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Structural basis of glyphosate tolerance resulting from mutations of Pro101 in Escherichia coli 5-enolpyruvylshikimate-3-phosphate synthase.

Healy-Fried ML, Funke T, Priestman MA, Han H, Schönbrunn E
J Biol Chem 282 32949-55 (2007)
Related entries: 2qfq, 2qfs, 2qft

Cited: 46 times
EuropePMC logo PMID: 17855366

Abstract

Glyphosate, the world's most used herbicide, is a massive success because it enables efficient weed control with minimal animal and environmental toxicity. The molecular target of glyphosate is 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), which catalyzes the sixth step of the shikimate pathway in plants and microorganisms. Glyphosate-tolerant variants of EPSPS constitute the basis of genetically engineered herbicide-tolerant crops. A single-site mutation of Pro(101) in EPSPS (numbering according to the enzyme from Escherichia coli) has been implicated in glyphosate-resistant weeds, but this residue is not directly involved in glyphosate binding, and the basis for this phenomenon has remained unclear in the absence of further kinetic and structural characterization. To probe the effects of mutations at this site, E. coli EPSPS enzymes were produced with glycine, alanine, serine, or leucine substituted for Pro(101). These mutant enzymes were analyzed by steady-state kinetics, and the crystal structures of the substrate binary and substrate.glyphosate ternary complexes of P101S and P101L EPSPS were determined to between 1.5- and 1.6-A resolution. It appears that residues smaller than leucine may be substituted for Pro(101) without decreasing catalytic efficiency. Any mutation at this site results in a structural change in the glyphosate-binding site, shifting Thr(97) and Gly(96) toward the inhibitor molecule. We conclude that the decreased inhibitory potency observed for glyphosate is a result of these mutation-induced long-range structural changes. The implications of our findings concerning the development and spread of glyphosate-resistant weeds are discussed.

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  1. Application of the PM6 semi-empirical method to modeling proteins enhances docking accuracy of AutoDock. Bikadi Z, Hazai E. J Cheminform 1 15 (2009)
  2. Virtual screening of natural products against 5-enolpyruvylshikimate-3-phosphate synthase using the Anagreen herbicide-like natural compound library. de Oliveira MVD, Bittencourt Fernandes GM, da Costa KS, Vakal S, Lima AH. RSC Adv 12 18834-18847 (2022)


Reviews citing this publication (8)

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  4. Structural basis of glyphosate resistance resulting from the double mutation Thr97 -> Ile and Pro101 -> Ser in 5-enolpyruvylshikimate-3-phosphate synthase from Escherichia coli. Funke T, Yang Y, Han H, Healy-Fried M, Olesen S, Becker A, Schönbrunn E. J Biol Chem 284 9854-9860 (2009)
  5. Mutations and amplification of EPSPS gene confer resistance to glyphosate in goosegrass (Eleusine indica). Chen J, Huang H, Zhang C, Wei S, Huang Z, Chen J, Wang X. Planta 242 859-868 (2015)
  6. Improvement of glyphosate resistance through concurrent mutations in three amino acids of the Ochrobactrum 5-enopyruvylshikimate-3-phosphate synthase. Tian YS, Xu J, Xiong AS, Zhao W, Fu XY, Peng RH, Yao QH. Appl Environ Microbiol 77 8409-8414 (2011)
  7. Physical Mapping of Amplified Copies of the 5-Enolpyruvylshikimate-3-Phosphate Synthase Gene in Glyphosate-Resistant Amaranthus tuberculatus. Dillon A, Varanasi VK, Danilova TV, Koo DH, Nakka S, Peterson DE, Tranel PJ, Friebe B, Gill BS, Jugulam M. Plant Physiol 173 1226-1234 (2017)
  8. Target and Non-target Site Mechanisms Developed by Glyphosate-Resistant Hairy beggarticks (Bidens pilosa L.) Populations from Mexico. Alcántara-de la Cruz R, Fernández-Moreno PT, Ozuna CV, Rojano-Delgado AM, Cruz-Hipolito HE, Domínguez-Valenzuela JA, Barro F, De Prado R. Front Plant Sci 7 1492 (2016)
  9. Isolation from Ochrobactrum anthropi of a novel class II 5-enopyruvylshikimate-3-phosphate synthase with high tolerance to glyphosate. Tian YS, Xiong AS, Xu J, Zhao W, Gao F, Fu XY, Xu H, Zheng JL, Peng RH, Yao QH. Appl Environ Microbiol 76 6001-6005 (2010)
  10. Concerted action of target-site mutations and high EPSPS activity in glyphosate-resistant junglerice (Echinochloa colona) from California. Alarcón-Reverte R, García A, Watson SB, Abdallah I, Sabaté S, Hernández MJ, Dayan FE, Fischer AJ. Pest Manag Sci 71 996-1007 (2015)
  11. A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. Cao G, Liu Y, Zhang S, Yang X, Chen R, Zhang Y, Lu W, Liu Y, Wang J, Lin M, Wang G. PLoS One 7 e38718 (2012)
  12. Identification of the first glyphosate transporter by genomic adaptation. Wicke D, Schulz LM, Lentes S, Scholz P, Poehlein A, Gibhardt J, Daniel R, Ischebeck T, Commichau FM. Environ Microbiol 21 1287-1305 (2019)
  13. A novel 5-enolpyruvylshikimate-3-phosphate synthase from Rahnella aquatilis with significantly reduced glyphosate sensitivity. Peng RH, Tian YS, Xiong AS, Zhao W, Fu XY, Han HJ, Chen C, Jin XF, Yao QH. PLoS One 7 e39579 (2012)
  14. Functional characterization of Class II 5-enopyruvylshikimate-3-phosphate synthase from Halothermothrix orenii H168 in Escherichia coli and transgenic Arabidopsis. Tian YS, Xu J, Xiong AS, Zhao W, Gao F, Fu XY, Peng RH, Yao QH. Appl Microbiol Biotechnol 93 241-250 (2012)
  15. Multiple mechanism confers natural tolerance of three lilyturf species to glyphosate. Mao C, Xie H, Chen S, Valverde BE, Qiang S. Planta 243 321-335 (2016)
  16. Mutation by DNA shuffling of 5-enolpyruvylshikimate-3-phosphate synthase from Malus domestica for improved glyphosate resistance. Tian YS, Xu J, Peng RH, Xiong AS, Xu H, Zhao W, Fu XY, Han HJ, Yao QH. Plant Biotechnol J 11 829-838 (2013)
  17. Desensitizing plant EPSP synthase to glyphosate: Optimized global sequence context accommodates a glycine-to-alanine change in the active site. Dong Y, Ng E, Lu J, Fenwick T, Tao Y, Bertain S, Sandoval M, Bermudez E, Hou Z, Patten P, Lassner M, Siehl D. J Biol Chem 294 716-725 (2019)
  18. From tolerance to resistance: mechanisms governing the differential response to glyphosate in Chloris barbata. Bracamonte E, Silveira HMD, Alcántara-de la Cruz R, Domínguez-Valenzuela JA, Cruz-Hipolito HE, De Prado R. Pest Manag Sci 74 1118-1124 (2018)
  19. Amino Acid Biosynthetic Pathways Are Required for Klebsiella pneumoniae Growth in Immunocompromised Lungs and Are Druggable Targets during Infection. Silver RJ, Paczosa MK, McCabe AL, Balada-Llasat JM, Baleja JD, Mecsas J. Antimicrob Agents Chemother 63 e02674-18 (2019)
  20. Crystal structure of 5-enolpyruvylshikimate-3-phosphate (EPSP) synthase from the ESKAPE pathogen Acinetobacter baumannii. Sutton KA, Breen J, Russo TA, Schultz LW, Umland TC. Acta Crystallogr F Struct Biol Commun 72 179-187 (2016)
  21. Response to imazapyr and dominance relationships of two imidazolinone-tolerant alleles at the Ahasl1 locus of sunflower. Sala CA, Bulos M, Altieri E, Weston B. Theor Appl Genet 124 385-396 (2012)
  22. EPSPS duplication and mutation involved in glyphosate resistance in the allotetraploid weed species Poa annua L. Brunharo CACG, Morran S, Martin K, Moretti ML, Hanson BD. Pest Manag Sci 75 1663-1670 (2019)
  23. Editorial Editorial: Aromatic Amino Acid Metabolism. Han Q, Phillips RS, Li J. Front Mol Biosci 6 22 (2019)
  24. Genetic variation in Dip5, an amino acid permease, and Pdr5, a multiple drug transporter, regulates glyphosate resistance in S. cerevisiae. Rong-Mullins X, Ravishankar A, McNeal KA, Lonergan ZR, Biega AC, Creamer JP, Gallagher JEG. PLoS One 12 e0187522 (2017)
  25. Identification of a new gene encoding 5-enolpyruvylshikimate-3-phosphate synthase using genomic library construction strategy. Zhou CY, Tian YS, Xu ZS, Zhao W, Chen C, Bao WH, Bian L, Cai R, Wu AZ. Mol Biol Rep 39 10939-10947 (2012)
  26. Characterization of multiple-herbicide-resistant Italian ryegrass (Lolium perenne spp. multiflorum). Liu M, Hulting AG, Mallory-Smith CA. Pest Manag Sci 70 1145-1150 (2014)
  27. Does Glyphosate Affect the Human Microbiota? Puigbò P, Leino LI, Rainio MJ, Saikkonen K, Saloniemi I, Helander M. Life (Basel) 12 707 (2022)
  28. An intragenic approach to confer glyphosate resistance in chile (Capsicum annuum) by introducing an in vitro mutagenized chile EPSPS gene encoding for a glyphosate resistant EPSPS protein. Ortega JL, Rajapakse W, Bagga S, Apodaca K, Lucero Y, Sengupta-Gopalan C. PLoS One 13 e0194666 (2018)
  29. Evolution of Target-Site Resistance to Glyphosate in an Amaranthus palmeri Population from Argentina and Its Expression at Different Plant Growth Temperatures. Kaundun SS, Jackson LV, Hutchings SJ, Galloway J, Marchegiani E, Howell A, Carlin R, Mcindoe E, Tuesca D, Moreno R. Plants (Basel) 8 E512 (2019)
  30. Identifying Chloris Species from Cuban Citrus Orchards and Determining Their Glyphosate-Resistance Status. Bracamonte ER, Fernández-Moreno PT, Bastida F, Osuna MD, Alcántara-de la Cruz R, Cruz-Hipolito HE, De Prado R. Front Plant Sci 8 1977 (2017)
  31. The Triple Amino Acid Substitution TAP-IVS in the EPSPS Gene Confers High Glyphosate Resistance to the Superweed Amaranthus hybridus. García MJ, Palma-Bautista C, Rojano-Delgado AM, Bracamonte E, Portugal J, Alcántara-de la Cruz R, De Prado R. Int J Mol Sci 20 E2396 (2019)
  32. Unravelling the effect of two herbicide resistance mutations on acetolactate synthase kinetics and growth traits. Zhao N, Yan Y, Du L, Zhang X, Liu W, Wang J. J Exp Bot 71 3535-3542 (2020)
  33. Effects of glyphosate on soybean metabolism in strains bred for glyphosate-resistance. Li WY, Lu P, Xie H, Li GQ, Wang JX, Guo DY, Liang XY. Physiol Mol Biol Plants 25 523-532 (2019)
  34. Case Reports First high-quality draft genome of Ochrobactrum haematophilum P6BS-III, a highly glyphosate-tolerant strain isolated from agricultural soil in Argentina. Massot F, Gkorezis P, McAmmond B, d'Haen J, Van Hamme J, Merini LJ, Vangronsveld J, Thijs S. 3 Biotech 9 74 (2019)
  35. History and Outlook for Glyphosate-Resistant Crops. Green JM, Siehl DL. Rev Environ Contam Toxicol 255 67-91 (2021)
  36. Potential Role of EPSPS Mutations in the Resistance of Eleusine indica to Glyphosate. Chen J, Cui H, Li Z, Yu H, Hou Q, Li X. Int J Mol Sci 24 8250 (2023)


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