Molecular Biology Reports

, Volume 39, Issue 1, pp 33–39 | Cite as

Shine-Dalgarno sequence of bacteriophage T4: GAGG prevails in early genes

  • Naglis MalysEmail author


Translation initiation is governed by a limited number of mRNA sequence motifs within the translation initiation region (TIR). In bacteria and bacteriophages, one of the most important determinants is a Shine-Dalgarno (SD) sequence that base pairs with the anti-SD sequence GAUCACCUCCUUA localized in the 3′ end of 16S rRNA. This work assesses a diversity of TIR features in phage T4, focusing on the SD sequence, its spacing to the start codon and relationship to gene expression and essentiality patterns. Analysis shows that GAGG is predominant of all core SD motifs in T4 and its related phages, particularly in early genes. Possible implication of the RegB activity is discussed.


Translation initiation Shine-Dalgarno sequence Phage T4 T4-related phages Early genes RegB 



The author is grateful to anonymous reviewers for constructive and critical comments. N.M. acknowledges the support of the BBSRC/EPSRC Grant BB/C008219/1 “The Manchester Centre for Integrative Systems Biology (MCISB)”.

Supplementary material

11033_2011_707_MOESM1_ESM.doc (32 kb)
Supplementary material 1 (DOC 32 kb)
11033_2011_707_MOESM2_ESM.ppt (413 kb)
Supplementary material 2 (PPT 413 kb)


  1. 1.
    Gold L (1988) Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 57:199–233PubMedCrossRefGoogle Scholar
  2. 2.
    Kozak M (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234:187–208PubMedCrossRefGoogle Scholar
  3. 3.
    Nakamoto T (2011) Mechanisms of the initiation of protein synthesis: in reading frame binding of ribosomes to mRNA. Mol Biol Rep. doi: 10.1007/s11033-010-0176-1
  4. 4.
    Shine J, Dalgarno L (1974) The 3’-terminal sequence of Escherichia coli 16S ribosomal RNA complementarity to nonsense triplets and ribosome binding sites. Proc. Natl Acad Sci USA 71:1342–1346CrossRefGoogle Scholar
  5. 5.
    Calogero R, Pon C, Canonaco M, Gualerzi C (1988) Selection of the mRNA translation initiation region by Escherichia coli ribosomes. Proc Natl Acad Sci USA 85:6427–6431PubMedCrossRefGoogle Scholar
  6. 6.
    Hartz D, McPheeters DS, Green L, Gold L (1991) Detection of Escherichia coli ribosome binding at translation initiation sites in the absence of tRNA. J Mol Biol 218:99–105PubMedCrossRefGoogle Scholar
  7. 7.
    Hartz D, McPheeters DS, Gold L (1991) Influence of mRNA determinants on translation initiation in Escherichia coli. J Mol Biol 218:83–97PubMedCrossRefGoogle Scholar
  8. 8.
    Simonetti A, Marzi A, Jenner L, Myasnikov A, Romby P, Yusupova G, Klaholz BP, Yusupov M (2009) A structural view of translation initiation in Bacteria. Cell Mol Life Sci 66:423–436PubMedCrossRefGoogle Scholar
  9. 9.
    Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, Stormo GD, Gold L (1992) Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol Microbiol 6:1129–1219CrossRefGoogle Scholar
  10. 10.
    Vellanoweth RL, Rabinowitz JC (1992) The influence of ribosome binding site on translational efficiency in Bacillus subtilis and Escherichia coli in vivo. Mol Microbiol 6:1105–1114PubMedCrossRefGoogle Scholar
  11. 11.
    de Smit MH, van Duin J (1994) Control of translation by mRNA secondary structure in Escherichia coli. A quantitative analysis of literature data. J Mol Biol 244:144–150PubMedCrossRefGoogle Scholar
  12. 12.
    Draper DE, Gluick TC, Schlax PJ (1998) Pseudoknots, RNA folding and translational regulation. In: Simons RW, Grunberg-Manago M (eds) RNA structure and function. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 415–436Google Scholar
  13. 13.
    Ma J, Campbell A, Karlin S (2002) Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J Bacteriol 184:5733–5745PubMedCrossRefGoogle Scholar
  14. 14.
    Kozak M (1983) Comparison of initiation of protein synthesis in prokaryotes, eukaryotes, and organelles. Microbiol Rev 47:1–45PubMedGoogle Scholar
  15. 15.
    de Smit MH, van Duin J (1994) Translational initiation on structured messengers. Another role for the Shine-Dalgarno interaction. J Mol Biol 235:173–184PubMedCrossRefGoogle Scholar
  16. 16.
    Wagner LA, Gesteland RF, Dayhuff TJ, Weiss RB (1994) An efficient Shine-Dalgarno sequence but not translation is necessary for lacZ mRNA stability in Escherichia coli. J Bacteriol 176:1683–1688PubMedGoogle Scholar
  17. 17.
    Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Ruger W (2003) Bacteriophage T4 genome. Microbiol Mol Biol Rev 67:86–156PubMedCrossRefGoogle Scholar
  18. 18.
    Chen H, Bjerknes M, Kumar R, Jay E (1994) Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs. Nucleic Acids Res 22:4953–4957PubMedCrossRefGoogle Scholar
  19. 19.
    Shultzaberger RK, Bucheimer RE, Rudd KE, Schneider TD (2001) Anatomy of Escherichia coli ribosome binding sites. J Mol Biol 313:215–228PubMedCrossRefGoogle Scholar
  20. 20.
    Miller ES, Karam JD, Spicer E (1994) Control of translation initiation: mRNA structure and protein repressors. In: Karam JD et al (eds) Molecular biology of bacteriophage T4. American Society for Microbiology, Washington, DC, pp 193–205Google Scholar
  21. 21.
    Nivinskas R, Malys N, Klausa V, Vaiškūnaitė R, Gineikienė E (1999) Post-transcriptional control of bacteriophage T4 gene 25 expression mRNA secondary structure that enhances translational initiation. J Mol Biol 288:291–304PubMedCrossRefGoogle Scholar
  22. 22.
    Malys N, Nivinskas R (2009) Non-canonical RNA arrangement in T4-even phages: accommodated ribosome binding site at the gene 26–25 intercistronic junction. Mol Microbiol 73:1115–1127PubMedCrossRefGoogle Scholar
  23. 23.
    Sanson B, Hu R-M, Troitskaya E, Mathy N, Uzan M (2000) Endoribonuclease RegB from bacteriophage T4 is necessary for the degradation of early but not middle or late mRNAs. J Mol Biol 297:1063–1074PubMedCrossRefGoogle Scholar
  24. 24.
    Durand S, Richard G, Bisaglia M, Laalami S, Bontems F, Uzan M (2006) Activation of RegB endoribonuclease by S1 ribosomal protein requires an 11 nt conserved sequence. Nucleic Acids Res 34:6549–6560PubMedCrossRefGoogle Scholar
  25. 25.
    Zajančkauskaite A, Truncaite L, Strazdaite-Žieliene Ž, Nivinskas R (2008) Involvement of the Escherichia coli endoribonucleases G and E in the secondary processing of RegB-cleaved transcripts of bacteriophage T4. Virology 375:342–353PubMedCrossRefGoogle Scholar
  26. 26.
    Piešiniene L, Truncaite L, Zajančkauskaite A, Nivinskas R (2004) The sequences and activities of RegB endoribonucleases of T4-related bacteriophages. Nucleic Acids Res 32:5582–5595PubMedCrossRefGoogle Scholar
  27. 27.
    Malys N, McCarthy JEG (2011) Translation initiation: variations in the mechanism can be anticipated. Cell Mol Life Sci 68:991–1003PubMedCrossRefGoogle Scholar
  28. 28.
    Markham NR, Zuker M (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res 33:W577–W581PubMedCrossRefGoogle Scholar
  29. 29.
    Schurr T, Nadir E, Margalit H (1993) Identification and characterization of E. coli ribosomal binding sites by free energy computation. Nucleic Acid Res 21:4019–4023PubMedCrossRefGoogle Scholar
  30. 30.
    Zajančkauskaite A, Malys N, Nivinskas R (1997) A rare type of overlapping genes in bacteriophage T4: gene 30.3’ is completely embedded within gene 30.3 by one position downstream. Gene 194:157–162PubMedCrossRefGoogle Scholar
  31. 31.
    Liu H, He R, Zhang H, Huang Y, Tian M, Zhang J (2010) Analysis of synonymous codon usage in Zea mays. Mol Biol Rep 37:677–684PubMedCrossRefGoogle Scholar
  32. 32.
    Zhou M, Li X (2009) Analysis of synonymous codon usage patterns in different plant mitochondrial genomes. Mol Biol Rep 36:2039–2046PubMedCrossRefGoogle Scholar
  33. 33.
    Komarova AV, Tchufistova LS, Dreyfus M, Boni IV (2005) AU-rich sequences within 5′ untranslated leaders enhance translation and stabilize mRNA in Escherichia coli. J Bacteriol 187:1344–1349PubMedCrossRefGoogle Scholar
  34. 34.
    Boni IV, Artamonova VS, Tzareva NV, Dreyfus M (2001) Non-canonical mechanism for translational control in bacteria: synthesis of ribosomal protein S1. EMBO J 20:4222–4232PubMedCrossRefGoogle Scholar
  35. 35.
    Hering O, Brenneis M, Beer J, Suess B, Soppa J (2009) A novel mechanism for translation initiation operates in Haloarchaea. Mol Microbiol 71:1451–1463PubMedCrossRefGoogle Scholar
  36. 36.
    Gray NK, Hentze MW (1994) Regulation of protein synthesis by mRNA structure. Mol Biol Rep 19:195–200PubMedCrossRefGoogle Scholar
  37. 37.
    Vimberg V, Tats A, Remm M, Tenson T (2007) Translation initiation region sequence preferences in Escherichia coli. BMC Mol Biol 8:100PubMedCrossRefGoogle Scholar
  38. 38.
    Uzan M, Miller ES (2010) Post-transcriptional control by bacteriophage T4: mRNA decay and inhibition of translation initiation. Virol J 7:360PubMedCrossRefGoogle Scholar
  39. 39.
    Uzan M (2001) Bacteriophage T4 RegB endoribonuclease. Methods Enzymol 342:467–480PubMedCrossRefGoogle Scholar
  40. 40.
    Uzan M (2009) RNA processing and decay in bacteriophage T4. Prog Mol Biol Trans Sci 85:43–89CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Faculty of Life Sciences, MCISB, MIBUniversity of ManchesterManchesterUK

Personalised recommendations