Summary
We searched the complete 39,936 base DNA sequence of bacteriophage T7 for nonrandomness that might be attributed to natural selection. Codon usage in the 50 genes of T7 is nonrandom, both over the whole code and among groups of synonymous codons. There is a great excess of purineany base-pyrimidine (RNY) codons. Codon usage varies between genes, but from the pooled data for the whole genome (12,145 codons) certain putative selective constraints can be identified. Codon usage appears to be influenced by host tRNA abundance (particularly in highly expressed genes), tRNA-mRNA interactions (one such interaction being perhaps responsible for maintaining the excess of RNY codons) and a lack of short palindromes. This last constraint is probably due to selection against host restriction enzyme recognition sites; this is the first report of an effect of this kind on codon usage. Selection against susceptibility to mutational damage does not appear to have been involved.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adams J., Rothman ED (1982) Estimation of phylogenetic relationships from DNA restriction patterns and selection of endonuclease cleavage sites. Proc Natl Acad Sci USA79: 3560–3564
Andersson SGE, Buckingham RH, Kurland CG (1984) Does codon composition influence ribosome function? EMBO J 3: 91–94
Blaisdell BE (1983) A prevalent persistent global nonrandomness that distinguishes coding and non-coding eucaryotic nuclear DNA sequences. J. Mol. Evol 19:122–133
Clarke BC (1970) Darwinian evolution of proteins. Science 168: 1009–1011
Dunn JJ, Studier FW (1983) Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 166:477–535
Eigen M, Gardiner W, Schuster P, Winkler-Oswatitsch R (1981) The origin of genetic information. Sci Am 244(4):78–94
Fitch WM (1980) Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: comparison of several methods and three beta hemoglobin messenger RNA's. J Mol Evol 16:153–209
Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LG, Zablen LB, Blakemore R, Gupta R, Bonen L., Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463
Godson GN, Barrell BG, Staden R, Fiddes JC (1978) Nucleotide sequence of bacteriophage G4 DNA. Nature 276:236–247
Golding GB, Strobeck C (1982) Expected frequencies of codon use as a function of mutation rates and codon fitnesses. J. Mol Evol 18:379–386
Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074
Grantham R, Gautier C, Gouy M, Mercier R, Pave A (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Res 8:r49-r62
Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 9:r43-r79
Grosjean H, Fiers W (1982) Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18:199–209
Hausmann R (1976) Bacteriophage T7 genetics. Curr Top Microbiol Immunol 75:77–110
Ikemura T. (1981a) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21
Ikemura T (1981b) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for theE. coli translational system. J Mol Biol 151:389–409
Ikemura T (1982) Correlation between the abundance of yeast tRNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast andEscherichia coli with reference to the abundance of isoaccepting transfer RNAs. J Mol Biol 158:573–598
Ikemura T, Ozeki H (1982) Codon usage and transfer RNA contents: organism-specific codon-choice patterns in reference to the isoacceptor contents. Cold Spring Harbor Symp Quant Biol 47:1087–1097
Kimura M (1979) The neutral theory of molecular evolution. Sci Am 241:98–126
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798
Kreitman M (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus ofDrosophila melanogaster. Nature 304: 412–417
Kruger DH, Bickle TA (1983) Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol Rev 47:345–360
Kruger DH, Schroeder C (1981) Bacteriophage T3 and bacteriophage T7 virus-host cell interactions. Microbiol Rev 45: 9–51
Li W-H, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239
Lipman DJ, Wilbur WJ (1983) Contextual constraints on synonymous codon choice. J Mol Biol 163:363–376
Mahon GAT, McWilliam P, Gordon RL, McConnell DJ (1980) The time course of transcription. J Theor Biol 87:483–515
Miyata T, Hayashida H (1981) Extraordinarily high evolutionary rate of pseudogenes: evidence for the presence of selective pressure against changes between synonymous codons. Proc Natl Acad Sci USA 78:5739–5743
Miyata T, Hayashida H, Kukuno R, Hasegawa M, Kobayashi M, Koike K (1982) Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J. Mol Evol 19: 28–35
Modiano G, Battistuzzi G, Motulsky AG (1981) Nonrandom patterns of codon usage and of nucleotide substitutions in human α- and β-globin genes: an evolutionary strategy reducing the rate of mutations with drastic effects? Proc Natl Acad Sci USA 78:1110–1114
Moffat BA, Dunn JJ, Studier FW (1984) Nucleotide sequence of the gene for bacteriophage T7 RNA polymerase. J Mol Biol 173:265–269
Nichols BP, Yanofsky C (1979) Nucleotide sequences of trpA ofSalmonella typhimurium andEscherichia coli: an evolutionary comparison. Proc Natl Acad Sci USA 76:5244–5248
Nussinov R (1981) The universal dinucleotide asymmetry rules in DNA and the amino acid codon choice. J. Mol Evol 17: 237–244
Nussinov R (1984) Doublet frequencies in evolutionary distinct groups. Nucleic Acids Res 12:1749–1763
Pieczenik G (1980) Predicting coding function from nucleotide sequence or survival of “fitness” of tRNA. Proc Natl Acad Sci USA 77:3539–3543
Piekarowicz A, Bickle TA, Shepherd JCW, Ineichen K (1981) The DNA sequence recognized by the HinflII restriction endonuclease. J Mol Biol 146:167–172
Richmond RC (1970) Non-Darwinian evolution: a critique. Nature 225:1025–1028
Roberts RJ (1984) Restriction and modification enzymes and their recognition sequences. Nucleic Acids Res 12:r167-r204
Rosenberg AH, Simon MN, Studier FW (1979) Survey and mapping of restriction cleavage sites in bacteriophage T7 DNA. J Mol Biol 135:907–915
Sanger F, Coulson AR, Freidmann T, Air GM, Barrell BG, Brown NL, Fiddes JC, Hutchison CA, Slocombe PM, Smith M (1978) The nucleotide sequences of bacteriophage ϕX 174. J Mol Biol 125:225–246
Sanger F, Coulson AR, Hong GF, Hill DF, Petersen GB (1982) Nucleotide sequence of bacteriophage λ DNA. J Mol Biol 162:729–773
Shaw RF, Bloom RW, Bowman JE (1977) Hemoglobin and the genetic code. Evolution of protection against somatic mutation. J Mol Evol 9:225–230
Shepherd JCW (1981) Method to determine the reading frame of a protein from the purine/pyrimidine genome sequence and its possible evolutionary justification. Proc Natl Acad Sci USA 78:1596–1600
Smith TF, Waterman MS, Sadler JR (1983) Statistical characterization of nucleic acid sequence functional domains. Nucleic Acids Res 11:2205–2219
Studier FW (1972) Bacteriophage T7. Science 176:367–376
Studier FW (1975) Gene 0.3 of bacteriophage T7 acts to overcome the DNA restriction system of the host. J Mol Biol 94: 283–295
Van Valen L (1973) A new evolutionary law. Evol Theory 1: 1–30
Yuan R (1981) Structure and mechanism of multifunctional restriction endonucleases. Annu Rev Biochem 50:285–315
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sharp, P.M., Rogers, M.S. & McConnell, D.J. Selection pressures on codon usage in the complete genome of bacteriophage T7. J Mol Evol 21, 150–160 (1985). https://doi.org/10.1007/BF02100089
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF02100089