfuron. Theor. Appl. Genet. 80:353358.Google Scholar
22. Haughn, G., Smith, J., Mazur, B., and Somerville, C. 1988. Transformation with a mutant Arabidopsis acetolactate synthase gene renders tobacco resistant to sulfonylurea herbicides. Mol. Gen. Genet. 211:266271.CrossRefGoogle Scholar
23. Hollander, H. and Amrhein, N. 1980. The site of the inhibition of the shikimate pathway by glyphosate. Plant Physiol. 66:23829.Google Scholar
24. Kishore, G. and Shah, D. 1988. Amino acid biosynthesis inhibitors as herbicides. Annu. Rev. Biochem. 57:627663.Google Scholar
25. Kishore, G. and Shah, D. 1990. Glyphosate tolerant 5-enolpyruvyl 3-phosphoshikimate synthase. U.S. Patent 4,971,908.Google Scholar
26. Kishore, G., Brundage, L., Kolk, K., Padgette, S., Rochester, D., Huynh, Q., and della-Cioppa, G. 1986. Isolation, purification and characterization of a glyphosate tolerant mutant E. coli EPSP synthase. Fed. Proc. 456:1506.Google Scholar
27. Klee, H., and Rogers, S. 1989. Plant gene vectors and genetic transformation: plant transformation systems based on the use of Agrobacterium tumefaciens . p. 220 in Schell, J. and Vasil, I. K., eds. Cell Culture and Somatic Cell Genetics of Plants, Vol. 6, Academic Press, Inc., New York.Google Scholar
28. Maltais, B. and Bouchard, C. 1987. Une moutarde des osiearux (Brassica rapa L.) resistantes a l'atrazine. Phytoprotection 59:117119.Google Scholar
29. Miki, B., Labbe, , Hattori, H., Ouellet, T., Gabard, J., Sunohara, G., Charest, P., and Iyer, V. 1990. Transformation of Brassic napus canola cultivars with Arabidopsis thaliana acetohydroxyacid synthase genes and analysis of herbicide resistance. Theor. Appl. Genet. 80:449458.Google Scholar
30. Mousdale, D. and Coggins, J. 1985. Subcellular localization of the common shikimate pathway enzymes in Pisum sativum L. Planta 163:241249.CrossRefGoogle ScholarPubMed
31. Padgette, S., della-Cioppa, G., Shah, D., Fraley, R., and Kishore, G. 1989. Selective herbicide tolerance through protein engineering. p. 441475 in Schell, J. and Vasil, I. K., eds. Cell Culture and Somatic Cell Genetics. Academic Press, New York.Google Scholar
32. Potrykus, I. 1990. Gene transfer to cereals: An assessment. Bio/Technology 8:535542.Google Scholar
33. Rogers, S., Brand, L., Holder, S., Sharps, E., and Brackin, M. 1983. Amplification of the aroA gene from Escherichia coli results in tolerance to the herbicide glyphosate. Appl. Environ. Microbiol. 46:3743.Google Scholar
34. Schultz, G., Bickel, H., Buchholz, B., and Soll, J. 1981. The plastidic shikimate pathway and its role in the synthesis of plastoquinone-9, alpha-tocopheroi and phylloquinone in spinach chloroplasts. p. 311318 in Akoyunoglou, G., ed. Photosynthesis. Balaban Int. Sci. Serv., Philadelphia, PA.Google Scholar
35. Schulz, A., Kruper, A., and Amrhein, N. 1985. Differential sensitivity of bacterial 5-enolpyruvylshikimate 3-phosphate synthases to the herbicide glyphosate. FEMS Microbiol. Lett. 28:297301.Google Scholar
36. Schulz, A., Wengenmayer, F., and Goodman, H. 1990. Genetic engineering of herbicide resistance in plants. p. 115 in Conger, B. V. ed., Crit. Rev. Plant Sci., Boca Raton, Florida.Google Scholar
37. Sebastian, S., Fader, G., Ulrich, J., Forney, D., and Chaleff, R. 1989. Semidominant soybean mutation for resistance to sulfonylurea herbicides. Crop Sci. 29:14031408.Google Scholar
38. Shah, D., Horsch, R., Klee, H., Kishore, G., Winter, J., Turner, N., Hironaka, C., Sanders, P., Gasser, C., Aykent, S., Siegel, N., Rogers, S., and Fral, R. Engineering herbicide tolerance in transgenic plants. Science 233478481.Google Scholar
39. Shimamoto, K., Terada, R., Izawa, T., and Fujimoto, H. 1989. Fertile transgenic rice plants regenerated from transformed protoplasts. Nature 338:274276.Google Scholar
40. Sost, D., Schulz, A., and Amrhein, N. 1984. Characterization of glyphosate-insensitive 5-enolpyruvylshikimic acid 3-phosphate synthase. FEBS Lett. 173238242.CrossRefGoogle Scholar
41. Sost, D. and Amrhein, N. 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. 282:433436.Google Scholar
42. Stalker, D., McBride, K., and Malyj, L. 1988. Herbicide resistance in transgenic plants expressing a bacterial detoxification gene. Science 242:419423.Google Scholar
43. Steinrucken, H., Schulz, A., Amrhein, N., Porter, C., and Fraley, R. 1986. Overproduction of 5-enolpyruvylshikimate 3-phosphate synthase in a glyphosate-tolerant Petunia hybrida cell line. Arch. Biochem. Biophys. 244:169178.Google Scholar
44. Steinrucken, H. and Amrhein, N. 1980. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimate acid 3-phosphate synthase. Biochem. Biophys. Res. Commun. 94:12071212.CrossRefGoogle Scholar
45. Swanson, E., Herrgesell, M., Arnolodo, M., Sippell, D., and Wong, R. 1989. Microspore mutagenesis and selection: canola plants with field tolerance to imidazolinones. Theor. Appl. Genet. 78:525530.Google Scholar
46. Vasil, I. 1990. Transgenic cereals becoming a reality. Bio/Technology 8:797.Google Scholar