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Genetics. May 1999; 152(1): 269–280.
PMCID: PMC1460604

Synonymous rates at the RpII215 gene of Drosophila: variation among species and across the coding region.

Abstract

The region encompassing the RpII215 gene that encodes the largest component of the RNA polymerase II complex (1889 amino acids) has been sequenced in Drosophila subobscura, D. madeirensis, D. guanche, and D. pseudoobscura. Nonsynonymous divergence estimates (Ka) indicate that this gene has a very low rate of amino acid replacements. Given its low Ka and constitutive expression, synonymous substitution rates are, however, unexpectedly high. Sequence comparisons have allowed the molecular clock hypothesis to be tested. D. guanche is an insular species and it is therefore expected to have a reduced effective size relative to D. subobscura. The significantly higher rate of synonymous substitutions detected in the D. guanche lineage could be explained if synonymous mutations behave as nearly neutral. Significant departure from the molecular clock hypothesis for synonymous and nonsynonymous substitutions was detected when comparing the D. subobscura, D. pseudoobscura, and D. melanogaster lineages. Codon bias and synonymous divergence between D. subobscura and D. melanogaster were negatively correlated across the RpII215 coding region, which indicates that selection coefficients for synonymous mutations vary across the gene. The C-terminal domain (CTD) of the RpII215 protein is structurally and functionally differentiated from the rest of the protein. Synonymous substitution rates were significantly different in both regions, which strongly indicates that synonymous mutations in the CTD and in the non-CTD regions are under detectably different selection coefficients.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 1994 Mar;136(3):927–935. [PMC free article] [PubMed]
  • Akashi H. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics. 1995 Feb;139(2):1067–1076. [PMC free article] [PubMed]
  • Jokerst RS, Weeks JR, Zehring WA, Greenleaf AL. Analysis of the gene encoding the largest subunit of RNA polymerase II in Drosophila. Mol Gen Genet. 1989 Jan;215(2):266–275. [PubMed]
  • Kimura M. Evolutionary rate at the molecular level. Nature. 1968 Feb 17;217(5129):624–626. [PubMed]
  • Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. [PubMed]
  • Allison LA, Moyle M, Shales M, Ingles CJ. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell. 1985 Sep;42(2):599–610. [PubMed]
  • Kimura M, Ota T. On the rate of molecular evolution. J Mol Evol. 1971;1(1):1–17. [PubMed]
  • Allison LA, Wong JK, Fitzpatrick VD, Moyle M, Ingles CJ. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function. Mol Cell Biol. 1988 Jan;8(1):321–329. [PMC free article] [PubMed]
  • Barrio E, Ayala FJ. Evolution of the Drosophila obscura species group inferred from the Gpdh and Sod genes. Mol Phylogenet Evol. 1997 Feb;7(1):79–93. [PubMed]
  • Barrio E, Latorre A, Moya A, Ayala FJ. Phylogenetic reconstruction of the Drosophila obscura group, on the basis of mitochondrial DNA. Mol Biol Evol. 1992 Jul;9(4):621–635. [PubMed]
  • Baskaran R, Dahmus ME, Wang JY. Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11167–11171. [PMC free article] [PubMed]
  • Langley CH, Fitch WM. An examination of the constancy of the rate of molecular evolution. J Mol Evol. 1974;3(3):161–177. [PubMed]
  • Bingham PM, Levis R, Rubin GM. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. [PubMed]
  • Lawrence JG, Hartl DL, Ochman H. Molecular considerations in the evolution of bacterial genes. J Mol Evol. 1991 Sep;33(3):241–250. [PubMed]
  • Bulmer M. Estimating the variability of substitution rates. Genetics. 1989 Nov;123(3):615–619. [PMC free article] [PubMed]
  • Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991 Nov;129(3):897–907. [PMC free article] [PubMed]
  • Marfany G, Gonzàlez-Duarte R. Characterization and evolution of the Adh genomic region in Drosophila guanche and Drosophila madeirensis. Mol Phylogenet Evol. 1993 Mar;2(1):13–22. [PubMed]
  • Comeron JM, Aguadé M. Synonymous substitutions in the Xdh gene of Drosophila: heterogeneous distribution along the coding region. Genetics. 1996 Nov;144(3):1053–1062. [PMC free article] [PubMed]
  • McCracken S, Fong N, Rosonina E, Yankulov K, Brothers G, Siderovski D, Hessel A, Foster S, Shuman S, Bentley DL. 5'-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 1997 Dec 15;11(24):3306–3318. [PMC free article] [PubMed]
  • Comeron JM, Aguadé M. Synonymous substitutions in the Xdh gene of Drosophila: heterogeneous distribution along the coding region. Genetics. 1996 Nov;144(3):1053–1062. [PMC free article] [PubMed]
  • Comeron JM, Aguadé M. An evaluation of measures of synonymous codon usage bias. J Mol Evol. 1998 Sep;47(3):268–274. [PubMed]
  • Comeron JM, Kreitman M. The correlation between synonymous and nonsynonymous substitutions in Drosophila: mutation, selection or relaxed constraints? Genetics. 1998 Oct;150(2):767–775. [PMC free article] [PubMed]
  • Comeron JM, Kreitman M, Aguadé M. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999 Jan;151(1):239–249. [PMC free article] [PubMed]
  • Morton BR. Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability. J Mol Evol. 1993 Sep;37(3):273–280. [PubMed]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [PMC free article] [PubMed]
  • Nonet M, Sweetser D, Young RA. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell. 1987 Sep 11;50(6):909–915. [PubMed]
  • Eyre-Walker A, Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993 Sep 25;21(19):4599–4603. [PMC free article] [PubMed]
  • Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. [PMC free article] [PubMed]
  • Gillespie JH. Lineage effects and the index of dispersion of molecular evolution. Mol Biol Evol. 1989 Nov;6(6):636–647. [PubMed]
  • Papaceit M, Prevosti A. Differences in chromosome A arrangement between Drosophila madeirensis and Drosophila subobscura. Experientia. 1989 Mar 15;45(3):310–312. [PubMed]
  • Hasegawa M, Yasunaga T, Miyata T. Secondary structure of MS2 phage RNA and bias in code word usage. Nucleic Acids Res. 1979 Dec 11;7(7):2073–2079. [PMC free article] [PubMed]
  • Parsch J, Tanda S, Stephan W. Site-directed mutations reveal long-range compensatory interactions in the Adh gene of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):928–933. [PMC free article] [PubMed]
  • Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. [PubMed]
  • Precup J, Parker J. Missense misreading of asparagine codons as a function of codon identity and context. J Biol Chem. 1987 Aug 15;262(23):11351–11355. [PubMed]
  • Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed]
  • Ramos-Onsins S, Segarra C, Rozas J, Aguadé M. Molecular and chromosomal phylogeny in the obscura group of Drosophila inferred from sequences of the rp49 gene region. Mol Phylogenet Evol. 1998 Feb;9(1):33–41. [PubMed]
  • True JR, Mercer JM, Laurie CC. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Yuryev A, Corden JL. Suppression analysis reveals a functional difference between the serines in positions two and five in the consensus sequence of the C-terminal domain of yeast RNA polymerase II. Genetics. 1996 Jun;143(2):661–671. [PMC free article] [PubMed]
  • Segarra C, Aguadé M. Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics. 1992 Mar;130(3):513–521. [PMC free article] [PubMed]
  • Zeng LW, Comeron JM, Chen B, Kreitman M. The molecular clock revisited: the rate of synonymous vs. replacement change in Drosophila. Genetica. 1998;102-103(1-6):369–382. [PubMed]
  • Shields DC, Sharp PM, Higgins DG, Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. [PubMed]
  • Zhang J, Corden JL. Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J Biol Chem. 1991 Feb 5;266(4):2290–2296. [PubMed]
  • Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. [PMC free article] [PubMed]
  • Stephan W, Kirby DA. RNA folding in Drosophila shows a distance effect for compensatory fitness interactions. Genetics. 1993 Sep;135(1):97–103. [PMC free article] [PubMed]

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