Abstract
The dinitroaniline herbicides (such as trifluralin and oryzalin) have been developed for the selective control of weeds in arable crops. However, prolonged use of these chemicals has resulted in the selection of resistant biotypes of goosegrass, a major weed. These herbicides bind to the plant tubulin protein but not to mammalian tubulin1. Here we show that the major α-tubulin gene of the resistant biotype has three base changes within the coding sequence. These base changes swap cytosine and thymine, most likely as the result of the spontaneous deamination of methylated cytosine. One of these base changes causes an amino-acid change in the protein: normal threonine at position 239 is changed to isoleucine. This position is close to the site of interaction between tubulin dimers in the microtubule protofilament. We show that the mutated gene is the cause of the herbicide resistance by using it to transform maize and confer resistance to dinitroaniline herbicides. Our results provide a molecular explanation for the resistance of goosegrass to dinitroanaline herbicides, a phenomenon that has arisen, and been selected for, as a result of repeated exposure to this class of herbicide.
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References
Morejohn, L. C., Bureau, T. E., Molé-Bajer, J., Bajer, A. S. & Fosket, D. E. Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta 172, 252–264 (1987).
Parka, S. J. & Soper, O. F. The physiology and mode of action of the dinitroaniline herbicides. Weed Sci. 25, 79–87 (1977).
Appleby, A. P. & Valverde, B. E. Behaviour of dinitroaniline herbicides in plants. Weed Technol. 3, 198–206 (1989).
Mudge, L. C., Gossett, B. J. & Murphy, T. R. Resistance of goosegrass (Eleusine indica) to dinitroaniline herbicides. Weed Sci. 32, 591–594 (1984).
Vaughn, K. C., Marks, M. D. & Weeks, D. P. Adinitroaniline resistant mutant of Eleusine indica exhibits cross-resistance and supersensitivity to antimicrotubule herbicides and drugs. Plant Physiol. 83, 956–964 (1987).
Waldin, T. R., Ellis, J. R. & Hussey, P. J. Tubulin isotope analysis of two grass species resistant to dinitroaniline herbicides. Planta 188, 258–264 (1992).
Akashi, T. et al. Effects of propyzamide on tobacco cell microtubules in vivo and in vitro. Plant Cell Physiol. 29, 1053–1062 (1988).
Morejohn, L. C. & Fosket, D. E. The biochemistry of compounds with anti-microtubule activity in plant cells. Pharmacol. Ther. 51, 217–230 (1991).
Villemur, R. et al. The α-tubulin gene family in maize (Zea mays L.): evidence for two ancient α-tubulin genes in plants. J. Mol. Biol. 227, 81–86 (1992).
Hussey, P. J. et al. The β-tubulin gene family in Zea mays: two differentially expressed β-tubulin genes. Plant Mol. Biol. 15, 957–972 (1990).
Jiang, C.-J. & Sonobe, S. Identification and preliminary charactisation of a 65 kDa higher-plant microtubule-associated protein. J. Cell Sci. 105, 891–901 (1993).
Burns, R. G. & Surridge, C. D. in Microtubules (eds Hyams, J. S. & Lloyd, C. W.) 3–31 (Wiley-Liss, New York, (1994)).
Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199–203 (1998).
Lowe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203–206 (1998).
Ausubel, F. M. et al. Current Protocols in Molecular Biology (Greene Publishing and Wiley InterScience, New York, (1992)).
Frame, B. R. et al. Production of fertile transgenic maize plants by silicon carbide whisker-mediated transformation. Plant J. 6, 941–948 (1994).
Last, D. I. et al. PEMU: an improved promoter for gene expression in cereal cells. Theor. Appl. Genet. 81, 581–588 (1991).
Thompson, C. et al. Degradation of oxalic acid by transgenic oilseed rape plants expressing oxalate oxidase. Euphytica 85, 169–172 (1995).
Field, J. et al. Purification of a RAS-responsive adenyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8, 2159–2165 (1988).
Acknowledgements
We thank J. Lowe and L. Amos for discussion about the structures of FtsZ and tubulin, E. Nogales and K. Downing for providing the coordinates of the αβ-tubulin dimer and K. Roberts and H. Dickinson for critical reading of the paper. This work was supported by the Biotechnology and Biological Sciences Research Council (R.G.A., T.R.W., P.J.H.) and, in part, by Zeneca Agrochemicals (J.R., S.B.). This paper is dedicated to the memory of the late Ray Ellis with whom the work was initiated.
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Anthony, R., Waldin, T., Ray, J. et al. Herbicide resistance caused by spontaneous mutation of the cytoskeletal protein tubulin. Nature 393, 260–263 (1998). https://doi.org/10.1038/30484
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DOI: https://doi.org/10.1038/30484
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