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. 1987 Jan;6(1):43–48. doi: 10.1002/j.1460-2075.1987.tb04716.x

Selection of AUG initiation codons differs in plants and animals.

H A Lütcke, K C Chow, F S Mickel, K A Moss, H F Kern, G A Scheele
PMCID: PMC553354  PMID: 3556162

Abstract

The influence of the nucleotide at position -3 relative to the AUG initiation codon on the initiation of protein synthesis was studied in two different in vitro translation systems using synthetic mRNAs. The four mRNAs, transcribed from cDNAs directed by an SP6 promoter, were identical except for mutations at nucleotide -3. In each case, translation of mRNAs produced a single protein of Mr = 12,600. Relative translational efficiencies showed a hierarchy in the reticulocyte lysate system (100, 85, 61 and 38% for A, G, U and C in position -3, respectively) but no differences in the wheat germ system. Differential mRNA degradation or polypeptide chain elongation were excluded as causes of the differences observed in translation in the reticulocyte lysate. mRNA competition increased the differences observed in translational efficiencies in reticulocyte lysate but showed no effect in wheat germ. Analysis of 61 plant and 209 animal mRNA sequences revealed qualitative and quantitative differences between the consensus sequences surrounding AUG initiation codons. Whereas the consensus sequence for animals was CACCAUG that for plants was AACAAUGGC. Both the structural and functional findings suggest that the factors which select AUG initiation codons in plants and animals differ significantly.

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Selected References

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

  1. Bellini W. J., Englund G., Rozenblatt S., Arnheiter H., Richardson C. D. Measles virus P gene codes for two proteins. J Virol. 1985 Mar;53(3):908–919. doi: 10.1128/jvi.53.3.908-919.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bloom K. S., Amaya E., Carbon J., Clarke L., Hill A., Yeh E. Chromatin conformation of yeast centromeres. J Cell Biol. 1984 Nov;99(5):1559–1568. doi: 10.1083/jcb.99.5.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  4. Cashmore A. R. Structure and expression of a pea nuclear gene encoding a chlorophyll a/b-binding polypeptide. Proc Natl Acad Sci U S A. 1984 May;81(10):2960–2964. doi: 10.1073/pnas.81.10.2960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dunsmuir P. The petunia chlorophyll a/b binding protein genes: a comparison of Cab genes from different gene families. Nucleic Acids Res. 1985 Apr 11;13(7):2503–2518. doi: 10.1093/nar/13.7.2503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ernst H., Shatkin A. J. Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc Natl Acad Sci U S A. 1985 Jan;82(1):48–52. doi: 10.1073/pnas.82.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ernst V., Levin D. H., Ranu R. S., London I. M. Control of protein synthesis in reticulocyte lysates: effects of 3':5'-cyclic AMP, ATP, and GTP on inhibitions induced by hemedeficiency, double-stranded RNA, and a reticulocyte translationa inhibitor. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1112–1116. doi: 10.1073/pnas.73.4.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Giorgi C., Blumberg B. M., Kolakofsky D. Sendai virus contains overlapping genes expressed from a single mRNA. Cell. 1983 Dec;35(3 Pt 2):829–836. doi: 10.1016/0092-8674(83)90115-0. [DOI] [PubMed] [Google Scholar]
  9. Goldberg M. L., Lifton R. P., Stark G. R., Williams J. G. Isolation of specific RNA's using DNA covalently linked to diazobenzyloxymethyl cellulose or paper. Methods Enzymol. 1979;68:206–220. doi: 10.1016/0076-6879(79)68016-3. [DOI] [PubMed] [Google Scholar]
  10. Guo L. H., Wu R. New rapid methods for DNA sequencing based in exonuclease III digestion followed by repair synthesis. Nucleic Acids Res. 1982 Mar 25;10(6):2065–2084. doi: 10.1093/nar/10.6.2065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  12. Kerfelec B., LaForge K. S., Puigserver A., Scheele G. Primary structures of canine pancreatic lipase and phospholipase A2 messenger RNAs. Pancreas. 1986;1(5):430–437. doi: 10.1097/00006676-198609000-00007. [DOI] [PubMed] [Google Scholar]
  13. Kohorn B. D., Harel E., Chitnis P. R., Thornber J. P., Tobin E. M. Functional and mutational analysis of the light-harvesting chlorophyll a/b protein of thylakoid membranes. J Cell Biol. 1986 Mar;102(3):972–981. doi: 10.1083/jcb.102.3.972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kozak M. Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature. 1984 Mar 15;308(5956):241–246. doi: 10.1038/308241a0. [DOI] [PubMed] [Google Scholar]
  16. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
  17. Kozak M. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res. 1981 Oct 24;9(20):5233–5252. doi: 10.1093/nar/9.20.5233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lamppa G. K., Morelli G., Chua N. H. Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol Cell Biol. 1985 Jun;5(6):1370–1378. doi: 10.1128/mcb.5.6.1370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marcus A., Efron D., Weeks D. P. The wheat embryo cell-free system. Methods Enzymol. 1974;30:749–754. doi: 10.1016/0076-6879(74)30073-0. [DOI] [PubMed] [Google Scholar]
  21. Pelham H. R., Jackson R. J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem. 1976 Aug 1;67(1):247–256. doi: 10.1111/j.1432-1033.1976.tb10656.x. [DOI] [PubMed] [Google Scholar]
  22. Pichersky E., Bernatzky R., Tanksley S. D., Breidenbach R. B., Kausch A. P., Cashmore A. R. Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (tomato). Gene. 1985;40(2-3):247–258. doi: 10.1016/0378-1119(85)90047-2. [DOI] [PubMed] [Google Scholar]
  23. Pichersky E., Bernatzky R., Tanksley S. D., Cashmore A. R. Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3880–3884. doi: 10.1073/pnas.83.11.3880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pinck M., Guilley E., Durr A., Hoff M., Pinck L., Fleck J. Complete sequence of one of the mRNAs coding for the small subunit of ribulose bisphosphate carboxylase of Nicotiana sylvestris. Biochimie. 1984 Jul-Aug;66(7-8):539–545. doi: 10.1016/0300-9084(84)90148-2. [DOI] [PubMed] [Google Scholar]
  25. Pinsky S. D., LaForge K. S., Luc V., Scheele G. Identification of cDNA clones encoding secretory isoenzyme forms: sequence determination of canine pancreatic prechymotrypsinogen 2 mRNA. Proc Natl Acad Sci U S A. 1983 Dec;80(24):7486–7490. doi: 10.1073/pnas.80.24.7486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pinsky S. D., LaForge K. S., Scheele G. Differential regulation of trypsinogen mRNA translation: full-length mRNA sequences encoding two oppositely charged trypsinogen isoenzymes in the dog pancreas. Mol Cell Biol. 1985 Oct;5(10):2669–2676. doi: 10.1128/mcb.5.10.2669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Scheele G., Jacoby R., Carne T. Mechanism of compartmentation of secretory proteins: transport of exocrine pancreatic proteins across the microsomal membrane. J Cell Biol. 1980 Dec;87(3 Pt 1):611–628. doi: 10.1083/jcb.87.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shaw M. W., Choppin P. W., Lamb R. A. A previously unrecognized influenza B virus glycoprotein from a bicistronic mRNA that also encodes the viral neuraminidase. Proc Natl Acad Sci U S A. 1983 Aug;80(16):4879–4883. doi: 10.1073/pnas.80.16.4879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tumer N. E., Clark W. G., Tabor G. J., Hironaka C. M., Fraley R. T., Shah D. M. The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves. Nucleic Acids Res. 1986 Apr 25;14(8):3325–3342. doi: 10.1093/nar/14.8.3325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wicker C., Puigserver A., Rausch U., Scheele G., Kern H. Multiple-level caerulein control of the gene expression of secretory proteins in the rat pancreas. Eur J Biochem. 1985 Sep 16;151(3):461–466. doi: 10.1111/j.1432-1033.1985.tb09124.x. [DOI] [PubMed] [Google Scholar]

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