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PMID: 1379177 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Co-ordinate expression of the two threonyl-tRNA synthetase genes in Bacillus subtilis: control by transcriptional antitermination involving a conserved regulatory sequence.

The EMBO journal ·Vol. 11 ·No. 8 ·1992-08-00 ·Pages 3117-27

Putzer H, Gendron N, Grunberg-Manago M

Abstract

In Bacillus subtilis, two genes, thrS and thrZ, encode distinct threonyl-tRNA synthetase enzymes. Normally, only the thrS gene is expressed. Here we show that either gene, thrS or thrZ, is sufficient for normal cell growth and sporulation. Reducing the intracellular ThrS protein concentration induces thrZ expression in a dose-compensatory manner. Starvation for threonine simultaneously induces thrZ and stimulates thrS expression. The 5'-leader sequences of thrS and thrZ contain, respectively, one and three transcription terminators preceded by a conserved sequence. We show that this sequence is essential for the regulation of thrS via a transcriptional antitermination mechanism. We propose that both genes, thrS and thrZ, are regulated by the same mechanism such that the additional regulatory domains present before thrZ account for its non-expression. In contrast to Escherichia coli, structurally similar regulatory domains, i.e. the consensus sequence preceding a terminator structure, are found in the leader regions of most aminoacyl-tRNA synthetase genes of Gram-positive bacteria. This suggests that they are regulated by a common mechanism.

Related Genes
MeSH Terms
Bacillus subtilis/enzymology,genetics Base Sequence Chromosomes, Bacterial DNA, Bacterial/genetics,metabolism Gene Expression Regulation, Bacterial Gene Expression Regulation, Enzymologic Genes, Bacterial Genes, Lethal Genes, Regulator Genotype Kinetics Molecular Sequence Data Multigene Family Open Reading Frames Plasmids RNA, Bacterial/genetics,isolation & purification Recombinant Fusion Proteins/isolation & purification,metabolism Suppression, Genetic Threonine-tRNA Ligase/genetics,isolation & purification,metabolism Transcription, Genetic beta-Galactosidase/genetics,metabolism
Chemicals
DNA, Bacterial RNA, Bacterial Recombinant Fusion Proteins beta-Galactosidase Threonine-tRNA Ligase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Putzer H
CNRS, URA 1139, Institut de Biologie Physico-Chimique, Paris, France.
Gendron N
Grunberg-Manago M
References (43)
43 references, click to expand
  1. Internal homologies in the two aspartokinase-homoserine dehydrogenases of Escherichia coli K-12.
    Proc Natl Acad Sci U S A. 1984 May;81(10):3019-23 PMID: 6374650
  2. Positive regulatory gene for temperature-controlled proteins in Escherichia coli.
    Biochem Biophys Res Commun. 1981 May 29;100(2):894-900 PMID: 7023474
  3. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  4. Identification of two copies of the gene for the elongation factor EF-Tu in E. coli.
    Nature. 1975 Oct 9;257(5526):458-62 PMID: 1101072
  5. Transcriptional regulation of the ilv-leu operon of Bacillus subtilis.
    J Bacteriol. 1992 May;174(10):3212-9 PMID: 1577690
  6. Analysis of the Bacillus subtilis tyrS gene: conservation of a regulatory sequence in multiple tRNA synthetase genes.
    J Bacteriol. 1992 Feb;174(4):1299-306 PMID: 1735721
  7. A gene encoding a tyrosine tRNA synthetase is located near sacS in Bacillus subtilis.
    DNA Seq. 1991;1(4):251-61 PMID: 1806041
  8. The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes.
    J Bacteriol. 1990 Jan;172(1):86-93 PMID: 2104615
  9. Induction of levansucrase in Bacillus subtilis: an antitermination mechanism negatively controlled by the phosphotransferase system.
    J Bacteriol. 1990 Feb;172(2):1043-50 PMID: 2105292
  10. The mtr locus is a two-gene operon required for transcription attenuation in the trp operon of Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8726-30 PMID: 2123343
  11. The sacT gene regulating the sacPA operon in Bacillus subtilis shares strong homology with transcriptional antiterminators.
    J Bacteriol. 1990 Jul;172(7):3966-73 PMID: 2163394
  12. Homology of lysS and lysU, the two Escherichia coli genes encoding distinct lysyl-tRNA synthetase species.
    Nucleic Acids Res. 1990 Jan 25;18(2):305-12 PMID: 2183178
  13. Multiple regulatory elements for the glpA operon encoding anaerobic glycerol-3-phosphate dehydrogenase and the glpD operon encoding aerobic glycerol-3-phosphate dehydrogenase in Escherichia coli: further characterization of respiratory control.
    J Bacteriol. 1990 Jan;172(1):179-84 PMID: 2403539
  14. In vivo synthesis of adenylylated bis(5'-nucleosidyl) tetraphosphates (Ap4N) by Escherichia coli aminoacyl-tRNA synthetases.
    Proc Natl Acad Sci U S A. 1989 Nov;86(21):8275-9 PMID: 2554306
  15. The pMTL nic- cloning vectors. I. Improved pUC polylinker regions to facilitate the use of sonicated DNA for nucleotide sequencing.
    Gene. 1988 Aug 15;68(1):139-49 PMID: 2851488
  16. Genetic mapping of rpoD implicates the major sigma factor of Bacillus subtilis RNA polymerase in sporulation initiation.
    Mol Gen Genet. 1985;201(1):88-95 PMID: 2997585
  17. cis-acting sites in the transcript of the Bacillus subtilis trp operon regulate expression of the operon.
    J Bacteriol. 1988 Jul;170(7):3080-8 PMID: 3133360
  18. Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis.
    Mol Microbiol. 1988 Nov;2(6):689-99 PMID: 3145384
  19. Cloning and nucleotide sequence of the structural gene coding for Bacillus subtilis tryptophanyl-tRNA synthetase.
    Gene. 1988 Dec 20;73(2):537-43 PMID: 3149612
  20. A transcription terminator in the 5' non-coding region of the tyrosyl tRNA synthetase gene from Bacillus stearothermophilus.
    Eur J Biochem. 1986 Aug 1;158(3):505-10 PMID: 3525162
  21. Genetic analysis of ribonucleic acid polymerase mutants of Bacillus subtilis.
    J Bacteriol. 1973 Apr;114(1):103-13 PMID: 4144588
  22. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  23. Recombinant plasmids capable to replication in B. subtilis and E. coli.
    Mol Gen Genet. 1978 Jun 1;162(1):59-67 PMID: 97514
  24. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination.
    Biochemistry. 1977 Oct 18;16(21):4743-51 PMID: 911786
  25. Transcriptional antitermination in the bgl operon of E. coli is modulated by a specific RNA binding protein.
    Cell. 1990 Sep 21;62(6):1153-63 PMID: 1698125
  26. Control of Escherichia coli lysyl-tRNA synthetase expression by anaerobiosis.
    J Bacteriol. 1991 Dec;173(24):7903-10 PMID: 1744045
  27. Methionyl-tRNA synthetase from Bacillus stearothermophilus: structural and functional identities with the Escherichia coli enzyme.
    Nucleic Acids Res. 1991 Jul 11;19(13):3673-81 PMID: 1852609
  28. Independent genes for two threonyl-tRNA synthetases in Bacillus subtilis.
    J Bacteriol. 1990 Aug;172(8):4593-602 PMID: 2115870
  29. Structure and nucleotide sequence of the Bacillus subtilis phenylalanyl-tRNA synthetase genes.
    Biochimie. 1990 Oct;72(10):725-34 PMID: 2127701
  30. BISANCE: a French service for access to biomolecular sequence databases.
    Comput Appl Biosci. 1990 Oct;6(4):355-6 PMID: 2257496
  31. On finding all suboptimal foldings of an RNA molecule.
    Science. 1989 Apr 7;244(4900):48-52 PMID: 2468181
  32. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution.
    Proc Natl Acad Sci U S A. 1989 Apr;86(7):2172-5 PMID: 2648393
  33. Cloning and complete nucleotide sequence of the Bacillus stearothermophilus tryptophanyl tRNA synthetase gene.
    Gene. 1986;46(1):37-45 PMID: 3026925
  34. Cloning and nucleotide sequence of the Bacillus subtilis hom gene coding for homoserine dehydrogenase. Structural and evolutionary relationships with Escherichia coli aspartokinases-homoserine dehydrogenases I and II.
    J Biol Chem. 1988 Oct 15;263(29):14654-60 PMID: 3139660
  35. The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing.
    EMBO J. 1988 Feb;7(2):473-83 PMID: 3284745
  36. A protein required for splicing group I introns in Neurospora mitochondria is mitochondrial tyrosyl-tRNA synthetase or a derivative thereof.
    Cell. 1987 Jul 31;50(3):331-45 PMID: 3607872
  37. Catabolic repression of bacterial sporulation.
    Proc Natl Acad Sci U S A. 1965 Sep;54(3):704-11 PMID: 4956288
  38. Use of phi(glp-lac) in studies of respiratory regulation of the Escherichia coli anaerobic sn-glycerol-3-phosphate dehydrogenase genes (glpAB).
    J Bacteriol. 1984 Feb;157(2):591-8 PMID: 6363389
  39. New versatile cloning and sequencing vectors based on bacteriophage M13.
    Gene. 1983 Dec;26(1):91-9 PMID: 6323254
  40. Escherichia coli K-12 lysyl-tRNA synthetase mutant with a novel reversion pattern.
    J Bacteriol. 1984 May;158(2):615-20 PMID: 6373723
  41. Evolutionary divergence of genes for ornithine and aspartate carbamoyl-transferases--complete sequence and mode of regulation of the Escherichia coli argF gene; comparison of argF with argI and pyrB.
    Nucleic Acids Res. 1984 Aug 10;12(15):6277-89 PMID: 6382166
  42. Posttranscriptional modification of mRNA conformation: mechanism that regulates erythromycin-induced resistance.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7079-83 PMID: 6938954
  43. Multiple forms of lysyl-transfer ribonucleic acid synthetase in Escherichia coli.
    J Bacteriol. 1981 Apr;146(1):345-51 PMID: 7012120
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-08-00
Pages
3117-27
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556796
Subset
IM
Databases
GENBANK
X04963, X66121, X66358, X66359, X66360, X66361, X66362, X66363, X66364, X66365
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