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.
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)
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)
Blundell, M., Kennell, D.: Evidence for endonucleolytic attack in decay of lac messenger RNA in Escherichia coli. J. Mol. Biol. 83, 143–163 (1974)
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)
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)
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)
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)
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)
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)
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)
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)
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)
Kano, Y., Imamoto, F.: Polarity in segments of the Escherichia coli trp operon with deleted intraoperonic translational initiation signals. Genetics 80, 651–666 (1975)
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)
Lennox, E.S.: Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1, 190–206 (1955)
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)
Lozeron, H.A., Dahlberg, J.E., Szybalski, W.: Processing of the major leftward mRNA of coliphage lambda. Virology 71, 262–277 (1976)
Mangiarotti, G., Schlessinger, D., Kuwano, M.: Initiation of ribosome-dependent breakdown of T4-specific messenger RNA. J. Mol. Biol. 60, 411–452 (1971)
Miozzari, G.F., Yanofsky, C.: Translation of the leader region of the Escherichia coli tryptophan operon. J. Bacteriol. 133, 1457–1466 (1978)
Morikawa, N., Imamoto, F.: On the degradation of messenger RNA for the tryptophan operon in Escherichia coli. Nature 223, 37–40 (1969)
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)
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)
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)
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)
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)
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)
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)
Vogel, H.J., Bonner, D.M.: Acetylornitinase of Escherichia coli: Partial purification and some properties. J. Biol. Chem. 218, 97–106 (1956)
Webster, R.E., Zinder, N.D.: Fate of the message-ribosome complex upon translation of termination signals. J. Mol. Biol. 42, 425–440 (1969)
Yamada, Y., Nakada, D.: Translation of T7 RNA in vitro without cleavage by R Nase III. Virology 18, 1155–1159 (1976)
Yamada, Y., Whitaker, P.A., Nakada, D.: Functional instability of T7 early mRNA. Nature 248, 335–338 (1974)
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)
Author information
Authors and Affiliations
Additional information
Communicated by T. Yura
Rights 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
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00276211