Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 Feb;171(2):1028–1034. doi: 10.1128/jb.171.2.1028-1034.1989

Genetic characterization of frameshift suppressors with new decoding properties.

D Hughes 1, S Thompson 1, M O'Connor 1, T Tuohy 1, B P Nichols 1, J F Atkins 1
PMCID: PMC209697  PMID: 2644219

Abstract

Suppressor mutants that cause ribosomes to shift reading frame at specific and new sequences are described. Suppressors for trpE91, the only known suppressible -1 frameshift mutant, have been isolated in Escherichia coli and in Salmonella typhimurium. E. coli hopR acts on trpE91 within the 9-base-pair sequence GGA GUG UGA, is dominant, and is located at min 52 on the chromosome. Its Salmonella homolog maps at an equivalent position and arises as a rarer class in that organism as compared with E. coli. The Salmonella suppressor, hopE, believed to be in a duplicate copy of the same gene, maps at min 17. The +1 suppressor, sufT, acts at the nonmonotonous sequence CCGU, is dominant, and maps at min 59 on the Salmonella chromosome.

Full text

PDF
1034

Selected References

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

  1. An G., Friesen J. D. The nucleotide sequence of tufB and four nearby tRNA structural genes of Escherichia coli. Gene. 1980 Dec;12(1-2):33–39. doi: 10.1016/0378-1119(80)90013-x. [DOI] [PubMed] [Google Scholar]
  2. Atkins J. F., Nichols B. P., Thompson S. The nucleotide sequence of the first externally suppressible--1 frameshift mutant, and of some nearby leaky frameshift mutants. EMBO J. 1983;2(8):1345–1350. doi: 10.1002/j.1460-2075.1983.tb01590.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atkins J. F., Ryce S. UGA and non-triplet suppressor reading of the genetic code. Nature. 1974 Jun 7;249(457):527–530. doi: 10.1038/249527a0. [DOI] [PubMed] [Google Scholar]
  4. Bossi L., Kohno T., Roth J. R. Genetic characterization of the sufj frameshift suppressor in Salmonella typhimurium. Genetics. 1983 Jan;103(1):31–42. doi: 10.1093/genetics/103.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bossi L., Roth J. R. Four-base codons ACCA, ACCU and ACCC are recognized by frameshift suppressor sufJ. Cell. 1981 Aug;25(2):489–496. doi: 10.1016/0092-8674(81)90067-2. [DOI] [PubMed] [Google Scholar]
  6. Bossi L., Smith D. M. Suppressor sufJ: a novel type of tRNA mutant that induces translational frameshifting. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6105–6109. doi: 10.1073/pnas.81.19.6105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cummins C. M., Culbertson M. R., Knapp G. Frameshift suppressor mutations outside the anticodon in yeast proline tRNAs containing an intervening sequence. Mol Cell Biol. 1985 Jul;5(7):1760–1771. doi: 10.1128/mcb.5.7.1760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cummins C. M., Donahue T. F., Culbertson M. R. Nucleotide sequence of the SUF2 frameshift suppressor gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3565–3569. doi: 10.1073/pnas.79.11.3565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Curran J. F., Yarus M. Reading frame selection and transfer RNA anticodon loop stacking. Science. 1987 Dec 11;238(4833):1545–1550. doi: 10.1126/science.3685992. [DOI] [PubMed] [Google Scholar]
  10. Falahee M. B., Weiss R. B., O'Connor M., Doonan S., Gesteland R. F., Atkins J. F. Mutants of translational components that alter reading frame by two steps forward or one step back. J Biol Chem. 1988 Dec 5;263(34):18099–18103. [PubMed] [Google Scholar]
  11. Gaber R. F., Culbertson M. R. The yeast frameshift suppressor gene SUF16-1 encodes an altered glycine tRNA containing the four-base anticodon 3'-CCCG-5'. Gene. 1982 Sep;19(2):163–172. doi: 10.1016/0378-1119(82)90002-6. [DOI] [PubMed] [Google Scholar]
  12. Hartman P. E., Hartman Z., Stahl R. C. Classification and mapping of spontaneous and induced mutations in the histidine operon of Salmonella. Adv Genet. 1971;16:1–34. doi: 10.1016/s0065-2660(08)60352-1. [DOI] [PubMed] [Google Scholar]
  13. Herrington M. B., Kohli A., Faraci M. Frameshift suppression by thyA mutants of Escherichia coli K-12. Genetics. 1986 Nov;114(3):705–716. doi: 10.1093/genetics/114.3.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hughes D., Atkins J. F., Thompson S. Mutants of elongation factor Tu promote ribosomal frameshifting and nonsense readthrough. EMBO J. 1987 Dec 20;6(13):4235–4239. doi: 10.1002/j.1460-2075.1987.tb02772.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Isono K., Yourno J. Chemical carcinogens as frameshift mutagens: Salmonella DNA sequence sensitive to mutagenesis by polycyclic carcinogens. Proc Natl Acad Sci U S A. 1974 May;71(5):1612–1617. doi: 10.1073/pnas.71.5.1612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Isono S., Yourno J. Non-suppressible addition frameshift in Salmonella. J Mol Biol. 1974 Jan 25;82(3):355–360. doi: 10.1016/0022-2836(74)90596-8. [DOI] [PubMed] [Google Scholar]
  17. Kohno T., Bossi L., Roth J. R. New suppressors of frameshift mutations in Salmonella typhimurium. Genetics. 1983 Jan;103(1):23–29. doi: 10.1093/genetics/103.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kohno T., Roth J. R. A Salmonella frameshift suppressor that acts at runs of A residues in the messenger RNA. J Mol Biol. 1978 Nov 25;126(1):37–52. doi: 10.1016/0022-2836(78)90278-4. [DOI] [PubMed] [Google Scholar]
  19. Kraft R., Tardiff J., Krauter K. S., Leinwand L. A. Using mini-prep plasmid DNA for sequencing double stranded templates with Sequenase. Biotechniques. 1988 Jun;6(6):544-6, 549. [PubMed] [Google Scholar]
  20. Kuchino Y., Yabusaki Y., Mori F., Nishimura S. Nucleotide sequences of three proline tRNAs from Salmonella typhimurium. Nucleic Acids Res. 1984 Feb 10;12(3):1559–1562. doi: 10.1093/nar/12.3.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lehner A. F., Hill C. W. Merodiploidy in Escherichia coli-Salmonella typhimurium crosses: the role of unequal recombination between ribosomal RNA genes. Genetics. 1985 Jul;110(3):365–380. doi: 10.1093/genetics/110.3.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Li M., Tzagoloff A. Assembly of the mitochondrial membrane system: sequences of yeast mitochondrial valine and an unusual threonine tRNA gene. Cell. 1979 Sep;18(1):47–53. doi: 10.1016/0092-8674(79)90352-0. [DOI] [PubMed] [Google Scholar]
  23. Low K. B. Escherichia coli K-12 F-prime factors, old and new. Bacteriol Rev. 1972 Dec;36(4):587–607. doi: 10.1128/br.36.4.587-607.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Murgola E. J., Pagel F. T. Codon recognition by glycine transfer RNAs of Escherichia coli in vivo. J Mol Biol. 1980 Apr 25;138(4):833–844. doi: 10.1016/0022-2836(80)90067-4. [DOI] [PubMed] [Google Scholar]
  25. Ota N., Galsworthy P. R., Pardee A. B. Genetics of sulfate transport by Salmonella typhimurium. J Bacteriol. 1971 Mar;105(3):1053–1062. doi: 10.1128/jb.105.3.1053-1062.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pope W. T., Reeves R. H. Purification and characterization of a tRNA methylase from Salmonella typhimurium. J Bacteriol. 1978 Oct;136(1):191–200. doi: 10.1128/jb.136.1.191-200.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reeves R. H., Roth J. R. Transfer ribonucleic acid methylase deficiency found in UGA supressor strains. J Bacteriol. 1975 Oct;124(1):332–340. doi: 10.1128/jb.124.1.332-340.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Riddle D. L., Carbon J. Frameshift suppression: a nucleotide addition in the anticodon of a glycine transfer RNA. Nat New Biol. 1973 Apr 25;242(121):230–234. doi: 10.1038/newbio242230a0. [DOI] [PubMed] [Google Scholar]
  29. Riddle D. L., Roth J. R. Frameshift suppressors. 3. Effects of suppressor mutations on transfer RNA. J Mol Biol. 1972 May 28;66(3):495–506. doi: 10.1016/0022-2836(72)90429-9. [DOI] [PubMed] [Google Scholar]
  30. Riddle D. L., Roth J. R. Frameshift suppressors. II. Genetic mapping and dominance studies. J Mol Biol. 1972 May 28;66(3):483–493. doi: 10.1016/0022-2836(72)90428-7. [DOI] [PubMed] [Google Scholar]
  31. Riyasaty S., Atkins J. F. External suppression of a frameshift mutant in salmonella. J Mol Biol. 1968 Jun 28;34(3):541–557. doi: 10.1016/0022-2836(68)90179-4. [DOI] [PubMed] [Google Scholar]
  32. Roth J. R. Frameshift suppression. Cell. 1981 Jun;24(3):601–602. doi: 10.1016/0092-8674(81)90086-6. [DOI] [PubMed] [Google Scholar]
  33. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983 Sep;47(3):410–453. doi: 10.1128/mr.47.3.410-453.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Straus D. S. Selection for a large genetic duplication in Salmonella typhimurium. Genetics. 1975 Jun;80(2):227–237. doi: 10.1093/genetics/80.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Turnbough C. L., Jr, Neill R. J., Landsberg R., Ames B. N. Pseudouridylation of tRNAs and its role in regulation in Salmonella typhimurium. J Biol Chem. 1979 Jun 25;254(12):5111–5119. [PubMed] [Google Scholar]
  36. Uemura H., Thorbjarnardóttir S., Gamulin V., Yano J., Andrésson O. S., Söll D., Eggertsson G. supN ochre suppressor gene in Escherichia coli codes for tRNALys. J Bacteriol. 1985 Sep;163(3):1288–1289. doi: 10.1128/jb.163.3.1288-1289.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Van Delft J. H., Schmidt D. S., Bosch L. The tRNA-tufB operon transcription termination and processing upstream from tufB. J Mol Biol. 1987 Oct 20;197(4):647–657. doi: 10.1016/0022-2836(87)90471-2. [DOI] [PubMed] [Google Scholar]
  38. Weiss-Brummer B., Sakai H., Kaudewitz F. A mitochondrial frameshift-suppressor (+1) [corrected] of the yeast S. cerevisiae maps in the mitochondrial 15S rRNA locus. Curr Genet. 1987;11(4):295–301. doi: 10.1007/BF00355403. [DOI] [PubMed] [Google Scholar]
  39. Weiss R. B., Dunn D. M., Atkins J. F., Gesteland R. F. Slippery runs, shifty stops, backward steps, and forward hops: -2, -1, +1, +2, +5, and +6 ribosomal frameshifting. Cold Spring Harb Symp Quant Biol. 1987;52:687–693. doi: 10.1101/sqb.1987.052.01.078. [DOI] [PubMed] [Google Scholar]
  40. Wilson P. G., Culbertson M. R. SUF12 suppressor protein of yeast. A fusion protein related to the EF-1 family of elongation factors. J Mol Biol. 1988 Feb 20;199(4):559–573. doi: 10.1016/0022-2836(88)90301-4. [DOI] [PubMed] [Google Scholar]
  41. Winey M., Mendenhall M. D., Cummins C. M., Culbertson M. R., Knapp G. Splicing of a yeast proline tRNA containing a novel suppressor mutation in the anticodon stem. J Mol Biol. 1986 Nov 5;192(1):49–63. doi: 10.1016/0022-2836(86)90463-8. [DOI] [PubMed] [Google Scholar]
  42. Yoshimura M., Kimura M., Ohno M., Inokuchi H., Ozeki H. Identification of transfer RNA suppressors in Escherichia coli. III. Ochre suppressors of lysine tRNA. J Mol Biol. 1984 Aug 25;177(4):609–625. doi: 10.1016/0022-2836(84)90040-8. [DOI] [PubMed] [Google Scholar]
  43. Yourno J., Kohno T. Externally suppressible proline quadruplet ccc U. Science. 1972 Feb 11;175(4022):650–652. doi: 10.1126/science.175.4022.650. [DOI] [PubMed] [Google Scholar]
  44. Yourno J., Tanemura S. Restoration of in-phase translation by an unlinked suppressor of a frameshift mutation in Salmonella typhimurium. Nature. 1970 Jan 31;225(5231):422–426. doi: 10.1038/225422a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES