Differences in amino acid composition of carrot α-tubulin potentially confer the resistance to dinitroaniline herbicides

O. G. Melnyk; R. Y. Blume; P. A. Karpov

doi:10.7124/FEEO.v32.1534

O. G. Melnyk Institute of Food Biotechnology and Genomics, NAS of Ukraine, Ukraine, 04123, Kyiv, Baidy-Vyshnevetskoho str., 2А https://orcid.org/0000-0002-4249-9175
R. Y. Blume Institute of Food Biotechnology and Genomics, NAS of Ukraine, Ukraine, 04123, Kyiv, Baidy-Vyshnevetskoho str., 2А https://orcid.org/0000-0003-4936-1803
P. A. Karpov Institute of Food Biotechnology and Genomics, NAS of Ukraine, Ukraine, 04123, Kyiv, Baidy-Vyshnevetskoho str., 2А https://orcid.org/0000-0002-6876-642X

DOI: https://doi.org/10.7124/FEEO.v32.1534

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Keywords: α-tubulin, dinitroaniline, resistance, oryzalin, microtubules, herbicides

Abstract

Aim. To reveal the features of amino acid composition of carrot α-tubulin isotypes that potentially determine natural tolerance to dinitroaniline herbicides. Methods. Literature and database search. Comparison of protein sequences and structures: multiple sequence alignment, phylogenetic profiling, protein and ligand structure modeling, etc. Results. Genomic and proteomic analysis of Daucus carota has revealed at least eight unique isotypes of α-tubulin that differ in amino acid sequences and gene loci. Remarkable differences in amino acid composition of the dinitroanilinebinding-like (DBL) region of analyzed α-tubulin have been revealed, which may be the reason of its natural resistance to these compounds. Сonclusions. Differences in amino acids at positions of canonical mutations – Cys4 (TBA1, 2, 3, 6, 7 and 8), Thr53 (TBA6), Ile202 (TBA1 and 7) and Met202 (TBA5), as well as previously undescribed non-canonical substitutions – Ile4 (TBA4 and 5), Cys52 (TBA6), Ser201 (TBA1, 2, 3 and 8) and Val194 (TBA4 and 5), were noted as potentially associated with natural tolerance of the carrot to dinitroaniline herbicides.

References

Vaughan M. A., Vaughn K. C. Carrot microtubules are dinitroaniline resistant. I. Cytological and cross-resistance studies. Weed Research. 1988. Vol. 28. P. 73–83. doi: 10.1111/j.1365-3180.1988.tb00789.x.

Chen J., Yu Q., Patterson E., Sayer C., Powles S. Dinitroaniline herbicide resistance and mechanisms in weeds. Front Plant Sci. 2021. Vol. 25. 12. # 634018. doi: 10.3389/fpls.2021.634018.

Oakley B. R. Microtubule mutants. Can J Biochem Cell Biol. 1985. Vol. 63 (6). P. 479–488. doi: 10.1139/o85-067.

Akella J. S., Wloga D., Kim J., Starostina N. G., Lyons-Abbott S., Morrissette N. S., Dougan S. T., Kipreos E. T., Gaertig J. MEC-17 is an alpha-tubulin acetyltransferase. Nature. 2010. Vol. 467 (7312). P. 218–222. doi: 10.1038/nature09324.

Anthony R. G., Reichelt S., Hussey P. J. Dinitroaniline herbicide-resistant transgenic tobacco plants generated by cooverexpression of a mutant alpha-tubulin and a beta-tubulin. Nat Biotechnol. 1999. Vol. 17 (7). P. 712–716. doi: 10.1038/10931.

Chen J., Yu Q., Owen M., Han H., Powles S. Dinitroaniline herbicide resistance in a multiple-resistant Lolium rigidum population. Pest Manag Sci. 2018. Vol. 74 (4). P. 925–932. doi: 10.1002/ps.4790.

Chu Z., Chen J., Nyporko A., Han H., Yu Q., Powles S. Novel α-tubulin mutations conferring resistance to dinitroaniline herbicides in Lolium rigidum. Front Plant Sci. 2018. Vol. 9: 97. eCollection. 2018. doi: 10.3389/fpls.2018.00097.

Délye C., Menchari Y., Michel S., Darmency H. Molecular bases for sensitivity to tubulin-binding herbicides in green foxtail. Plant Physiol. 2004. Vol. 136 (4). P. 3920–3932. doi: 10.1104/pp.103.037432.

Gaertig J., Thatcher T. H., Gu L., Gorovsky M. A. Electroporation-mediated replacement of a positively and negatively selectable beta-tubulin gene in Tetrahymena thermophila. Proc Natl Acad Sci U S A. 1994. Vol. 91 (10). P 4549–4553. doi: 10.1073/pnas.91.10.4549.

Hashim S., Jan A., Sunohara Y., Hachinohe M., Ohdan H., Matsumoto H. Mutation of alpha-tubulin genes in trifluralin-resistant water foxtail (Alopecurus aequalis). Pest Manag Sci. 2012. Vol. 68 (3). P. 422–429. doi: 10.1002/ps.2284.

James S. W., Silflow C. D., Stroom P., Lefebvre P. A. A mutation in the alpha 1-tubulin gene of Chlamydomonas reinhardtii confers resistance to anti-microtubule herbicides. J Cell Sci. 1993. Vol. 106 (Pt. 1). P. 209–218. doi: 10.1242/jcs.106.1.209.

Lyons-Abbott S., Sackett D. L., Wloga D., Gaertig J., Morgan R. E., Werbovetz K. A., Morrissette N. S. α-Tubulin mutations alter oryzalin affinity and microtubule assembly properties to confer dinitroaniline resistance. Eukaryot Cell. 2010. Vol. 9 (12). P. 1825–1834. doi: 10.1128/EC.00140-10.

Ma C., Li C., Ganesan L., Oak J., Tsai S., Sept D., Morrissette N. S. Mutations in alpha-tubulin confer dinitroaniline resistance at a cost to microtubule function. Mol Biol Cell. 2007. Vol. 18 (12). P. 4711–4720. doi: 10.1091/mbc.e07-04-0379.

Ma C., Tran J., Li C., Ganesan L., Wood D., Morrissette N. Secondary mutations correct fitness defects in Toxoplasma gondii with dinitroaniline resistance mutations. Genetics. 2008. Vol. 180 (2). P. 845–856. doi: 10.1534/genetics.108.092494.

Morrissette N. S., Sept D. Dinitroaniline interactions with tubulin: genetic and computational approaches to define the mechanisms of action and resistance. In The Plant Cytoskeleton: a Key Tool for Agro-Biothecnology; Blume Ya. B., Baird W. V., Yemets A. I., Breviario D., Eds. Springer, 2008. P. 327–349.

Varberg J. M., Padgett L. R., Arrizabalaga G., Sullivan W. J. Jr. TgATAT-Mediated α-Tubulin Acetylation Is Required for Division of the Protozoan Parasite Toxoplasma gondii. mSphere. 2016. Vol. 1 (1). e00088-15. doi: 10.1128/mSphere.00088-15.

Yamamoto E., Zeng L., Baird W. V. Alpha-tubulin missense mutations correlate with antimicrotubule drug resistance in Eleusine indica. Plant Cell. 1998. Vol. 10 (2). P. 297–308. doi: 10.1105/tpc.10.2.297.

Aguayo-Ortiz R., Dominguez L. Unveiling the Possible Oryzalin-Binding Site in the α-Tubulin of Toxoplasma gondii. ACS Omega. 2022. Vol. 7 (22). P. 18434–18442. doi: 10.1021/acsomega.2c00729.

Mitra A., Sept D. Binding and interaction of dinitroanilines with apicomplexan and kinetoplastid alpha-tubulin. J Med Chem. 2006. Vol. 49 (17). P. 5226–5231. doi: 10.1021/jm060472+.

Morrissette N. S., Mitra A., Sept D., Sibley L. D. Dinitroanilines bind alpha-tubulin to disrupt microtubules. Mol Biol Cell. 2004. Vol. 15 (4). P. 1960–1968. doi: 10.1091/mbc.e03-07-0530.

Blume Y. B., Nyporko A. Y., Yemets A. I., Baird W. V. Structural modeling of the interaction of plant alpha-tubulin with dinitroaniline and phosphoroamidate herbicides. Cell Biol Int. 2003. Vol. 27 (3). P. 171–174. doi: 10.1016/s1065-6995(02)00298-6.

Nyporko A. Y., Yemets A. I., Brytsun V. N., Lozinsky M. O., Blume Y. B. Structural and biological characterization of the tubulin interaction with dinitroanilines. Cytol. Genet. 2009. Vol. 43. P. 267–282. doi: 10.3103/S0095452709040082.

Yang J., Wang Y., Wang T., Jiang J., Botting C.H., Liu H., Chen Q., Yang J., Naismith J.H., Zhu X., Chen L. Pironetin reacts covalently with cysteine-316 of α-tubulin to destabilize microtubule. Nat Commun. 2016. Vol. 7. #12103. doi: 10.1038/ncomms12103.

Ladunga I. Finding Homologs in Amino Acid Sequences Using Network BLAST Searches. Curr Protoc Bioinformatics. 2017. Vol. 59. P. 3.4.1–3.4.24. doi: 10.1002/cpbi.34.

Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987. Vol. 4 (4). P. 406–425. doi: 10.1093/oxfordjournals.molbev.a040454