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Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes

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Abstract

We present a new approach for analyzing directional mutation pressure and nucleotide content in protein-coding genes. Directional mutation pressure, the heterogeneity in the likelihood of different nucleotide substitutions, is used to explain the increasing or decreasing guanine-cytosine content (GC%) in DNA and is represented by µD, in agreement with Sueoka (1962, Proc Natl Acad Sci USA 48:582–592). The new method uses simulation to facilitate identification of significant A + T or G + C pressure as well as the comparison of directional mutation pressure among genes, even when they are translated by different genetic codes. We use the method to analyze the evolution of directional mutation pressure and nucleotide content of mitochondrial cytochrome b genes. Results from a survey of 110 taxa indicate that the cytochrome b genes of most taxa are subjected to significant directional mutation pressure and that the gene is subject to A + T pressure in most cases. Only in the anseriform bird Cairina moschata is the cytochrome b gene subject to significant G + C pressure. The GC% at nonsynonymous codon sites decreases proportionately with increasing A + T pressure, and with a slope less than one, indicating a presence of selective constraints. The cytochrome b genes of insects, nematodes, and eumycotes are subject to extreme A + T pressures (µD = 0.123, 0.224, and 0.130) and, in parallel, the GC% of the nonsynonymous codon sites has decreased from about 0.44 in organisms that are not subjected to A + T or G + C pressure to about 0.332, 0.323, and 0.367, respectively. The distribution of taxa according to the GC% at nonsynonymous codon sites and directional mutation pressure supports the notion that variation in these parameters is a phylogenetic component.

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References

  • Asakawa S, Kumuzawa Y, Araki T, Himeno H, Miura K-I, Watanabe K (1991) Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32: 511–520

    Google Scholar 

  • Asawaka S, Himeno H, Miura K-I, Watanabe K (1994) Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics (submitted)

  • Belozersky AN, Spirin AS (1958) A correlation between the compositions of deoxyribonucleic and ribonucleic acids. Nature 182: 111–112

    Google Scholar 

  • Bernardi G (1989) The isochore organization of the human genome. Annu Rev Genet 23: 637–661

    Google Scholar 

  • Bernardi G, Olofsson B, Filipski J, Zerial M, Salanis J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228: 953–958

    Google Scholar 

  • Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24: 1–11

    Google Scholar 

  • Clayton DA (1992) Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol 141: 217–323

    Google Scholar 

  • Collins DW, Jukes TH (1993) Relationship between G + G in silent sites of codons and amino acid composition of human proteins. J Mol Evol 36: 201–213

    Google Scholar 

  • Cox EC, Yanofsky C (1967) Altered base ratios in the DNA of an Echerichia coli mutator strain. Proc Natl Acad Sci USA 58: 1895–1902

    Google Scholar 

  • Crozier RH, Crozier YC (1992) The cytochrome b and ATPase genes of honeybee mitochondrial DNA. Mol Biol Evol 9: 474–482

    Google Scholar 

  • Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 113: 97–117

    Google Scholar 

  • di Rago J-P, Netter P, Slonimski PP (1990) Pseudo-wild type revertants from inactive apocytochrome b mutants as a tool for the analysis of the structure/function relationships of the mitochondrial ubiquinol-cytochrome c reductase of Saccharomyces cerevisiae. J Biol Chem 265: 3332–3339

    Google Scholar 

  • D'Onofrio GD, Mouchiroud D, Aïssani B, Gautier C, Bernardi G (1991) Correlations between the compositional properties of human genes, codon usage, and amino acid composition of proteins. J Mol Evol 32: 504–510

    Google Scholar 

  • Freese E (1962) On the evolution of base composition of DNA. J Theor Biol 3: 82–101

    Google Scholar 

  • Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54: 1015–1069

    Google Scholar 

  • Helm-Bychowski K, Cracraft J (1993) Recovering phylogenetic signal from DNA sequences: relationship within the Corvine assemblage (Class Aves) as inferred from complete sequences of the mtDNA cytochrome b gene. Mol Biol Evol 10: 1196–1214

    Google Scholar 

  • Hemmingsen SM, Woolford C, van der Vies SM, Tilly K, Bennis DT, Georgopoulos C, Hendrix RW, Ellis RJ (1989) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333: 330–334

    Google Scholar 

  • Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4: 445–472

    Google Scholar 

  • Howell N (1989) Evolutionary conservation of protein regions in the protonmotive cytochrome b and their possible roles in redox catalysis. J Mol Evol 29: 157–169

    Google Scholar 

  • Howell N, Gilbert K (1988) Mutational analysis of the mouse mitochondrial cytochrome b gene. J Mol Biol 203: 607–618

    Google Scholar 

  • Irwin DA, Kocher TD, Wilson AC (1991) Evolution of cytochrome b gene of mammals. J Mol Evol 32: 128–144

    Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Pääbo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137: 243–256

    Google Scholar 

  • Jermiin LS, Crozier RH (1994) The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in hymenoptera may be associated with nucleotide content. J Mol Evol 38: 282–294

    Google Scholar 

  • Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G + C content of some mitochondrial and bacterial genes. J Mol Evol 24: 39–44

    Google Scholar 

  • Kagawa Y, Nojima H, Nukiwa N, Ishizuka M, Nakajima T, Yasuhara T, Tanaka T, Oshima T (1984) High guanine plus cytosine content in third letter of codons of an extreme thermophile. J Biol Chem 259: 2956–2960

    Google Scholar 

  • Kornegay JR, Kocher TD, Williams LA, Wilson AC (1993) Pathways of lysosyme evolution inferred from the sequences of cytochrome b in birds. J Mol Evol 37: 367–379

    Google Scholar 

  • Kushino A, Shimizu M, Tomita K-I (1987) Molecular cloning and sequence determination of the tuf gene coding for the elongation factor Tu of Thermus thermophilus HB8. Eur J Biochem 170: 93–98

    Google Scholar 

  • Kunkel TA (1985) The mutational specificity of DNA polymerase-α and -γ during in vitro DNA synthesis. J Biol Chem 135: 327–351

    Google Scholar 

  • Kusmierski R, Borgia G, Crozier RH, Chan BHY (1993) Molecular information on bower-bird phylogeny and the evolution of exaggerated male characteristics. J Evol Biol 6: 737–752

    Google Scholar 

  • Lee KY, Wahl R, Barbu E (1956) Contenu en bases puriques et pyrimidiques des acids desoxyribonucleiques des bacteries. Ann Inst Pasteur 91: 212–224

    Google Scholar 

  • Li W-H, Graur D (1991) Fundamentals of molecular evolution. Sinaur Associates, Sunderland, MA, pp 1–284

    Google Scholar 

  • Ma D-P, Zharkikh A, Graur D, VandeBerg JL, Li W-H (1993) Structure and evolution of opussum, guinea pig, and porcupine cytochrome b genes. J Mol Evol 36: 327–334

    Google Scholar 

  • Martin AP, Palumbi SR (1993) Protein evolution in different cellular environments: cytochrome b in sharks and mammals. Mol Biol Evol 10: 873–891

    Google Scholar 

  • Mouchiroud D, Gautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol 27: 311–320

    Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84: 166–169

    Google Scholar 

  • Ohama T, Yamao F, Muto A, Osawa S (1987) Organization and codon usage of the streptomycin operon in Micrococcus luteus, a bacterium with a high genomic G + C content. J Bacteriol 169: 7440–4777

    Google Scholar 

  • Ohama T, Yamao F, Muto A, Osawa S (1989) Sprectinomycin operon of Micrococcus luteus: evolutionary implications of organization and novel codon usage. J Mol Evol 29: 381–395

    Google Scholar 

  • Ohkubo S, Muto A, Kawauchi Y, Yamao F, Osawa S (1987) The ribosomal protein gene cluster of Mycoplasma capricolum. Mol Gen Genet 210: 314–322

    Google Scholar 

  • Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130: 471–498

    Google Scholar 

  • Osawa S, Jukes TH, Watanabe K, Muto A (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56: 229–264

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223–225

    Google Scholar 

  • Rolfe R, Meselson M (1959) The relative homogeneity of microbial DNA. Proc Natl Acad Sci USA 45: 1039–1043

    Google Scholar 

  • Sueoka N (1959) A statistical analysis of deoxyribonucleic acid distribution in density gradient centrifugation. Proc Natl Acad Sci USA 45: 1480–1490

    Google Scholar 

  • Sueoka N (1961a) Correlation between base composition of deoxyribonucleic acid and amino acid composition of protein. Proc Natl Acad Sci USA 47: 1141–1149

    Google Scholar 

  • Sueoka N (1961b) Compositional correlation between deoxyribonucleic acid and protein. Cold Spring Harbor Symp Quant Biol 26: 35–43

    Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48: 582–592

    Google Scholar 

  • Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85: 2653–2657

    Google Scholar 

  • Sueoka N (1992) Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol 34: 95–114

    Google Scholar 

  • Sueoka N, Marmur J, Doty P (1959) Heterogeneity in deoxyribonucleic acids. II. Dependence of the density of deoxyribonucleic acids on the guanine-cytocine. Nature 183: 1427–1431

    Google Scholar 

  • Tamura K (1992) The rate and pattern of nucleotide substitution in Drosophila mtDNA. Mol Biol Evol 9: 814–825

    Google Scholar 

  • Tron T, Crimi M, Colson A-M, Degli Esposti M (1991) Structure/function relationships in mitochondrial cytochrome b revealed by the kinetic and circular dichroic properties of two yeast inhibitor-resistant mutants. Eur J Biochem 199: 753–760

    Google Scholar 

  • Wada A, Suyama A (1986) Local stability of DNA and RNA secondary structure and its relation to biological functions. Prog Biophys Mol Biol 47: 113–157

    Google Scholar 

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  1. Dan Graur

    Present address: Department of Zoology, George S. Wise Faculty of Life Science, Tel Aviv University, Ramat Aviv 69978, Israel

Authors and Affiliations

  1. School of Genetics and Human Variation, La Trobe University, 3083, Bundoora, Victoria, Australia

    Lars S. Jermiin, Dan Graur, Roger M. Lowe & Ross H. Crozier

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  1. Lars S. Jermiin
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  3. Roger M. Lowe
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Jermiin, L.S., Graur, D., Lowe, R.M. et al. Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes. J Mol Evol 39, 160–173 (1994). https://doi.org/10.1007/BF00163805

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