Functional characterization of Class II 5-enopyruvylshikimate-3-phosphate synthase from Halothermothrix orenii H168 in Escherichia coli and transgenic Arabidopsis

Applied Microbiology and Biotechnology

Volumn 93, Issue 1, 2012, Pages 241-250

  Tian, Yong Sheng ^a   Xu, Jing ^a   Xiong, Ai Sheng ^a   Zhao, Wei ^a   Gao, Feng ^a   Fu, Xiao Yan ^a   Peng, Ri He ^a   Yao, Quan Hong ^a  

^a INSTITUTE OF EDIBLE FUNGI   (China)

Author keywords

5 Enopyruvylshikimate 3 phosphate synthase; Enzyme kinetic values; Halothermothrix orenii; Transgenic Arabidopsis

Indexed keywords

AGROBACTERIUM TUMEFACIENS STRAIN; AMINO ACID RESIDUES; CLASS II; DNA SYNTHESISS; E. COLI; FULL-LENGTH ENZYMES; FUNCTIONAL CHARACTERIZATION; GLYPHOSATES; HALOTHERMOTHRIX ORENII; HIGH AFFINITY; KINETIC ANALYSIS; KINETIC VALUES; PHOSPHOENOLPYRUVATES; PURIFIED ENZYME; SITE DIRECTED MUTAGENESIS; SYNTHASES; TRANSGENIC ARABIDOPSIS; TUMEFACIENS;

AMINO ACIDS; BEHAVIORAL RESEARCH; CLONING; ENZYMES; ESCHERICHIA COLI; GENE ENCODING; HERBICIDES; KINETICS; PLANTS (BOTANY); SYNTHESIS (CHEMICAL);

POLYMERASE CHAIN REACTION;

5 ENOPYRUVYLSHIKIMATE 3 PHOSPHATE SYNTHASE; GLYPHOSATE; PHOSPHOENOLPYRUVATE; SYNTHETASE; UNCLASSIFIED DRUG;

COLIFORM BACTERIUM; DICOTYLEDON; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GENE EXPRESSION; KINETIC ENERGY; TRANSGENIC PLANT;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HALOPHILE; HALOTHERMOTHRIX ORENII; NONHUMAN; POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; TRANSGENIC PLANT;

3-PHOSPHOSHIKIMATE 1-CARBOXYVINYLTRANSFERASE; ARABIDOPSIS; CLONING, MOLECULAR; DNA, BACTERIAL; DRUG RESISTANCE; ESCHERICHIA COLI; GENE EXPRESSION; GLYCINE; GRAM-POSITIVE BACTERIA; HERBICIDES; KINETICS; MUTAGENESIS, SITE-DIRECTED; PHOSPHOENOLPYRUVATE; PLANTS, GENETICALLY MODIFIED; POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

AGROBACTERIUM TUMEFACIENS; ARABIDOPSIS; ESCHERICHIA COLI; HALOTHERMOTHRIX ORENII;

EID: 84856267353     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3443-8     Document Type: Article

References (44)

1. SR Baerson DJ Rodriguez M Tran Y Feng NA Biest GM Dill 2002 Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase Plant Physiol 129 1265 1275 10.1104/pp.001560 1:CAS:528:DC%2BD38XlsFajtrw%3D 10.1104/pp.001560
2. R Bentley 1990 The Shikimate pathway-a metabolic tree with many branches Crit Rev Biochem Mol Biol 25 307 384 10.3109/10409239009090615 1:CAS:528:DyaK3MXit1emu7c%3D 10.3109/10409239009090615
3. PJ Berti P Chindemi 2009 Catalytic residues and an electrostatic sandwich that promote enolpyruvyl shikimate 3-phosphate synthase (AroA) catalysis Biochemistry 48 3699 3707 10.1021/bi802251s 1:CAS:528:DC%2BD1MXksVSlsrY%3D 10.1021/bi802251s
4. JL Cayol B Ollivier BK Patel G Prensier J Guezennec JL Garcia 1994 Isolation and characterization of Halothermothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fermentative, strictly anaerobic bacterium Int J Syst Bacteriol 44 534 540 1:CAS:528:DyaK2cXmsFWju7Y%3D 10.1099/00207713-44-3-534
5. L Chen S Pradhan TC Evans Jr 2001 Herbicide resistance from a divided EPSPS protein: the split Synechocystis DnaE intein as an in vivo affinity domain Gene 263 39 48 1:CAS:528:DC%2BD3MXht1Okurg%3D 10.1016/S0378-1119(00)00568-0
6. G Della-Cioppa SC Bauer BK Klein DM Shah RT Fraley GM Kishore 1986 Translocation of the precursor of 5-enolpyruvylshikimate-3-phosphate synthase into chloroplasts of higher plants in vitro Proc Natl Acad Sci USA 83 6873 6877 1:CAS:528:DyaL28XlsV2rtrk%3D 10.1073/pnas.83.18.6873
7. GM Dill CA Cajacob SR Padgette 2008 Glyphosate-resistant crops: adoption, use and future considerations Pest Manag Sci 64 326 331 10.1002/ps.1501 1:CAS:528:DC%2BD1cXksVGqtLk%3D 10.1002/ps.1501
8. S Eschenburg ML Healy MA Priestman GH Lushington E Schönbrunn 2002 How the mutation glycine96 to alanine confers glyphosate insensitivity to 5-enolpyruvyl shikimate-3-phosphate synthase from Escherichia coli Planta 216 129 135 10.1007/s00425-002-0908-0 1:CAS:528:DC%2BD38Xps1ehtL0%3D 10.1007/s00425-002-0908-0
9. Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: a unique global herbicide. American Chemical Society Monograph 189, American Chemical Society, Washington DC
10. T Funke H Han ML Healy-Fried M Fischer E Schönbrunn 2006 Molecular basis for the herbicide resistance of Roundup Ready crops Proc Natl Acad Sci USA 103 13010 13015 1:CAS:528:DC%2BD28XptlWju7s%3D 10.1073/pnas.0603638103
11. T Funke Y Yang H Han M Healy-Fried S Olesen A Becker E Schönbrunn 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 J Biol Chem 284 9854 9860 1:CAS:528:DC%2BD1MXjvFKrsr8%3D 10.1074/jbc.M809771200
12. Haslam E (1993) Shikimic acid: metabolism and metabolites. John Wiley and Sons, New York
13. M He ZY Yang YF Nie J Wang P Xu 2001 A new type of class I bacterial 5-enopyruvylshikimate-3-phosphate synthase mutants with enhanced tolerance to glyphosate Biochim Biophys Acta 1568 1 6 1:CAS:528:DC%2BD3MXos1Kiu7s%3D 10.1016/S0304-4165(01)00181-7
14. M He YF Nie P Xu 2003 A T42M substitution in bacterial 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) generates enzymes with increased resistance to glyphosate Biosci Biotechnol Biochem 67 1405 1409 1:CAS:528:DC%2BD3sXltlens78%3D 10.1271/bbb.67.1405
15. ML Healy-Fried T Funke MA Priestman H Han E Schönbrunn 2007 Structural basis of glyphosate tolerance resulting from mutations of Pro101 in Escherichia coli 5-enolpyruvylshikimate-3-phosphate synthase J Biol Chem 282 32949 32955 1:CAS:528:DC%2BD2sXht1Clur7N 10.1074/jbc.M705624200
16. D Kahrizi AH Salmanian A Afshari A Moieni A Mousavi 2007 Simultaneous substitution of Gly96 to Ala and Ala183 to Thr in 5-enolpyruvylshikimate-3- phosphate synthase gene of E. coli (K12) and transformation of rapeseed (Brassica napus L.) in order to make tolerance to glyphosate Plant Cell Rep 26 95 104 10.1007/s00299-006-0208-4 1:CAS:528:DC%2BD28Xht12gs7jN 10.1007/s00299-006-0208-4
17. GM Kishore DM Shah 1988 Amino acid biosynthesis inhibitors as herbicides Annu Rev Biochem 57 627 663 1:CAS:528:DyaL1cXkvVyjsLs%3D 10.1146/annurev.bi.57. 070188.003211
18. HJ Klee YM Muskopf CS Gasser 1987 Cloning of an Arabidopsis thaliana gene encoding 5-enolpyruvylshikimate-3-phosphate synthase: sequence analysis and manipulation to obtain glyphosate-tolerant plants Mol Gen Genet 210 437 442 1:CAS:528:DyaL1cXitFOjurs%3D 10.1007/BF00327194
19. PA Lanzetta LJ Alvarez PS Reinach OA Candia 1979 An improved assay for nanomole amounts of inorganic phosphate Anal Biochem 100 95 97 1:CAS:528:DyaL3cXlsVGhuw%3D%3D 10.1016/0003-2697(79)90115-5
20. L Li W Lu Y Han S Ping W Zhang M Chen Z Zhao Y Yan Y Jiang M Lin 2009 A novel RPMXR motif among class II 5-enolpyruvylshikimate-3-phosphate synthases is required for enzymatic activity and glyphosate resistance J Biotechnol 144 330 336 1:CAS:528:DC%2BD1MXhsV2hur%2FP 10.1016/j.jbiotec.2009.09.014
21. A Liang J Sha W Lu M Chen L Li D Jin Y Yan J Wang S Ping W Zhang Y Wang M Lin 2008 A single residue mutation of 5-enoylpyruvylshikimate-3-phosphate synthase in Pseudomonas stutzeri enhances resistance to the herbicide glyphosate Biotechnol Lett 30 1397 1401 10.1007/s10529-008-9703-8 1:CAS:528: DC%2BD1cXnsVCrs7s%3D 10.1007/s10529-008-9703-8
22. K Mavromatis N Ivanova I Anderson A Lykidis SD Hooper H Sun V Kunin A Lapidus P Hugenholtz B Patel NC Kyrpides 2009 Genome analysis of the anaerobic thermohalophilic bacterium Halothermothrix orenii PLoS One 4 1 e4192 10.1371/journal.pone.0004192 10.1371/journal.pone.0004192
23. S Mizyed JE Wright B Byczynski PJ Berti 2003 Identification of the catalytic residues of AroA (enolpyruvylshikimate 3-phosphate synthase) using partitioning analysis Biochemistry 42 6986 6995 10.1021/bi027217l 1:CAS:528:DC%2BD3sXjvFCnt7c%3D 10.1021/bi027217l
24. T Murashige F Skoog 1962 A revised medium for rapid growth and bio assays with tobacco tissue cultures Plant Physiol 15 473 497 1:CAS:528:DyaF3sXksFKm 10.1111/j.1399-3054.1962.tb08052.x
25. EE Murray J Lotzer M Eberle 1989 Codon usage in plant genes Nucleic Acids Res 17 477 498 1:CAS:528:DyaL1MXht12ktb4%3D 10.1093/nar/17.2.477
26. SR Padgette QK Huynh S Aykent RD Sammons JA Sikorski GM Kishore 1988 Identification of the reactive cysteines of Escherichia coli 5-enolpyruvylshikimate-3-phosphate synthase and their nonessentiality for enzymatic catalysis J Biol Chem 263 1798 1802 1:CAS:528:DyaL1cXht1Olsrw%3D
27. SR Padgette DB Re CS Gasser DA Eichholtz RB Frazier CM Hironaka EB Levine DM Shah RT Fraley GM Kishore 1991 Site-directed mutagenesis of a conserved region of the 5-enolpyruvylshikimate-3-phosphate synthase active site J Biol Chem 266 22364 22369 1:CAS:528:DyaK3MXmslCnurg%3D
28. RH Peng AS Xiong QH Yao 2006 A direct and efficient PAGE-mediated overlap extension PCR method for gene multiple-site mutagenesis Appl Microbiol Biotechnol 73 234 240 10.1007/s00253-006-0583-3 1:CAS:528:DC%2BD28XhtFSnsLjK 10.1007/s00253-006-0583-3
29. E Schönbrunn S Eschenburg WA Shuttleworth JV Schloss N Amrhein JN Evans W Kabsch 2001 Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail Proc Natl Acad Sci USA 98 1376 1380 10.1073/pnas.98.4.137698/4/1376 10.1073/pnas.98.4.1376
30. Spencer M, Mumm R, Gwyn J (2000) Glyphosate tolerant maize line. U.S. patent no. 6040497.
31. DM Stalker WR Hiatt L Comai 1985 A single amino acid substitution in the enzyme 5-enolpyruvylshikimate-3-phosphate synthase confers resistance to the herbicide glyphosate J Biol Chem 260 4724 4728 1:CAS:528:DyaL2MXitFKitrc%3D
32. WC Stallings SS Abdel-Meguid LW Lim HS Shieh HE Dayringer NK Leimgruber RA Stegeman KS Anderson JA Sikorski SR Padgette GM Kishore 1991 Structure and topological symmetry of the glyphosate target 5-enolpyruvylshikimate-3-phosphate synthase: a distinctive protein fold Proc Natl Acad Sci USA 88 5046 5050 1:CAS:528:DyaK3MXmtVWqsro%3D 10.1073/pnas.88.11.5046
33. HC Steinrücken N Amrhein 1980 The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase Biochem Biophys Res Commun 94 1207 1212 10.1016/0006-291X(80)90547-1
34. YC Sun YC Chen ZX Tian FM Li XY Wang J Zhang ZL Xiao M Lin N Gilmartin DN Dowling YP Wang 2005 Novel AroA with high tolerance to glyphosate, encoded by a gene of Pseudomonas putida 4G-1 isolated from an extremely polluted environment in China Appl Environ Microbiol 71 4771 4776 1:CAS:528:DC%2BD2MXoslGhs7o%3D 10.1128/AEM.71.8.4771-4776.2005
35. YS Tian AS Xiong J Xu W Zhao F Gao XY Fu H Xu JL Zheng RH Peng QH Yao 2010 Isolation from Ochrobactrum anthropi of a novel class II 5-enopyruvylshikimate-3-phosphate synthase with high tolerance to glyphosate Appl Environ Microbiol 76 6001 6005 1:CAS:528:DC%2BC3cXht1WmsL%2FN 10.1128/AEM.00770-10
36. P Vaithanomsat KA Brown 2007 Isolation and mutation of recombinant EPSP synthase from pathogenic bacteria Pseudomonas aeruginosa Proc Biochem 42 592 598 1:CAS:528:DC%2BD2sXjtFGlsbw%3D 10.1016/j.procbio.2006.11.006
37. AS Xiong QH Yao RH Peng H Duan X Li HQ Fan ZM Cheng Y Li 2006 PCR-based accurate synthesis of long DNA sequences Nat Protoc 1 791 797 1:CAS:528:DC%2BD28XhtFOitLfN 10.1038/nprot.2006.103
38. AS Xiong RH Peng JG Liu J Zhuang YS Qiao F Xu B Cai Z Zhang JM Chen QH Yao 2007 High efficiency and throughput system in directed evolution in vitro of reporter gene Appl Microbiol Biotechnol 74 160 168 10.1007/s00253-006-0659-0 1:CAS:528:DC%2BD2sXhtVagu7s%3D 10.1007/s00253-006-0659-0
39. H Xu AS Xiong W Zhao YS Tian RH Peng JM Chen QH Yao 2010 Characterization of a glucose-, xylose-, sucrose-, and D-galactose-stimulated β-glucosidase from the alkalophilic bacterium Bacillus halodurans C-125 Curr Microbiol 62 833 839 10.1007/s00284-010-9766-3 10.1007/s00284-010-9766-3
40. J Xu YS Tian RH Peng AS Xiong B Zhu XF Jin F Gao XY Fu XL Hou QH Yao 2010 AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis Planta 231 1251 1260 10.1007/s00425-010-1122-0 1:CAS:528:DC%2BC3cXkslSjtb4%3D 10.1007/s00425-010- 1122-0
41. Y Xue R Peng A Xiong X Li D Zha Q Yao 2009 Yeast heat-shock protein gene HSP26 enhances freezing tolerance in Arabidopsis J Plant Physiol 166 844 850 1:CAS:528:DC%2BD1MXmsFWjtb0%3D 10.1016/j.jplph.2008.11.013
42. X Zhang R Henriques SS Lin QW Niu NH Chua 2006 Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method Nat Protoc 1 641 646 1:CAS:528:DC%2BD28XhtFOitLnP 10.1038/nprot.2006.97
43. H Zhao W Zha 2006 In vitro 'sexual' evolution through the PCR-based staggered extension process (StEP) Nat Protoc 1 1865 1871 1:CAS:528: DC%2BD2sXhtFagtrjN 10.1038/nprot.2006.309
44. M Zhou H Xu X Wei Z Ye L Wei W Gong Y Wang Z Zhu 2006 Identification of a glyphosate-resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy Plant Physiol 140 184 195 1:CAS:528:DC%2BD28XhtVCgsbg%3D 10.1104/pp.105.068577