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Research Articles

Functional characterization of novel mutations in the conserved region of EPSPS for herbicide resistance in pigeonpea: structure-based coherent design

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Pages 6065-6080 | Received 02 Feb 2023, Accepted 21 Jun 2023, Published online: 31 Aug 2023

References

  • Achary, V. M. M., Sheri, V., Manna, M., Panditi, V., Borphukan, B., Ram, B., Agarwal, A., Fartyal, D., Teotia, D., Masakapalli, S. K., Agrawal, P. K., & Reddy, M. K. (2020). Overexpression of improved EPSPS gene results in field level glyphosate tolerance and higher grain yield in rice. Plant Biotechnology Journal, 18(12), 2504–2519. https://doi.org/10.1111/pbi.13428
  • Ajawatanawong, P. (2016). Molecular phylogenetics: Concepts for a newcomer. In I. Nookaew (Ed.), Network biology. Advances in biochemical engineering/biotechnology (Vol. 160, pp. 185–196). Springer. https://doi.org/10.1007/10_2016_49
  • American Chemical Society (1997). Glyphosate: A unique global herbicide. American Chemical Society Monograph.
  • Arndell, T., Sharma, N., Langridge, P., Baumann, U., Watson-Haigh, N. S., & Whitford, R. (2019). gRNA validation for wheat genome editing with the CRISPR-Cas9 system. BMC Biotechnology, 19(1), 71. https://doi.org/10.1186/s12896-019-0565-z
  • Azimi, S., Tapan, K., & Gandhi, T. K. (2021). 3-D maximum likelihood estimation sample consensus for correspondence grouping in 3-D plant point cloud. IEEE Sensors Letters, 5(6), 1–4. https://doi.org/10.1109/LSENS.2021.3075459
  • Baerson, S. R., Rodriguez, D. J., Tran, M., Feng, Y., Biest, N. A., & Dill, G. M. (2002). Glyphosate resistant goose grass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiology, 129(3), 1265–1275. https://doi.org/10.1104/pp.001560
  • Bentley, R., & Haslam, E. (1990). The shikimate pathway—A metabolic tree with many branch. Critical Reviews in Biochemistry and Molecular Biology, 25(5), 307–384. https://doi.org/10.3109/10409239009090615
  • Blaxter, M., Archibald, J. M., Childers, A. K., Coddington, J. A., Crandall, K. A., Palma, F. D., Durbin, R., Edwards, S. V., Graves, J. A. M., Hackett, K. J., Hall, N., Jarvis, E. D., Johnson, R. N., Karlsson, E. K., Kress, W. J., Kuraku, S., Lawniczak, M. K. N., Lindblad-Toh, K., Lopez, J. V., … Lewin, H. A. (2022). Why sequence all eukaryotes? Proceedings of the National Academy of Sciences of the United States of America, 119(4), e2115636118. https://doi.org/10.1073/pnas.2115636118
  • Bray, S. A., Senapathi, T., Barnett, C. B., & Grüning, B. A. (2020). Intuitive, reproducible high-throughput molecular dynamics in Galaxy: A tutorial. bioRxiv Preprint. https://doi.org/10.1101/2020.05.08.084780
  • Cao, G., Liu, Y., Zhang, S., Yang, X., Chen, R., Zhang, Y., Lu, W., Liu, Y., Wang, J., Lin, M., & Wang, G. (2012). A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. PLOS One, 7(6), e38718. https://doi.org/10.1371/journal.pone.0038718
  • Chahal, P., Varanasi, V., Jugulam, M., & Jhala, A. (2017). Glyphosate-resistant Palmer Amaranth (Amaranthus palmeri) in Nebraska: Confirmation, EPSPS gene amplification, and response to POST corn and soybean herbicides. Weed Technology, 31(1), 80–93. https://doi.org/10.1614/WT-D-16-00109.1
  • Chandrasekhar, K., Reddy, G. M., Singh, J., Vani, K., Vijayalakshmi, M., Kaul, T., & Reddy, M. K. (2014). Development of transgenic rice harbouring mutated rice 5-enol pyruvyl shikimate 3-phosphate synthase (Os-mEPSPS) and Allium sativum leaf agglutinin (ASAL) genes conferring tolerance to herbicides and sap-sucking insects. Plant Molecular Biology Reporter, 32(6), 1146–1157. https://doi.org/10.1007/s11105-014-0715-3
  • Chhapekar, S., Raghavendrarao, S., Pavan, G., Ramakrishna, C., Singh, V. K., Phanindra, M. L., Dhandapani, G., Sreevathsa, R., & Ananda Kumar, P. (2015). Transgenic rice expressing a codon-modified synthetic CP4-EPSPS confers tolerance to broad-spectrum herbicide, glyphosate. Plant Cell Reports, 34(5), 721–731. https://doi.org/10.1007/s00299-014-1732-2
  • Cockerton, H. M., Kaundun, S. S., Nguyen, L., Hutchings, S. J., Dale, R. P., Howell, A., & Neve, P. (2021). Fitness cost associated with enhanced EPSPS gene copy number and glyphosate resistance in an Amaranthus tuberculatus population. Frontiers in Plant Science, 12, 651381. https://doi.org/10.3389/fpls.2021.651381
  • Comai, L., Facciotti, D., Hiatt, W. R., Thompson, G., Rose, R. E., & Stalker, D. M. (1985). Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature, 317(6039), 741–744. https://doi.org/10.1038/317741a0
  • Dong, Y., Ng, E., Lu, J., Fenwick, T., Tao, Y., Bertain, S., Sandoval, M., Bermudez, E., Hou, Z., Patten, P., Lassner, M., & Siehl, D. (2019). Desensitizing plant EPSP synthase to glyphosate: Optimized global sequence context accommodates a glycine-to-alanine change in the active site. The Journal of Biological Chemistry, 294(2), 716–725. https://doi.org/10.1074/jbc.RA118.006134
  • Du, J., Sun, H., Xi, L., Li, J., Yang, Y., Liu, H., & Yao, X. (2011). Molecular modelling study of checkpoint kinase 1 inhibitors by multiple docking strategies and prime/MM-GBSA calculation. Journal of Computational Chemistry, 32(13), 2800–2809. https://doi.org/10.1002/jcc.21859
  • Fazil, M. H., Kumar, S., Rao, N. S., Selvaraj, C., Singh, S. K., Pandey, H. P., & Singh, D. V. (2012). Comparative structural analysis of two proteins belonging to quorum sensing system in Vibrio cholerae. Journal of Biomolecular Structure & Dynamics, 30(5), 574–584. https://doi.org/10.1080/07391102.2012.687523
  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution; International Journal of Organic Evolution, 39(4), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  • Filiz, E., & Koc, I. (2016). Genome-wide identification and comparative analysis of EPSPS (aroA) genes in different plant species. Journal of Plant Biochemistry and Biotechnology, 25(1), 21–29. https://doi.org/10.1007/s13562-015-0303-0
  • Firdous, S., Iqbal, S., Anwar, S., & Jabeen, H. (2018). Identification and analysis of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene from glyphosate-resistant Ochrobactrum intermedium Sq20. Pest Management Science, 74(5), 1184–1196. https://doi.org/10.1002/ps.4624
  • Fonseca, E. C. M., Da., Costa, K. S., Lameira, J., Alves, C. N., & Lima, A. H. (2020). Investigation of the target-site resistance of EPSP synthase mutants P106T and T102I/P106S against glyphosate. RSC Advances, 10(72), 44352–44360. https://doi.org/10.1039/d0ra09061a
  • Funke, T., Han, H., Healy-Fried, M. L., Fischer, M., & Schonbrunn, E. (2006). Molecular basis for the herbicide resistance of Roundup Ready crops. Proceedings of the National Academy of Sciences of the United States of America, 103(35), 13010–13015. https://doi.org/10.1073/pnas.0603638103
  • Funke, T., Yang, Y., Han, H., Healy-Fried, M., Olesen, S., Becker, A., & Schönbrunn, E. (2009). Structural basis of glyphosate resistance resulting from the double mutation Thr97->Ile and Pro101->Ser in 5-enolpyruvylshikimate-3-phosphate synthase from Escherichia coli. The Journal of Biological Chemistry, 284(15), 9854–9860. https://doi.org/10.1074/jbc.M809771200
  • Gaines, T. A., Zhang, W., Wang, D., Bukun, B., Chisholm, S. T., Shaner, D. L., Nissen, S. J., Patzoldt, W. L., Tranel, P. J., Culpepper, A. S., Grey, T. L., Webster, T. M., Vencill, W. K., Sammons, R. D., Jiang, J., Preston, C., Leach, J. E., & Westra, P. (2010). Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proceedings of the National Academy of Sciences of the United States of America, 107(3), 1029–1034. https://doi.org/10.1073/pnas.0906649107
  • García, M. J., Palma-Bautista, C., Vazquez-Garcia, J. G., Rojano-Delgado, A. M., Osuna, M. D., Torra, J., & De Prado, R. (2020). Multiple mutations in the EPSPS and ALS genes of Amaranthus hybridus underlie resistance to glyphosate and ALS inhibitors. Scientific Reports, 10(1), 17681. https://doi.org/10.1038/s41598-020-74430-0
  • Garg, B., Vaid, N., & Tuteja, N. (2014). In-silico analysis and expression profiling implicate diverse role of EPSPS family genes in regulating developmental and metabolic processes. BMC Research Notes, 7(1), 58. https://doi.org/10.1186/1756-0500-7-58
  • Gazziero, D. L. P., Adegas, F., & Voll, E. (2008). Glifosate e a soja transgênica. Embrapa Soja Circ Tec, 60(INFOTECA-E), 1–4.
  • Giacomini, D., Westra, P., & Ward, S. M. (2014). Impact of genetic background in fitness cost studies: An example from glyphosate-resistant Palmer amaranth. Weed Science, 62(1), 29–37. https://doi.org/10.1614/WS-D-13-00066.1
  • Gong, Y., Liao, Z., Chen, M., Guo, B., Jin, H., Sun, X., & Tang, K. (2006). Characterization of 5-enolpyruvylshikimate 3-phosphate synthase gene from Camptotheca acuminata. Biologia Plantarum, 50(4), 542–550. https://doi.org/10.1007/s10535-006-0086-1
  • Goyal, M., Chauhan, S., Ankush, Goyal P., & Bishnoi, J. P. (2018). Structural modelling of shikimate pathway enzymes for herbicide and drug development: A review. Journal of Entomology and Zoology Studies, 6(2), 785–790.
  • Green, J. M., & Owen, M. D. (2011). Herbicide-resistant crops: Utilities and limitations for herbicide-resistant weed management. Journal of Agricultural and Food Chemistry, 59(11), 5819–5829. https://doi.org/10.1021/jf101286h
  • Griffin, S. L., Chekan, J. R., Lira, J. M., Robinson, A. E., Yerkes, C. N., Siehl, D. L., Wright, T. R., Nair, S. K., & Cicchillo, R. M. (2021). Characterization of a glyphosate-tolerant enzyme from Streptomyces svecius: A distinct class of 5-enolpyruvylshikimate-3-phosphate synthases. Journal of Agricultural and Food Chemistry, 69(17), 5096–5104. https://doi.org/10.1021/acs.jafc.1c00439
  • Gui-Rong, Y., Yan, L., Wen-Ping, D., Song, J., Lin, M., Li-Yuan, X., Fang-Ming, X., & Yong-Sheng, L. (2013). Optimization of Agrobacterium tumefaciens-mediated immature embryo transformation system and transformation of glyphosate-resistant gene 2mG2-EPSPS in maize (Zea mays L.). Journal of Integrative Agriculture, 12(12), 2134–2142. https://doi.org/10.1016/S2095-3119(13)60567-5
  • Halgren, T. A. (2009). Identifying and characterizing binding sites and assessing druggability. Journal of Chemical Information and Modeling, 49(2), 377–389. https://doi.org/10.1021/ci800324m
  • Han, H., Vila-Aiub, M. M., Jalaludin, A., Yu, Q., & Powles, S. B. (2017). A double EPSPS gene mutation endowing glyphosate resistance shows a remarkably high resistance cost. Plant, Cell & Environment, 40(12), 3031–3042. https://doi.org/10.1111/pce.13067
  • He, M., Yang, Z.-Y., Nie, Y.-F., Wang, J., & Xu, P. (2001). A new type of class I bacterial 5-enopyruvylshikimate-3-phosphate synthase mutants with enhanced tolerance to glyphosate. Biochimica et Biophysica Acta, 1568(1), 1–6. https://doi.org/10.1016/s0304-4165(01)00181-7
  • Heap, I., & Duke, S. O. (2018). Overview of glyphosate-resistant weeds worldwide. Pest Management Science, 74(5), 1040–1049. https://doi.org/10.1002/ps.4760
  • Heap, I. (2015). International survey of herbicide resistant weeds. Retrieved from www.weedscience.com
  • Hummel, A. W., Chauhan, R. D., Cermak, T., Mutka, A. M., Vijayaraghavan, A., Boyher, A., Starker, C. G., Bart, R., Voytas, D. F., & Taylor, N. J. (2018). Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnology Journal, 16(7), 1275–1282. https://doi.org/10.1111/pbi.12868
  • Imaizumi, T., Wang, G. X., Ohsako, T., & Tominaga, T. (2008). Genetic diversity of sulfonylurea-resistant and -susceptible Monochoria vaginalis populations in Japan. Weed Research, 48(2), 187–196. https://doi.org/10.1111/j.1365-3180.2008.00622.x
  • Iwakami, S., Shimono, Y., Manabe, Y., Endo, M., Shibaike, H., Uchino, A., & Tominaga, T. (2017). Copy number variation in acetolactate synthase genes of thifensulfuron-methyl resistant Alopecurus aequalis (Shortawn Foxtail) accessions in Japan. Frontiers in Plant Science, 8, 254. https://doi.org/10.3389/fpls.2017.00254
  • The International Service for the Acquisition of Agri-biotech Applications (Ed.). (2017). Global status of commercialized biotech/GM crops: Biotech crop adoption surges as economic benefits accumulate in 22 years. ISAAA.
  • Jiang, Y., Chai, Y., Qiao, D., Wang, J., Xin, C., Sun, W., Cao, Z., Zhang, Y., Zhou, Y., Wang, X. C., & Chen, Q. J. (2022). Optimized prime editing efficiently generates glyphosate-resistant rice plants carrying homozygous TAP-IVS mutation in EPSPS. Molecular Plant, 15(11), 1646–1649. https://doi.org/10.1016/j.molp.2022.09.006
  • Jin, M., Chen, L., Deng, X. W., & Tang, X. (2022). Development of herbicide resistance genes and their application in rice. The Crop Journal, 10(1), 26–35. https://doi.org/10.1016/j.cj.2021.05.007
  • Jones, D. T., Taylor, W. R., & Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences, 8(3), 275–282. https://doi.org/10.1093/bioinformatics/8.3.275
  • Karthik, K., Nandiganti, M., Thangaraj, A., Singh, S., Mishra, P., Rathinam, M., Sharma, M., Singh, N. K., Dash, P. K., & Sreevathsa, R. (2020). Transgenic cotton (Gossypium hirsutum L.) to combat weed vagaries: Utility of an apical meristem-targeted in planta transformation strategy to introgress a modified CP4-EPSPS gene for glyphosate tolerance. Frontiers in Plant Science, 11, 768. https://doi.org/10.3389/fpls.2020.00768
  • Kaundun, S. S., Zelaya, I. A., Dale, R. P., Lycett, A. J., Carter, P., Sharples, K. R., & McIndoe, E. (2008). Importance of the P106S target-site mutation in conferring resistance to glyphosate in a goosegrass (Eleusine indica) population from the Philippines. Weed Science, 56(5), 637–646. https://doi.org/10.3390/agronomy3020474
  • Kishore, G. M., & Shah, D. M. (1988). Amino acid biosynthesis inhibitors as herbicides. Annual Review of Biochemistry, 57(1), 627–663. https://doi.org/10.1146/annurev.bi.57.070188.003211
  • Leino, L., Tall, T., Helander, M., Saloniemi, I., Saikkonen, K., Ruuskanen, S., & Puigbò, P. (2021). Classification of the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase) for assessing sensitivity of organisms to the herbicide. Journal of Hazardous Materials, 408, 124556. https://doi.org/10.1016/j.jhazmat.2020.124556
  • Levin, J. G., & Sprinson, D. B. (1964). The enzymatic formation and isolation of 3-enolypyruvy l shikimate 5-phosphate. Journal of Biological Chemistry, 239(4), 1142–1150. https://doi.org/10.1016/S0021-9258(18)91404-3
  • Li, J., Meng, X., Zong, Y., Chen, K., Zhang, H., Liu, J., Li, J., & Gao, C. (2016). Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nature Plants, 2, 16139. https://doi.org/10.1038/nplants.2016.139
  • Mao, C., Xie, H., Chen, S., Valverde, B. E., & Qiang, S. (2017). Error-prone PCR mutation of Ls-EPSPS gene from Liriope spicata conferring to its enhanced glyphosate-resistance. Pesticide Biochemistry and Physiology, 141, 90–95. https://doi.org/10.1016/j.pestbp.2016.12.004
  • Moehs, C. P., Austill, W. J., Facciotti, D., Holm, A., Loeffler, D., Lu, Z., Mullenberg, J. C., Slade, A. J., Steine, M. N., Boxtel, J. V., & McGuire, C. (2020). Development of non-transgenic glyphosate tolerant wheat by TILLING. bioRxiv. https://doi.org/10.1101/2020.07.23.218883
  • Murphy, B. P., & Tranel, P. J. (2019). Target-site mutations conferring herbicide resistance. Plants, 8, 382. https://doi.org/10.3390/plants8100382
  • Mutte, S. K., & Weijers, D. (2020). High-resolution and deep phylogenetic reconstruction of ancestral states from large transcriptomic data sets. Bio-protocol, 10(6), e3566. https://doi.org/10.21769/BioProtoc.3566
  • Nandula, V., Ray, J., Ribeiro, D., Pan, Z., & Reddy, K. (2013). Glyphosate resistance in tall waterhemp (Amaranthus tuberculatus) from Mississippi is due to both altered target-site and nontarget-site mechanisms. Weed Science, 61(3), 374–383. https://doi.org/10.1614/WS-D-12-00155.1
  • Ouyang, C., Liu, W., Chen, S., Zhao, H., Chen, X., Jin, X., Li, X., Wu, Y., Zeng, X., Huang, P., He, X., & An, B. (2021). The naturally evolved EPSPS from goosegrass confers high glyphosate resistance to rice. Frontiers in Plant Science, 12, 756116. https://doi.org/10.3389/fpls.2021.756116
  • Park, K. B., Roh, J. Y., Kim, S. Y., Kim, N., Jo, Y. H., Jeong, R., Lee, W., Lee, H., Cho, S., Lee, Y. S., & Han, Y. S. (2021). Deep sequencing and phylogenetic analysis of severe fever with thrombocytopenia syndrome virus from the tick, Haemaphysalis longicornis, in Korea. Entomological Research, 51(1), 3–11. https://doi.org/10.1111/1748-5967.12478
  • Patterson, E. L., Saski, C. A., Sloan, D. B., Tranel, P. J., Westra, P., & Gaines, T. A. (2019). The draft genome of Kochia scoparia and the mechanism of glyphosate resistance via transposon-mediated EPSPS tandem gene duplication. Genome Biology and Evolution, 11(10), 2927–2940. https://doi.org/10.1093/gbe/evz198
  • Sastry, G. M., Adzhigirey, M., Day, T., Annabhimoju, R., & Sherman, W. (2013). Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments. Journal of Computer-Aided Molecular Design, 27(3), 221–234. https://doi.org/10.1007/s10822-013-9644-8
  • Sauer, N. J., Narváez-Vásquez, J., Mozoruk, J., Miller, R. B., Warburg, Z. J., Woodward, M. J., Mihiret, Y. A., Lincoln, T. A., Segami, R. E., Sanders, S. L., Walker, K. A., Beetham, P. R., Schöpke, C. R., & Gocal, G. F. (2016). Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiology, 170(4), 1917–1928. https://doi.org/10.1104/pp.15.01696
  • Soltis, P., & Soltis, D. (2003). Applying the bootstrap in phylogeny reconstruction. Statistical Science, 18(2), 256-267. https://doi.org/10.1214/ss/1063994980
  • Sony, S. K., Kaul, T., Motelb, K. F. A., Thangaraj, A., Bharti, J., Kaul, R., Verma, R., & Nehra, M. (2023). CRISPR-Cas9–mediated homology donor repair base editing system to confer herbicide resistance in rice (Oryza sativa L.). Frontiers in Plant Science, 14, 1122926. https://doi.org/10.3389/fpls.2023.1122926
  • Stallings, W. C., Abdel-Meguid, S. S., Lim, L. W., Shieh, H. S., Dayringer, H. E., Leimgruber, N. K., Stegeman, R. A., Anderson, K. S., Sikorski, J. A., Padgette, S. R., & Kishore, G. M. (1991). Structure and topological symmetry of the glyphosate target 5-enolpyruvylshikimate-3-phosphate synthase: A distinctive protein fold. Proceedings of the National Academy of Sciences of the United States of America, 88(11), 5046–5050. https://doi.org/10.1128/ecosalplus.3.6.1.8
  • Stecher, G., Tamura, K., & Kumar, S. (2020). Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution, 37(4), 1237–1239. https://doi.org/10.1093/molbev/msz312
  • Tall, T., & Puigbò, P. (2022). Rethinking the intrinsic sensitivity of fungi to glyphosate. BioTech, 11(3), 28. https://doi.org/10.3390/biotech11030028
  • Tall, T., & Puigbò, P. (2020). The glyphosate target enzyme 5-enolpyruvyl shikimate 3 phosphate synthase (EPSPS) contains several EPSPS-associated domains in fungi. Proceedings, 76, 6. https://doi.org/10.3390/IECGE-07146
  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739. https://doi.org/10.1093/molbev/msr121
  • Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
  • Tan, X. L., Othman, R. Y., & Teo, C. H. (2020). Isolation and functional characterization of 5-enolpyruvylshikimate 3-phosphate synthase gene from glyphosate-tolerant Pseudomonas nitroreducens strains FY43 and FY47. 3 Biotech, 10(4), 183. https://doi.org/10.1007/s13205-020-02176-7
  • Tian, Y. S., Xu, J., Peng, R. H., Xiong, A. S., Xu, H., Zhao, W., Fu, X. Y., Han, H. J., & Yao, Q. H. (2013). Mutation by DNA shuffling of 5-enolpyruvylshikimate-3-phosphate synthase from Malus domestica for improved glyphosate resistance. Plant Biotechnology Journal, 11(7), 829–838. https://doi.org/10.1111/pbi.12074
  • Tohge, T., Watanabe, M., Hoefgen, R., & Fernie, A. R. (2013). Shikimate and phenylalanine biosynthesis in the green lineage. Frontiers in Plant Science, 4, 62. https://doi.org/10.3389/fpls.2013.00062
  • Vila-Aiub, M. M., Neve, P., & Powles, S. B. (2009). Fitness costs associated with evolved herbicide resistance alleles in plants. The New Phytologist, 184(4), 751–767. https://doi.org/10.1111/j.1469-8137.2009.03055.x
  • Wakelin, A. M., & Preston, C. (2006). Inheritance of glyphosate resistance in several populations of rigid ryegrass (Lolium rigidum) from Australia. Weed Science, 54(2), 212–219. https://www.jstor.org/stable/4539381
  • Wang, H., Li, K., Susko, E., & Roger, A. J. (2008). A class frequency mixture model that adjusts for site-specific amino acid frequencies and improves inference of protein phylogeny. BMC Evolutionary Biology, 8, 331. https://doi.org/10.1186/1471-2148-8-331
  • Wang, M., Mao, Y., Lu, Y., Tao, X., & Zhu, J. K. (2017). Multiplex gene editing in rice using the CRISPR-Cpf1 system. Molecular Plant, 10(7), 1011–1013. https://doi.org/10.1016/j.molp.2017.03.001
  • Wang, Z., Wan, L., Xin, Q., Zhang, X., Song, Y., Wang, P., Hong, D., Fan, Z., & Yang, G. (2021). Optimizing glyphosate tolerance in rapeseed by CRISPR/Cas9-based geminiviral donor DNA replicon system with Csy4-based single-guide RNA processing. Journal of Experimental Botany, 72(13), 4796–4808. https://doi.org/10.1093/jxb/erab167
  • Willow, S. Y., Xie, B., Lawrence, J., Eisenberg, R. S., & Minh, D. D. L. (2020). On the polarization of ligands by proteins. Physical Chemistry Chemical Physics, 22(21), 12044–12057. https://doi.org/10.1039/d0cp00376j
  • Xiao, P., Liu, Y., & Cao, Y. (2019). Overexpression of G10-EPSPS in soybean provides high glyphosate tolerance. Journal of Integrative Agriculture, 18(8), 1851–1858. https://doi.org/10.1016/s2095-3119(18)62124-0
  • Yadav, M., & Khandelwal, S. (2019). Homology modeling and molecular dynamics Simulation study of β carbonic anhydrase of Ascaris lumbricoides. Bioinformation, 15(8), 572–578. https://doi.org/10.6026/97320630015572
  • Yaqoob, U., Kaul, T., Pandey, S., & Nawchoo, I. A. (2016). In-silico characterization, structural modelling, docking studies and phylogenetic analysis of 5-enolpyruvylshikimate-3-phosphate synthase gene of Oryza sativa L. Medicinal & Aromatic Plants, 5(6), 274. https://doi.org/10.4172/2167-0412.1000274
  • Yu, Q., Jalaludin, A., Han, H., Chen, M., Sammons, R. D., & Powles, S. B. (2015). Evolution of a double amino acid substitution in the 5-enolpyruvylshikimate-3-phosphate synthase in Eleusine indica conferring high-level glyphosate resistance. Plant Physiology, 167(4), 1440–1447. https://doi.org/10.1104/pp.15.00146
  • Yuan, Y., Zhou, Z., Zhan, Y., Ke, X., Yan, Y., Lin, M., Li, P., Jiang, S., Wang, J., & Lu, W. (2022). A highly glyphosate-resistant EPSPS mutant from laboratory evolution. Applied Sciences, 12(11), 5723. https://doi.org/10.3390/app12115723
  • Zhou, M., Xu, H., Wei, X., Ye, Z., Wei, L., Gong, W., Wang, Y., & Zhu, Z. (2006). Identification of a glyphosate resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy. Plant Physiology, 140(1), 184–195. https://doi.org/10.1104/pp.105.068577

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