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Mutations in the red rice ALS gene associated with resistance to imazethapyr

Published online by Cambridge University Press:  20 January 2017

Satyendra N. Rajguru ,
Nilda R. Burgos ,
Vinod K. Shivrain  and
James McD. Stewart
Satyendra N. Rajguru
Affiliation:
Crop, Soil, and Environmental Sciences, 1366 West Altheimer Drive, University of Arkansas, Fayetteville, AR 72704
Vinod K. Shivrain
Affiliation:
Crop, Soil, and Environmental Sciences, 1366 West Altheimer Drive, University of Arkansas, Fayetteville, AR 72704
James McD. Stewart
Affiliation:
Crop, Soil, and Environmental Sciences, PTSC115, University of Arkansas, Fayetteville, AR 72701
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Abstract

The introduction of Clearfield (CL) rice cultivars resistant to imidazolinone herbicides, acetolactate synthase (ALS) inhibitors, has raised concerns of gene flow to weedy rice genotypes collectively called “red rice” that infest rice-growing areas in the southern United States. This experiment was conducted to study hybridization between CL rice and red rice using simple sequence repeats (SSR) markers, identify mutations in the ALS gene of imazethapyr-resistant red rice, and to detect the introgression of the ALS-resistant gene from CL rice into red rice. Natural outcrossing experiments between CL rice and strawhull (SH) red rice were set up in Stuttgart, AR, in 2002 and 2003. Putative red rice hybrids were detected among volunteer plants in the following year. Hybridization was confirmed using SSR markers, and introgression of the resistant ALS gene from CL rice to red rice was detected by ALS gene sequencing. The ALS gene sequences of U.S. rice cultivars ‘Bengal’ and ‘Cypress’, SH red rice, CL rice (CL161), and imazethapyr-resistant red rice/CL rice hybrids were compared. Nucleotide sequences of the ALS gene from the rice cultivars were identical. Three point mutations were present in the SH red rice ALS gene coding region relative to Bengal/Cypress. One of these resulted in the substitution of Asp630 for Glu630. The ALS gene sequences of confirmed hybrids were identical to that of the herbicide-resistant pollen source, CL161. We identified four ALS gene mutations in the herbicide-resistant red rice hybrids relative to the susceptible rice cultivars. One point mutation, resulting in a substitution of Ser653 with Asn, was linked to ALS resistance in callus tissue derived from a Kinmaze rice line from Japan. The other three mutations (Ser186—Pro, Lys416—Glu, and Leu662—Pro) are novel. This experiment confirmed that gene flow from imidazolinone-resistant rice resulted in herbicide-resistant red rice plants.

Keywords

Imazethapyrred rice, Oryza sativa L. ORSATrice, Oryza sativa L.ALS gene sequencecrop–weed hybridizationgene flowherbicide-resistant croppoint mutation
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 53 , Issue 5 , October 2005 , pp. 567 - 577
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Arias, D. M. and Rieseberg, L. H. 1994. Gene flow between cultivated and wild sunflowers. Theor. Appl. Genet 89:655–660.Google Scholar
Arnold, M. L. 1992. Natural hybridization as an evolutionary process. Annu. Rev. Ecol. Syst 23:237–261.Google Scholar
Arnold, M. L. 1997. Natural Hybridization and Evolution. New York: Oxford University Press.CrossRefGoogle Scholar
Arriola, P. E. and Ellstrand, N. C. 1996. Crop-to-weed gene flow in the genus Sorghum (Poaceae): spontaneous interspecific hybridization between johnsongrass, Sorghum halepense, and crop sorghum, S. bicolor . Am. J. Bot 83:1153–1159.Google Scholar
Bedbrook, J. R., Chaleff, R. S., Falco, S. C., Mazur, B. J., Somerville, C. R., and Yadev, N. S. inventors. 1995. Nucleic acid fragment encoding herbicide-resistant plant acetolactate synthase. U.S. patent 5,378,824.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 270:17381–17385.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 55:507–516.Google Scholar
Christopher, J. T., Powles, S. B., and Holtum, J. A. M. 1992. Resistance to acetolactate synthase-inhibiting herbicides in annual ryegrass (Lolium rigidum) involves at least two mechanisms. Plant Physiol 100:1909–1913.Google Scholar
Christopher, J. T., Powles, S. B., Liljegren, D. R., and Holtum, J. A. M. 1991. Cross-resistance to herbicides in annual ryegrass (Lolium rigidum). II. Chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiol 95:1036–1043.Google Scholar
Colwell, R. K., Norse, E. A., Pimentel, D., Sharples, F. E., and Simberloff, D. 1985. Genetic engineering in agriculture. Science 229:111–112.CrossRefGoogle ScholarPubMed
Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890.Google Scholar
Cotterman, J. C. and Saari, L. L. 1992. Rapid metabolic inactivation is the basis for cross-resistance to chlorsulfuron in diclofop-methyl-resistant rigid ryegrass (lolium rigidum) biotype SR4/84. Pestic. Biochem. Physiol 43:182–192.Google Scholar
Croughan, T. P., Utomo, H. S., Sanders, D. E., and Braverman, M. P. 1996. Herbicide-resistant rice offers potential solution to red rice problem. LA Agric 39:10–12.Google Scholar
Devine, M. D. and Preston, C. 2000. The molecular basis of herbicide resistance. Pages 72–104 in Cobb, A. H. and Kirkwood, R. C. eds. Herbicides and Their Mechanisms of Action. Sheffield, Great Britain: Sheffield Academic.Google Scholar
Diebold, R. S., McNaughton, K. E., Lee, E. A., and Tardiff, F. J. 2003. Multiple resistance to imazethapyr and atrazine in Powell amaranth (Amaranthus powellii). Weed Sci 51:312–318.CrossRefGoogle Scholar
Doyle, J. J. and Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull 19:11–15.Google Scholar
Ellstrand, N. C., Prentice, H. C., and Hancock, J. F. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst 30:539–563.Google Scholar
Estorninos, L. E., Gealy, D. R., Baldwin, T. L., Baldwin, F. L., and Burgos, N. R. 2003. Estimates of outcrossing rates between IMI rice lines and red rice based on SSR fingerprinting and phenotypic characteristics. Pages 33–40 in B. R. Wells Rice Research Studies 2002. Research Ser. 504. Arkansas Agricultural Experiment Station.Google Scholar
Fischer, A. J., Bayer, D. E., Carriere, M. D., Ateh, C. M., and Yim, K. O. 2000. Mechanism of resistance to bispyribac-sodium in an Echinochloa phyllopogon accession. Pestic. Biochem. Physiol 68:156–165.Google Scholar
Forlani, G., Nielseren, F., Landi, P., and Tuberosa, R. 1991. Chlorsulfuron tolerance and acetolactate synthase activity in corn (Zea mays L.) inbred lines. Weed Sci 39:553–557.Google Scholar
Gressel, J. 2002. Molecular Biology of Weed Control. London: Taylor and Francis. 504 p.Google Scholar
Han, B. and Xue, Y. 2003. Genome-wide intraspecific DNA-sequence variations in rice. Curr. Opin. Plant Biol 6:134–138.Google Scholar
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 211:266–271.Google Scholar
Hinz, J. R. R. and Owen, M. D. K. 1977. Acetolactate synthase resistance in a common waterhemp (Amaranthus rudis) population. Weed Technol 11:13–18.Google Scholar
Langevin, S. A., Clay, K., and Grace, J. 1990. The incidence and effects of hybridization between cultivated rice and its related weed red rice (Oryza sativa L). Evolution 44:1000–1008.CrossRefGoogle ScholarPubMed
Menendez, J. M., De Prado, R., and Devine, M. D. 1997. Chlorsulfuron cross-resistance in a chlorotoluron-resistant biotype of Alopecurus myosuroides . Proc. Brighton Crop. Prot. Conf.—Weeds. Frnham, Great Britain: The British Crop Protection Council. P. 319.Google Scholar
Oh, K. J., Park, E. J., Yoon, M. Y., Han, T. R., and Choi, J. D. 2001. Roles of histidine residues in tobacco acetolactate synthase. Biochem. Biophys. Res. Commun 282:1237–1243.Google Scholar
Ott, K. H., Kwagh, J. G., Stockton, G. W., Sidirov, V., and Kakefuda, K. 1996. Rational molecular design and genetic engineering of herbicide resistant crops by structure modeling and site-directed mutagenesis of acetohydroxyacid synthase. J. Mol. Biol 263:359–368.Google Scholar
Paterson, A. H., Schertz, K. F., Lin, Y. R., Liu, S. C., and Chang, Y. L. 1995. The weediness of wild plants: molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L.) Pers. Proc. Natl. Acad. Sci. USA 92:6127–6131.Google Scholar
Patzoldt, W. L. and Tranel, P. J. 2001. ALS mutations conferring herbicide resistance in waterhemp. Proc. N. Cent. Weed Sci. Soc 56:67.Google Scholar
Preston, C. and Mallory-Smith, C. A. 2001. Biochemical mechanisms, inheritance, and molecular genetics of herbicide resistance in weeds. Pages 23–60 in Powles, S. B. and Shaner, D. L. eds. Herbicide Resistance and World Grains. Boca Raton, FL: CRC.Google Scholar
Rajguru, S. N., Burgos, N. R., Stewart, J. McD., and Gealy, D. 2002. Genetic diversity in red rice using SSR markers. Proc. Weed Sci. Soc. Am 55:115–116.Google Scholar
Rieseberg, L. H. 1995. The role of hybridization in evolution: old wine in new skins. Am. J. Bot 82:944–953.Google Scholar
Ritala, A., Nuutila, A. M., Aikasalo, R., Kauppinen, V., and Tammisola, J. 2002. Measuring gene flow in the cultivation of transgenic barley. Crop Sci 42:278–285.Google Scholar
Saari, L. L., Cotterman, J. C., and Thill, D. C. 1994. Resistance to acetolactate synthase inhibiting herbicides. Pages 83–139 in Powles, S. B. and Holtum, J.A.M. eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: CRC.Google Scholar
Scott, R. C. and Burgos, N. R. 2004 Nov 12. Clearfield rice/red rice outcross confirmed in Arkansas field. Delta Farm Press: 18.Google Scholar
Seefeldt, S. S., Zemetra, R., Young, F. L., and Jones, S. S. 1998. Production of herbicide-resistant jointed goatgrass (Aegilops cylindrica) × wheat (Triticum aestivum) hybrids in the field by natural hybridization. Weed Sci 46:632–634.Google Scholar
Shivrain, V. K. 2004. Phenotypic Characterization and Natural Variation in the ALS Gene of Red Rice. . University of Arkansas, Fayetteville, AR. 180 p.Google Scholar
Shivrain, V. K., Burgos, N. R., Moldenhauer, K. A., and Gealy, D. R. 2004a. Phenotypic and morphological diversity of red rice in Arkansas. Proc. South. Weed Sci. Soc. P. 207.Google Scholar
Shivrain, V. K., Burgos, N. R., Rajguru, S. N., Sparks, O. C., and Anders, M. M. 2004b. Potential for gene flow between imidazolinone-resistant rice and red rice. Proc. Weed Sci. Soc. Am 44:65.Google Scholar
Subramanian, M., Bernasconi, P., and Hess, F. D. 1996. Approaches to assess the frequency of resistance development to new herbicides. Proc. 2nd International Weed Control Congress; Copenhagen, Denmark. Pp. 1–8.Google Scholar
Tang, L. H. and Morishima, H. 1996. Genetic characteristics and origin of weedy rice. China Agric. University Press. Pp. 211–218.Google Scholar
Tranel, P. J. and Wright, T. R. 2002. Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700–712.Google Scholar
Uchino, A. and Watanabe, H. 2002. Mutations in the acetolactate synthase genes of sulfonylurea-resistant biotypes of Lindernia spp. Weed Biol. Manag 2:104–109.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 48:2986–2990.Google Scholar
Wright, T. R., Bascomb, N. F., Sturner, S. F., and Penner, D. 1998. Biochemical mechanism and molecular basis of ALS-inhibiting herbicide resistance in sugarbeet (Beta vulgaris) somatic cell selections. Weed Sci 46:13–23.Google Scholar
Zhang, W., Linscombe, S., Webster, E., and Oard, J. 2004. Risk assessment and genetic analysis of natural outcrossing in Louisiana commercial fields between Clearfield rice and the weed, red rice. 30th Rice Technical Working Group Meeting, New Orleans, LA. P. 195.Google Scholar
Zhi, P. S., Lu, B., Zhu, Y. G., and Chen, J. K. 2003. Gene flow from cultivated rice to the wild species Oryza rufipogon under experimental field conditions. New Phytol 157:657–665.Google Scholar