Skip to main content
Log in

Evidence for endonucleolytic cleavage at the 5′-proximal segment of the trp messenger RNA in Escherichia coli

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

The 5′-proximal trp leader RNA segment (about 5S) decays at 2 to 3 times slower rates than the distal trp mRNA sequence. This has been demonstrated by employing the deletion mutants which lack a large portion of the structural genes but retain the promoter-proximal region of the trp operon. Relative stability of the leader RNA is not merely due to the presence of an untranslatable region in the segment; the internal untranslatable segment of trp mRNA downstream from the nonsense alteration site of a double mutant trpAD28·trpE9758 decays as fast as the normal trp mRNA sequence. These results suggest that the trp mRNA is endonucleolytically cleaved to yield the small 5′-proximal leader RNA segment before the distal mRNA decays and that the leader RNA sequence is not subject to usual mode of mRNA decay in the 5′ to 3′ direction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Achord, D., Kennell, D.: Metabolism of messenger RNA from the gal operon of Escherichia coli. J. Mol. Biol. 90, 581–599 (1974)

    Google Scholar 

  • Bertrand, K., Korn, L., Lee, F., Platt, T., Squires, C.L., Yanofsky, C.: New features of the regulation of the tryptophan operon. Science 189, 22–26 (1975)

    Google Scholar 

  • Blundell, M., Kennell, D.: Evidence for endonucleolytic attack in decay of lac messenger RNA in Escherichia coli. J. Mol. Biol. 83, 143–163 (1974)

    Google Scholar 

  • Bronson, M.J., Squires, C., Yanofsky, C.: Nucleotide sequences from tryptophan messenger RNA of Escherichia coli: The sequence corresponding to the amino-terminal region of the first polypeptide specified by the operon. Proc. Natl. Acad. Sci. U.S.A. 70, 2335–2339 (1973)

    Google Scholar 

  • Craig, E., Cremer, K., Schlessinger, D.: Metabolism of T4 messenger RNA; Host messenger RNA and ribosomal RNA in T4-infected Escherichia coli B. J. Mol. Biol. 71, 701–715 (1972)

    Google Scholar 

  • Dunn, L.J., Studier, F.W.: T7 early RNAs and Escherichia coli ribosomal RNAs are cut from large precursor RNAs in vivo by ribonuclease III. Proc. Natl. Acad. Sci. U.S.A. 70, 3296–3300 (1973)

    Google Scholar 

  • Hercules, K., Schweiger, M., Sauerbier, W.: Cleavage by RNase III converts T3 and T7 early precursor RNA into translatable message. Proc. Natl. Acad. Sci. U.S.A. 71, 840–844 (1974)

    Google Scholar 

  • Imamoto, F.: Intragenic initiations of transcription of the tryptophan operon in Escherichia coli following dinitrophenol treatment without tryptophan. J. Mol. Biol. 43, 51–69 (1969)

    Google Scholar 

  • Imamoto, F.: Diversity of regulation of genetic transcription. I. Effect of antibiotics which inhibit the process of translation on RNA metabolism in Escherichia coli. J. Mol. Biol. 74, 113–136 (1973)

    Google Scholar 

  • Imamoto, F., Kano, Y., Tani, S.: Transcription of the tryptophan operon in nonsense mutants of Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 35, 471–490 (1970)

    Google Scholar 

  • Imamoto, F., Schlessinger, D.: Bearing of some recent results on the mechanisms of polarity and messenger RNA stability. Mol. Gen. Genet. 135, 29–38 (1974)

    Google Scholar 

  • Imamoto, F., Yanofsky, C.: Transcription of the tryptophan operon in polarity mutants of Escherichia coli. I. Characterization of the tryptophan messenger RNA of polar mutants. J. Mol. Biol. 28, 1–23 (1967)

    Google Scholar 

  • Kano, Y., Imamoto, F.: Polarity in segments of the Escherichia coli trp operon with deleted intraoperonic translational initiation signals. Genetics 80, 651–666 (1975)

    Google Scholar 

  • Kano, Y., Kuwano, M., Imamoto, F.: Initial trp operon sequence in Escherichia coli is transcribed without coupling to translation. Mol. Gen. Genet. 146, 179–188 (1976)

    Google Scholar 

  • Lennox, E.S.: Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1, 190–206 (1955)

    Google Scholar 

  • Lozeron, H.A., Adevski, P.J., Apirion, D.: Antitermination and absence of processing of the leftward transcript of coliphage lambda in the RNAase III deficient host. J. Mol. Biol. 109, 359–365 (1977)

    Google Scholar 

  • Lozeron, H.A., Dahlberg, J.E., Szybalski, W.: Processing of the major leftward mRNA of coliphage lambda. Virology 71, 262–277 (1976)

    Google Scholar 

  • Mangiarotti, G., Schlessinger, D., Kuwano, M.: Initiation of ribosome-dependent breakdown of T4-specific messenger RNA. J. Mol. Biol. 60, 411–452 (1971)

    Google Scholar 

  • Miozzari, G.F., Yanofsky, C.: Translation of the leader region of the Escherichia coli tryptophan operon. J. Bacteriol. 133, 1457–1466 (1978)

    Google Scholar 

  • Morikawa, N., Imamoto, F.: On the degradation of messenger RNA for the tryptophan operon in Escherichia coli. Nature 223, 37–40 (1969)

    Google Scholar 

  • Morse, D.E., Mosteller, R., Baker, R.F., Yanofsky, C.: Direction of in vivo degradation of tryptophan mRNA — a correction. Nature 223, 40–43 (1969)

    Google Scholar 

  • Nikolaev, N., Silengo, L., Schlessinger, D.: A role for ribonuclease III in processing of ribosomal ribonucleic acid and messenger ribonucleic acid precursors in Escherichia coli. J. Biol. Chem. 248, 7967–7969 (1973)

    Google Scholar 

  • Platt, T., Squires, C., Yanofsky, C.: Ribosome-protected regions in the leader-trpE sequence of Escherichia coli tryptophan operon messenger RNA. J. Mol. Biol. 103, 411–420 (1976)

    Google Scholar 

  • Schlessinger, D., Jacobs, K.A., Gupta, R.S., Kano, Y., Imamoto, F.: Decay of individual Escherichia coli trp messenger RNA molecules is sequentially ordered. J. Mol. Biol. 110, 421–439 (1977)

    Google Scholar 

  • Schmeissner, U., Ganem, D., Miller, J.H.: Genetic studies of the lac repressor II. Fine structure deletion map of the lacI gene, and its correlation with the physical map. J. Mol. Biol. 109, 303–326 (1977)

    Google Scholar 

  • Squires, C., Lee, F., Bertrand, K., Squires, C.L., Bronson, M.J., Yanofsky, C.: Nucleotide Sequence of the 5′ end of tryptophan messenger RNA of Escherichia coli. J. Mol. Biol. 103, 351–381 (1976)

    Google Scholar 

  • Tani, S., Imamoto, F.: Functions of the trp and N message synthesized originating at the P L promoter in lambda trp phage. J. Mol. Biol. 92, 305–309 (1975)

    Google Scholar 

  • Vogel, H.J., Bonner, D.M.: Acetylornitinase of Escherichia coli: Partial purification and some properties. J. Biol. Chem. 218, 97–106 (1956)

    Google Scholar 

  • Webster, R.E., Zinder, N.D.: Fate of the message-ribosome complex upon translation of termination signals. J. Mol. Biol. 42, 425–440 (1969)

    Google Scholar 

  • Yamada, Y., Nakada, D.: Translation of T7 RNA in vitro without cleavage by R Nase III. Virology 18, 1155–1159 (1976)

    Google Scholar 

  • Yamada, Y., Whitaker, P.A., Nakada, D.: Functional instability of T7 early mRNA. Nature 248, 335–338 (1974)

    Google Scholar 

  • Yamamoto, T., Imamoto, F.: Differential stability of trp mRNA synthesized originating at trp promoter and P L promoter of λtrp. J. Mol. Biol. 92, 289–309 (1975)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by T. Yura

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kano, Y., Imamoto, F. Evidence for endonucleolytic cleavage at the 5′-proximal segment of the trp messenger RNA in Escherichia coli . Molec. Gen. Genet. 172, 25–30 (1979). https://doi.org/10.1007/BF00276211

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00276211

Keywords

Navigation