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. 1979 Aug;139(2):573–582. doi: 10.1128/jb.139.2.573-582.1979

Suppression of a deletion mutation in the glutamine amidotransferase region of the Salmonella typhimurium trpD gene by mutations in pheA and tyrA.

S Tanemura, R Bauerle
PMCID: PMC216906  PMID: 378978

Abstract

Prototrophic revertants of a trpD deletion mutant that lacks the glutamine amidotransferase domain of the bifunctional component II subunit of the anthranilate synthetase-phosphoribosyltransferase complex have been found to arise by the occurrence of sublethal missense mutations in either the pheA or tyrA loci. Such suppressor mutations were obtained directly by mutation of the wild-type pheA gene as well as indirectly by partial reversion of a variety of nonleaky pheA and tyrA mutations. The suppressor strains have only a portion of the normal level of the pheA or tyrA enzyme activity and thus experience a partial limitation in the synthesis of phenylalanine or tyrosine. This limitation leads to a relaxation of end-product regulation of the phenylalanine- or tyrosine-specific enzymes of the common aromatic pathway and to the overproduction of the branch point intermediate, chorismic acid, which is one of the substrates of the anthranilate synthetase reaction. It is proposed that the high intracellular level of chorismic acid acts to elevate the non-physiological NH3-dependent anthranilate synthetase activity of the component I subunit, thereby eliminating the need for the glutamine amidotransferase activity of the component II subunit. Consistent with this is the finding that phenylalanine and tyrosine are specific inhibitors of growth of the pheA and tyrA suppressor strains, respectively, causing a shutdown of the overproduction of chorismic acid by reestablishing normal end-product control of the common pathway.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bauerle R. H., Margolin P. A multifunctional enzyme complex in the tryptophan pathway of Salmonella typhimurium: comparison of polarity and pseudopolarity mutations. Cold Spring Harb Symp Quant Biol. 1966;31:203–214. doi: 10.1101/sqb.1966.031.01.028. [DOI] [PubMed] [Google Scholar]
  2. Bauerle R. H., Margolin P. The functional organization of the tryptophan gene cluster in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1966 Jul;56(1):111–118. doi: 10.1073/pnas.56.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Campbell J. H., Lengyel J. A., Langridge J. Evolution of a second gene for beta-galactosidase in Escherichia coli. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1841–1845. doi: 10.1073/pnas.70.6.1841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dayan J., Sprinson D. B. Enzyme alterations in tyrosine and phenylalanine auxotrophs of Salmonella typhimurium. J Bacteriol. 1971 Dec;108(3):1174–1180. doi: 10.1128/jb.108.3.1174-1180.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DeLeo A. B., Sprinson D. B. 3-Deoxy-D-arabino-heptulosonic acid 7-phosphate synthase mutants of Salmonella typhimurium. J Bacteriol. 1975 Dec;124(3):1312–1320. doi: 10.1128/jb.124.3.1312-1320.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Demerec M., Adelberg E. A., Clark A. J., Hartman P. E. A proposal for a uniform nomenclature in bacterial genetics. Genetics. 1966 Jul;54(1):61–76. doi: 10.1093/genetics/54.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gibson F. Chorismic acid: purification and some chemical and physical studies. Biochem J. 1964 Feb;90(2):256–261. doi: 10.1042/bj0900256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grieshaber M., Bauerle R. Monomeric and dimeric forms of component II of the anthranilate synthetase--anthranilate 5-phosphoribosylpyrophosphate phosphoribosyltransferase complex of Salmonella typhimurium. Implications concerning the mode of assembly of the complex. Biochemistry. 1974 Jan 15;13(2):373–383. doi: 10.1021/bi00699a024. [DOI] [PubMed] [Google Scholar]
  9. Grieshaber M. On the evolution of an oligocephalic enzyme. glutamine-chorismate-amidotransferase-free anthranilate phosphoribosyltransferases from mutant strains of Salmonella typhimurium. Z Naturforsch C. 1978 Mar-Apr;33(3-4):235–244. doi: 10.1515/znc-1978-3-412. [DOI] [PubMed] [Google Scholar]
  10. Held W. A., Smith O. H. Regulation of the Escherichia coli tryptophan operon by early reactions in the aromatic pathway. J Bacteriol. 1970 Jan;101(1):202–208. doi: 10.1128/jb.101.1.202-208.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Henderson E. J., Zalkin H. On the composition of anthranilate synthetase-anthranilate 5-phosphoribosylpyrophosphate phosphoribosyltransferase from Salmonella typhimurium. J Biol Chem. 1971 Nov 25;246(22):6891–6898. [PubMed] [Google Scholar]
  12. Hwang L. H., Zalkin H. Multiple forms of anthranilate synthetase-anthranilate 5-phosphoribosylpyrophosphate phosphoribosyltransferase from Salmonella typhimurium. J Biol Chem. 1971 Apr 25;246(8):2338–2345. [PubMed] [Google Scholar]
  13. Itikawa H., Baumberg S., Vogel H. J. Enzymic basis for a genetic suppression: accumulation and deacylation of N-acetylglutamic gamma-semialdehyde in enterobacterial mutants. Biochim Biophys Acta. 1968 Jul 9;159(3):547–550. doi: 10.1016/0005-2744(68)90142-3. [DOI] [PubMed] [Google Scholar]
  14. Jackson E. N., Yanofsky C. Localization of two functions of the phosphoribosyl anthranilate transferase of Escherichia coli to distinct regions of the polypeptide chain. J Bacteriol. 1974 Feb;117(2):502–508. doi: 10.1128/jb.117.2.502-508.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kemper J. Evolution of a new gene substituting for the leuD gene of Salmonella typhimurium: origin and nature of supQ and newD mutations. J Bacteriol. 1974 Dec;120(3):1176–1185. doi: 10.1128/jb.120.3.1176-1185.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kemper J., Margolin P. Suppression by gene substitution for the leuD gene of Salmonella typhimurium. Genetics. 1969 Oct;63(2):263–279. doi: 10.1093/genetics/63.2.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuo T. T., Stocker B. A. Suppression of proline requirement of proA and proAB deletion mutants in Salmonella typhimurium by mutation to arginine requirement. J Bacteriol. 1969 May;98(2):593–598. doi: 10.1128/jb.98.2.593-598.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Li H. C., Buchanan J. M. Biosynthesis of the purines. 33. Catalytic properties of the glutamine site of formylglycinamide ribonucleotide amidotransferase from chicken liver. J Biol Chem. 1971 Aug 10;246(15):4713–4719. [PubMed] [Google Scholar]
  20. Nagano H., Zalkin H., Henderson E. J. The anthranilate synthetase-anthranilate-5-phosphorribosylpyrophosphate phosphoribosyltransferase aggregate. On the reaction mechanism of anthranilate synthetase from Salmonella typhimurium. J Biol Chem. 1970 Aug 10;245(15):3810–3820. [PubMed] [Google Scholar]
  21. Nishioka Y., Demerec M., Eisenstark A. Genetic analysis of aromatic mutants of Salmonella typhimurium. Genetics. 1967 Jun;56(2):341–351. doi: 10.1093/genetics/56.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pinel J. P., Chorover S. L. Inhibition by arousal of epilepsy induced by chlorambucil in rats. Nature. 1972 Mar 31;236(5344):232–234. doi: 10.1038/236232a0. [DOI] [PubMed] [Google Scholar]
  23. Sanderson K. E., Hartman P. E. Linkage map of Salmonella typhimurium, edition V. Microbiol Rev. 1978 Jun;42(2):471–519. doi: 10.1128/mr.42.2.471-519.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schmit J. C., Zalkin H. Chorismate mutase-prephenate dehydratase. Partial purification and properties of the enzyme from Salmonella typhimurium. Biochemistry. 1969 Jan;8(1):174–181. doi: 10.1021/bi00829a025. [DOI] [PubMed] [Google Scholar]
  25. Schwartz D. O., Beckwith J. R. Mutagens which cause deletions in Escherichia coli. Genetics. 1969 Feb;61(2):371–376. doi: 10.1093/genetics/61.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Smith H. O., Levine M. A phage P22 gene controlling integration of prophage. Virology. 1967 Feb;31(2):207–216. doi: 10.1016/0042-6822(67)90164-x. [DOI] [PubMed] [Google Scholar]
  27. Tanemura S., Bauerle R. Internal reinitiation of translation in polar mutants of the trpB gene of Salmonella typhimurium. Mol Gen Genet. 1977 Jun 8;153(2):135–143. doi: 10.1007/BF00264728. [DOI] [PubMed] [Google Scholar]
  28. Trotta P. P., Burt M. E., Haschemeyer R. H., Meister A. Reversible dissociation of carbamyl phosphate synthetase into a regulated synthesis subunit and a subunit required for glutamine utilization. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2599–2603. doi: 10.1073/pnas.68.10.2599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Umbarger H. E. Amino acid biosynthesis and its regulation. Annu Rev Biochem. 1978;47:532–606. doi: 10.1146/annurev.bi.47.070178.002533. [DOI] [PubMed] [Google Scholar]
  30. Yanofsky C., Horn V., Bonner M., Stasiowski S. Polarity and enzyme functions in mutants of the first three genes of the tryptophan operon of Escherichia coli. Genetics. 1971 Dec;69(4):409–433. doi: 10.1093/genetics/69.4.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zalkin H. Anthranilate synthetase. Adv Enzymol Relat Areas Mol Biol. 1973;38:1–39. doi: 10.1002/9780470122839.ch1. [DOI] [PubMed] [Google Scholar]
  32. Zalkin H., Kling D. Anthranilate synthetase. Purification and properties of component I from Salmonella typhimurium. Biochemistry. 1968 Oct;7(10):3566–3573. doi: 10.1021/bi00850a034. [DOI] [PubMed] [Google Scholar]
  33. Zalkin H., Murphy T. Utilization of ammonia for tryptophan synthesis. Biochem Biophys Res Commun. 1975 Dec 15;67(4):1370–1377. doi: 10.1016/0006-291x(75)90178-3. [DOI] [PubMed] [Google Scholar]

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