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Biochemical mechanism and molecular basis for ALS-inhibiting herbicide resistance in sugarbeet (Beta vulgaris) somatic cell selections

Published online by Cambridge University Press:  12 June 2017

Terry R. Wright
Affiliation:
Department of Crop and Soil Sciences, Michigan State University, East Lansing, MI 48824-1325
Newell F. Bascomb
Affiliation:
American Cyanamid, Agricultural Products Research Division, Princeton, NJ 08543-0400
Stephen F. Sturner
Affiliation:
American Cyanamid, Agricultural Products Research Division, Princeton, NJ 08543-0400
Donald Penner*
Affiliation:
Department of Crop and Soil Sciences, Michigan State University, East Lansing, MI 48824-1325
*
Corresponding author. pennerd@pilot.msu.edu

Abstract

Three sugarbeet selections differing in cross-resistance to three classes of acetolactate synthase (ALS)-inhibiting herbicides have been developed using somatic cell selection. Sugarbeet selections resistant to imidazolinone herbicides, Sir-13 and 93R30B, do not metabolize [14C]-imazethapyr any faster or differently than sensitive, wild-type sugarbeets or a sulfonylurea-resistant/imidazolinone-sensitive selection, Sur. ALS specific activity from the three herbicide-resistant selections ranged from 73 to 93% of the wild-type enzyme extracts in the absence of herbicide, indicating enzyme overexpression was not a factor in resistance. Acetolactate synthase from Sir-13 plants showed a 40-fold resistance to imazethapyr but no resistance to chlorsulfuron or flumetsulam. Polymerase chain reaction amplification and sequencing of two regions of the ALS gene spanning all known sites for ALS-based herbicide resistance in plants indicated a single nucleotide change in the Sir-13 gene (G337 to A337) resulting in a deduced substitution of threonine for alanine at position 113 in the sugarbeet amino acid sequence. Sur ALS was not significantly resistant to imazethapyr, but was 1,000- and 50-fold resistant to chlorsulfuron and flumetsulam, respectively. Sur gene sequencing indicated a single nucleotide change (C562 to T562) resulting in a serine for proline substitution at position 188 of the ALS primary structure. The 93R30B nucleotide sequence indicated two mutations resulting in two deduced amino acid substitutions: threonine for alanine at position 113 plus serine for proline at position 188. The 93R30B double mutant incorporated the changes observed in each of the single mutants above and correlated with higher resistance levels to imazethapyr (> 1,000-fold), chlorsulfuron (4,300-fold), and flumetsulam (200-fold) at the ALS level than observed in either of the single mutants. 93R30B represents the first double mutant derived by a two-step selection process that incorporates two class-specific ALS-inhibitor resistance mutations to form a single broad cross-resistance trait. The interaction of the two altered amino acids is synergistic with respect to enzyme resistance vs. the resistance afforded by each of the individual mutations.

Type
Physiology, Chemistry, and Biochemistry
Copyright
Copyright © 1998 by the Weed Science Society of America 

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References

Literature Cited

Anderson, P. C. and Georgeson, M. 1989. Herbicide-tolerant mutants of corn. Genome 31: 994999.Google Scholar
Anonymous. 1991. Preparation of genomic DNA from plant tissue. Pages 2.3.12.3.3 in Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., eds. Current Protocols in Molecular Biology. New York: J. Wiley.Google Scholar
Bedbrook, J. R., Chaleff, R. S., Falco, S. C., Mazur, B. J., Somerville, C. R., and Yadev, N. S. 1995. Nucleic acid fragment encoding herbicide resistant plant acetolactate synthase. US patent 5,378,824. Jan. 3.Google 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
Bradford, M. M. 1976. A rapid and scnsative method of the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72: 248254.Google Scholar
Bright, S.W.J., Ming, T., Evans, I. J., and MacDonald, M. J. 1992. Herbicide resistant plants. World patent WO92/08794. May 29.Google Scholar
Caretto, S., Giardina, M. C., Nicolodi, C., and Mariotti, D. 1994. Chlorsulfuron resistance in Daucus carota cell lines and plants: involvement of gene amplification. Theor. Appl. Genet. 88: 520524.CrossRefGoogle ScholarPubMed
Creason, G. L. and Chaleff, R. S. 1988. A second mutation enhances resistance of a tobacco mutant to sulfonylurea herbicides. Theor. Appl. Genet. 76: 177182.Google Scholar
D'Halluin, K. M., Bossut, M., Bonne, E., Mazur, B., Leemans, J., and Botterman, J. 1992. Transformation of sugarbeet (Beta vulgaris L.) and evaluation of herbicide resistance in transgenic plants. Bio/Technology 10: 309314.Google Scholar
Dietrich, G.E. 1992. Imidazolinone resistant AHAS mutations. European patent application EP0525384A2.Google Scholar
Donn, G., Tischer, E., Smith, J. A., and Goodman, H. M. 1984. Herbicideresistant alfalfa cells: an example of gene amplification in plants. J. Mol. Appl. Genet. 2: 621635.Google Scholar
Gerwick, B. C., Subramanian, M. V., and Loney-Gallant, V. I. 1990. Mechanism of action of the 1,2,4-triazolo[1,5-a]pyrimidines. Pestic. Sci. 29: 357364.Google Scholar
Grula, J. W., Hudspeth, R. L., Hobbs, S. L., and Anderson, D. M. 1995. Organization, inheritance and expression of acetohydroxyacid synthase genes in the cotton allotetraploid Gossypium hirsutum . Plant Mol. Biol. 28: 837846.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
Harms, C. T., Armour, S. L., DiMaio, J. J., et al. 1992. Herbicide resistance due to amplification of a mutant acetohydroxyacid synthase gene. Mol. Gen. Genet. 233: 427435.Google Scholar
Hart, S. E., Saunders, J. W., and Penner, D. 1992. Chlorsulfuron-resistant sugarbeet'. cross resistance and physiological basis of resistance. Weed Sci. 40: 378383.Google Scholar
Hart, S. E., Saunders, J. W., and Penner, D. 1993. Semidominant nature of monogenic sulfonylurea herbicide resistance in sugarbeet (Beta vulgaris). Weed Sci. 41: 317324.Google Scholar
Hattori, J., Brown, D., Mourad, G., Labbe, H., Ouellet, T., Sunohara, G., Rutledge, R., King, J., and Miki, B. 1995. An acetohydroxy acid synthase mutant reveals a single site involved in multiple herbicide resistance. Mol. Gen. Genet. 246: 419425.CrossRefGoogle ScholarPubMed
Hattori, J., Rutledge, R., Labbé, H., Brown, D., Sunohara, G., and Miki, B. 1992. Multiple resistance to sulfonylureas and imidazolinones conferred by an acetohydroxyacid synthase gene with separate mutations for selective resistance. Mol. Gen. Genet. 232: 167173.CrossRefGoogle ScholarPubMed
Haughn, G. W., 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.Google Scholar
Haughn, G. W. and Sommerville, C. 1986. Sulfonylurea-resistant mutants of Arabidopsis thaliana . Mol. Gen. Genet. 204: 430434.Google Scholar
Haughn, G. W. and Somerville, C. R. 1990. A mutation causing imidazolinone resistance maps to the Csrl locus of Arabidopsis thaliana . Plant Physiol. 92: 10811085.Google Scholar
Hauptmann, R. M., della-Cioppa, G., Smith, A. G., Kishore, G. M., and Widholm, J. M. 1988. Expression of glyphosate resistance in carrot somatic hybrid ccells through transfer of an amplified 5-enolpyruvylshikimic acid-3-phosphate synthase gene. Mol. Gen. Genet. 211: 357363.Google Scholar
Heering, D. C., Guenzi, A. C., Peeper, T. F., and Claypool, P. L. 1992. Growth response of wheat (Triticum aestivum) callus to imazapyr and in vitro selection for resistance. Weed Sci. 40: 174179.Google Scholar
Her, S. E., Swanton, C. J., and Pauls, K. P. 1993. In vitro selection of imazethapyr-tolerant tomato (Lycopersicon esculentum Mill.). Weed Sci. 41: 1217.Google Scholar
Johnson, D. H. and Talbert, R. E. 1993. Imazaquin, chlorimuron, and fomesafen may injure rotational vegetables and sunflower (Helianthus annuus) . Weed Technol. 7: 573577.Google Scholar
Kakefuda, G., Ott, K.-H., Kwagh, J.-G., and Stockton, G. W. 1996. Structure-based designed herbicide resistant products. World patent application WO96/33270. Oct. 24.Google Scholar
Ktausz, R. F., Kapusta, G., and Matthews, J. L. 1994. Soybean (Glycine max) and rotational crop response to PPI chlorimuron, clomazone, imazaquin, and imazethapyr. Weed Technol. 8: 224230.Google Scholar
Lee, A., Gotterdam, P. E., Chiu, T. Y., and Mallipudi, M. N. 1991. Plant metabolism. Pages 151165 in Shaner, D. L. and O'Connor, S. L., eds. The Imidazolinone Herbicides. Boca Raton, FL: CRC Press.Google Scholar
Lee, K. Y, Townsend, J., Tapperman, J., Black, M., Chui, C.-F., Mazur, B., Dunsmuir, P., and Bedbrook, J. 1988. The molecular basis of sulfonylurea herbicide resistance in tobacco. EMBO J. 7: 12411248.Google Scholar
Mallory-Smith, C. A., Thill, D. C., Dial, M. J., and Zemetra, R. S. 1990. Inheritance of sulfonylurea herbicide resistance in Lactuca spp. Weed Technol. 4: 787790.Google Scholar
McHughen, A. 1989. Agrobacterium mediated transfer of chlorsulfuron resistance to commercial flax cultivars. Plant Cell Rep. 8:445449.Google Scholar
Montoya, A., Jen, G., Harms, C., Carswell, G., Armour, S., and Volrath, S. 1990. Novel herbicide tolerant plants. Eur. Pat. Appl. EP030750A2.Google Scholar
Mourad, G., Haughn, G., and King, J. 1994. Intragenic recombination in the CSR1 locus of Arabidopsis . Mol. Gen. Genet. 243: 178184.Google Scholar
Mourad, G. and King, J. 1992. Effect of four classes of herbicides on growth and acetolactate-synthase activity in several variants of Arabidopsis thaliana . Planta 188: 491497.Google Scholar
Mourad, G., Williams, D., and King, J. 1995. A double mutant allele, csrl-4, of Arabidopsis thaliana encodes an acetolactate synthase with altered kinetics. Planta 196: 6468.Google Scholar
Moyer, J. R., Esau, R., and Kozub, G. C. 1990. Chlorsulfuron persistence and response of nine rotational crops in alkaline soils of southern Alberta. Weed Technol. 4: 543548.Google Scholar
Muller, Y. A. and Schulz, G. E. 1993. Structure of the thiamine- and flavin-dependent enzyme pyruvate oxidase. Science 259: 965967.Google Scholar
Newhouse, K., Singh, B., Shaner, D., and Stidham, M. 1991. Mutations in corn (Zea mays L.) conferring resistance to imidazolinone herbicides. Theor. Appl. Genet. 83: 6570.Google Scholar
Newhouse, K. E., Smith, W. A., Starrett, M. A., Schaefer, T. J., and Singh, B. K. 1992. Tolerance to imidazolinone herbicides in wheat. Plant Physiol. 100: 882886.Google Scholar
Ott, K.-H., Kwagh, J.-G., Stockton, G. W., Sidirov, V., and Kakefuda, G. 1996. Rational molecular design and genetic engineering of herbicide resistant crops by structure modeling and site-directed mutagenesis of acetohydroxyacid synthase. J. Mol. Biol. 263: 359368.Google Scholar
Ray, T. B. 1984. Site of action of chlorsulfuron. Plant Physiol. 75: 827831.Google Scholar
Renner, K. A. and Powell, G. E. 1991. Response of sugarbeet (Beta vulgaris) to herbicide residues in soil. Weed Technol. 5: 622627.Google Scholar
Saari, L. L., Cotterman, J. C., and Thill, D. C. 1994. Resistance to acetolactate synthase inhibiting herbicides. Pages 83139 in Powles, S. B. and Holtum, J.A.M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: Lewis Publications.Google Scholar
Sathasivan, K., Haughn, G. W., and Murai, N. 1991. Molecular basis of imidazolinone herbicide resistance in Arabidopsis thaliana var. Columbia. Plant Physiol. 97: 10441050.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
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.CrossRefGoogle 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
Shah, D. M., Horsch, R. B., Klee, H. J., et al. 1986. Engineering herbicide tolerance in transgenic plants. Science 233: 478481.Google Scholar
Shaner, D. L., Anderson, P. C., and Stidham, M. A. 1984. Imidazolinones: potential inhibitors of acetohydroxyacid synthase. Plant Physiol. 76: 545546.Google Scholar
Shaner, D. L. and Mallipudi, N. M. 1991. Mechanisms of selectivity of the imidazolinones. Pages 91102 in Shaner, D. L. and O'Connor, S. L., eds. The Imidazolinone Herbicides. Boca Raton, FL: CRC Press.Google Scholar
Singh, B. K., Stidham, M. A., and Shaner, D. L. 1988. Assay of acetohydroxyacid synthase. Anal. Biochem. 171: 173179.Google Scholar
Takahashi, S., Shigematsu, S., and Morita, A. 1991. KIH-2031, a new herbicide for cotton. Pages 5762 in Proceedings of the Brighton Crop Protection Conference. Farnham, Great Britain: Brighton Crop Protection Council.Google Scholar
Tecle, B., Da Cunha, A., and Shaner, D. L. 1993. Differential routes of metabolism of imidazolinones: basis for soybean (Glycine max) selectivity. Pestic. Biochem. Physiol. 46: 120130.Google Scholar
Umbarger, H. E. 1978. Amino acid biosynthesis and its regulation. Annu. Rev. Biochem. 47: 533606.Google Scholar
Walsh, J. D., DeFelice, M. S., and Sims, B. D. 1993. Soybean (Glycine max) herbicide carryover to grain and fiber crops. Weed Technol. 7: 625632.Google Scholar
Westerfield, W. W. 1945. A colorimetric determination of blood acetoin. J. Biol. Chem. 161: 495502.Google Scholar
Wiersma, P. A., Schmiemann, M. G., Condie, J. A., Crosby, W. L., and Moloney, M. M. 1989. Isolation, expression and phylogenic inheritance of an acetolactate synthase gene from Brassica napus . Mol. Gen. Genet. 219: 413420.Google Scholar
Woodworth, A., Bernasconi, P., Subramanian, M., and Rosen, B. 1996a. A second naturally occurring point mutation confers broad-based tolerance to acetolactate synthase inhibitors. Plant Physiol. 111: S105.Google Scholar
Woodworth, A. R., Rosen, B. A., and Bernasconi, P. 1996b. Broad range resistance to herbicides targeting acetolactate synthase (ALS) in a field isolate of Amaranthus sp . Is conferred by a Trp to Leu mutation in the ALS gene. Plant Physiol. 111: 1353.Google Scholar
Wright, T. R. and Penner, D. 1996. Mechanism of imidazolinone resistance of two sugarbeet somaclonal selections. Proc. N. Cent. Weed Sci. Soc. 51: 98.Google Scholar
Wright, T. R. and Penner, O. 1997. Selection and genetic analysis of two imidazolinone-resistant sugarbeets. Weed Sci. Soc. Am. Abstr. 37: 253.Google Scholar
Wright, T. R. and Penner, D. 1998. Cell selection and inheritance of imidazolinone resistance in sugarbeet (Beta vulgaris). Theor. Appl. Genet. In press.Google Scholar