Strong regional heterogeneity in base composition evolution on the Drosophila X chromosome

Genetics

Volumn 174, Issue 1, 2006, Pages 349-362

  Ko, Wen Ya ^a   Piao, Shengfu ^a   Akashi, Hiroshi ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME SUBSTITUTION; CONTROLLED STUDY; DNA BASE COMPOSITION; DROSOPHILA MELANOGASTER; EVOLUTION; GENE CONVERSION; GENE LOCUS; GENE MUTATION; GENE SILENCING; GENETIC HETEROGENEITY; GENOME; INTRON; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; TELOMERE; X CHROMOSOME;

ANIMALS; BASE COMPOSITION; CELL LINEAGE; CODON; DROSOPHILA; EVOLUTION, MOLECULAR; GENETIC VARIATION; INTRONS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; TELOMERE; VARIATION (GENETICS); X CHROMOSOME;

DROSOPHILA MELANOGASTER; DROSOPHILA ORENA; DROSOPHILA YAKUBA; MAMMALIA;

EID: 33748889490     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.105.054346     Document Type: Article

References (96)

1. ABAD, J. P., B. DE PABLOS, K. OSOEGAWA, P. J. DE JONG, A. MARTIN-GALLARDO et al., 2004 Genomic analysis of Drosophila melanogaster telomeres: full-length copies of HeT-A and TART elements at telomeres. Mol. Biol. Evol. 21: 1613-1619.
2. AKASHI, H., 1995 Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139: 1067-1076.
3. AKASHI, H., 1996 Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144: 1297-1307.
4. AKASHI, H., 1999 Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151: 221-238.
5. AKASHI, H., 2001 Gene expression and molecular evolution. Curr. Opin. Genet. Dev. 11: 660-666.
6. AKASHI, H., 2003 Translational selection and yeast proteome evolution. Genetics 164: 1291-1303.
7. AKASHI, H., W.-Y. KO, S. PIAO, A. JOHN, P. GOEL et al., 2006 Molecular evolution in the Drosophila melanogaster species subgroup: frequent parameter fluctuations on the timescale of molecular divergence. Genetics 172: 1711-1726.
8. ALTSCHUL, S. F., W. GISH, W. MILLER, E. W. MYERS and D. J. LIPMAN, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
9. ANDERSSON, S. G., and C. G. KURLAND, 1990 Codon preferences in free-living microorganisms. Microbiol. Rev. 54: 198-210.
10. ANDOLFATTO, P., 2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
11. ANDOLFATTO, P., and J. D. WALL, 2003 Linkage disequilibrium patterns across a recombination gradient in African Drosophila melanogaster. Genetics 165: 1289-1305.
12. ARNDT, P. F., D. A. PETROV and T. HWA, 2003 Distinct changes of genomic biases in nucleotide substitution at the time of mammalian radiation. Mol. Biol. Evol. 20: 1887-1896.
13. BACHTROG, D., 2003 Protein evolution and codon usage bias on the neo-sex chromosomes of Drosophila miranda. Genetics 165: 1221-1232.
14. BAILEY, J. A., L. CARREL, A. CHAKRAVARTI and E. E. EICHLER, 2000 Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc. Natl. Acad. Sci. USA 97: 6634-6639.
15. BEGUN, D. J., and P. WHITLEY, 2002 Molecular population genetics of Xdh and the evolution of base composition in Drosophila. Genetics 162: 1725-1735.
16. BELLE, E. M., L. DURET, N. GALTIER and A. EYRE-WALKER, 2004 The decline of isochores inmammals: an assessment of the GC content variation along the mammalian phylogeny. J. Mol. Evol. 58: 653-660.
17. BERGMAN, C. M., and M. KREITMAN, 2001 Analysis of conserved noncoding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences. Genome Res. 11: 1335-1345.
18. BERNARDI, G., 1995 The human genome: organization and evolutionary history. Annu. Rev. Genet. 29: 445-476.
19. BERNARDI, G., 2000 The compositional evolution of vertebrate genomes. Gene 259: 31-43.
20. BIESSMANN, H., and J. M. MASON, 1997 Telomere maintenance without telomerase. Chromosoma 106: 63-69.
21. BIESSMANN, H., S. PRASAD, M. F. WALTER and J. M. MASON, 2005 Euchromatic and heterochromatic domains at Drosophila telomeres. Biochem. Cell Biol. 83: 477-485.
22. BOIVIN, A., C. GALLY, S. NETTER, D. ANXOLABEHERE and S. RONSSERAY, 2003 Telomeric-associated sequences of Drosophila recruit polycomb-group proteins in vivo and can induce pairing-sensitive repression. Genetics 164: 195-208.
23. BRAVERMAN, J. M., B. P. LAZZARO, M. AGUADE and C. H. LANGLEY, 2005 DNA sequence polymorphism and divergence at the erect wing and suppressor of sable loci of Drosophila melanogaster and D. simulans. Genetics 170: 1153-1165.
24. BUSTAMANTE, C. D., J. WAKELEY, S. SAWYER and D. L. HARTL, 2001 Directional selection and the site-frequency spectrum. Genetics 159: 1779-1788.
25. CARREL, L., and H. F. WILLARD, 2005 X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
26. CASACUBERTA, E., and M. L. PARDUE, 2002 Coevolution of the telomeric retrotransposons across Drosophila species. Genetics 161: 1113-1124.
27. CASACUBERTA, E., and M. L. PARDUE, 2003a Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc. Natl. Acad. Sci. USA 100: 3363-3368.
28. CASACUBERTA, E., and M. L. PARDUE, 2003b HeT-A elements in Drosophila virilis: retrotransposon telomeres are conserved across the Drosophila genus. Proc. Natl. Acad. Sci. USA 100: 14091-14096.
29. CHARLESWORTH, B., 1994 The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63: 213-227.
30. CHEN, S. L., W. LEE, A. K. HOTTES, L. SHAPIRO and H. H. MCADAMS, 2004 Codon usage between genomes is constrained by genomewide mutational processes. Proc. Natl. Acad. Sci. USA 101: 3480-3485.
31. COMERON, J. M., M. KREITMAN and M. AGUADE, 1999 Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151: 239-249.
32. DANILEVSKAYA, O. N., C. TAN, J. WONG, M. ALIBHAI and M. L. PARDUE, 1998 Unusual features of the Drosophila melanogaster telomere transposable element HeT-A are conserved in Drosophila yakuba telomere elements. Proc. Natl. Acad. Sci. USA 95: 3770-3775.
33. DRYSDALE, R. A., M. A. CROSBY and the FLYBASE CONSORTIUM, 2005 FlyBase: genes and gene models. Nucleic Acids Res. 33: D390-D395.
34. DURET, L., 2002 Evolution of synonymous codon usage in metazoans. Curr. Opin. Genet. Dev. 12: 640-649.
35. DURET, L., M. SEMON, G. PIGANEAU, D. MOUCHIROUD and N. GALTIER, 2002 Vanishing GC-rich isochores in mammalian genomes. Genetics 162: 1837-1847.
36. FELSENSTEIN, J., 1974 Uncorrelated genetic drift of gene frequencies and linkage disequilibrium in some models of linked over-dominant polymorphisms. Genet Res. 24: 281-294.
37. FREESE, E., 1962 On the evolution of base composition at DNA. J. Theor. Biol. 3: 82-101.
38. GALTIER, N., and M. GOUY, 1998 Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis. Mol. Biol. Evol. 15: 871-879.
39. GILBERT, D. M., 2002 Replication timing and transcriptional control: beyond cause and effect. Curr. Opin. Cell Biol. 14: 377-383.
40. GIOVANNONI, S. J., H. J. TRIPP, S. GIVAN, M. PODAR, K. L. VERGIN et al., 2005 Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242-1245.
41. GRANTHAM, R., C. GAUTIER, M. GOUY, M. JACOBZONE and R. MERCIER, 1981 Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 9: r43-r74.
42. GU, X., D. HEWETT-EMMETT and W. H. LI, 1998 Directional mutational pressure affects the amino acid composition and hydrophobicity of proteins in bacteria. Genetica 102-103: 383-391.
43. HADDRILL, P. R., B. CHARLESWORTH, D. L. HALLIGAN and P. ANDOLFATTO, 2005 Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol. 6: R67.
44. HALLIGAN, D. L., A. EYRE-WALKER, P. ANDOLFATTO and P. D. KEIGHTLEY, 2004 Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res. 14: 273-279.
45. HASEGAWA, M., H. KISHINO and T. YANO, 1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160-174.
46. HEY, J., and R. M. KLIMAN, 2002 Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160: 595-608.
47. HIGGINS, D. G., and P. M. SHARP, 1988 CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237-244.
48. HILL, W. G., and A. ROBERTSON, 1966 The effect of linkage on limits to artificial selection. Genet. Res. 8: 269-294.
49. HWANG, D. G., and P. GREEN, 2004 Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc. Natl. Acad. Sci. USA 101: 13994-14001.
50. IKEMURA, T., 1985 Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2: 13-34.
51. KEIGHTLEY, P. D., and T. JOHNSON, 2004 MCALIGN: stochastic alignment of noncoding DNA sequences based on an evolutionary model of sequence evolution. Genome Res. 14: 442-450.
52. KERN, A. D., and D. J. BEGUN, 2005 Patterns of polymorphism and divergence from non-coding sequences of D. melanogaster and D. simulans: evidence for non-equilibrium processes. Mol. Biol. Evol. 22: 51-62.
53. KLIMAN, R. M., and J. HEY, 1993 Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10: 1239-1258.
54. KNIGHT, R. D., S. J. FREELAND and L. F. LANDWEBER, 2001 A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol. 2: RESEARCH0010.
55. KO, W. Y., R. M. DAVID and H. AKASHI, 2003 Molecular phylogeny of the Drosophila melanogaster species subgroup. J. Mol. Evol. 57: 562-573.
56. a) regions of the Drosophila melanogaster X chromosome. Genetics 156: 1837-1852.
57. LEMEUNIER, F., B. DUTRILLAUX and M. ASHBURNER, 1978 Relationships within the melanogaster subgroup species subgroup of the genus Drosophila (Sophophora). III. The mitotic chromosomes and quinacrine fluorescent patterns of the polytene chromosomes. Chromosoma 69: 349-361.
58. LI, W. H., 1987 Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J. Mol. Evol. 24: 337-345.
59. LOBRY, J. R., 1997 Influence of genomic G+C content on average amino-acid composition of proteins from 59 bacterial species. Gene 205: 309-316.
60. LYON, M. F., 1998 X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80: 133-137.
61. MARAIS, G., and G. PIGANEAU, 2002 Hill-Robertson interference is a minor determinant of variations in codon bias across Drosophila melanogaster and Caenorhabditis elegans genomes. Mol. Biol. Evol. 19: 1399-1406.
62. MARAIS, G., D. MOUCHIROUD and L. DURET, 2001 Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc. Natl. Acad. Sci. USA 98: 5688-5692.
63. MARAIS, G., D. MOUCHIROUD and L. DURET, 2003 Neutral effect of recombination on base composition in Drosophila. Genet. Res. 81: 79-87.
64. MARAIS, G., P. NOUVELLET, P. D. KEIGHTLEY and B. CHARLESWORTH, 2005 Intron size and exon evolution in Drosophila. Genetics 170: 481-485.
65. MCVEAN, G. A., and B. CHARLESWORTH, 2000 The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155: 929-944.
66. MELNIKOVA, L., and P. GEORGIEV, 2005 Drosophila telomeres: the non-telomerase alternative. Chromosome Res. 13: 431-441.
67. MIKHAILOVSKY, S., T. BELENKAYA and P. GEORGIEV, 1999 Broken chromosomal ends can be elongated by conversion in Drosophila melanogaster. Chromosoma 108: 114-120.
68. MORAN, N. A., 1996 Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93: 2873-2878.
69. MOUNT, S. M., C. BURKS, G. HERTZ, G. D. STORMO, O. WHITE et al., 1992 Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res. 20: 4255-4262.
70. MUNTÉ, A., M. AGUADÉ and C. SEGARRA, 2001 Changes in the recombinational environment affect divergence in the yellow gene of Drosophila. Mol. Biol. Evol. 18: 1045-1056.
71. MUTO, A., and S. OSAWA, 1987 The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl. Acad. Sci. USA 84: 166-169.
72. PARDUE, M. L., and P. G. DEBARYSHE, 2003 Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu. Rev. Genet. 37: 485-511.
73. PÉREZ, J. A., A. MUNTÉ, J. ROZAS, C. SEGARRA and M. AGUADÉ, 2003 Nucleotide polymorphism in the RpII215 gene region of the insular species Drosophila guanche: reduced efficacy of weak selection on synonymous variation. Mol. Biol. Evol. 20: 1867-1875.
74. POWELL, J., E. SEZZI, E. MORIYAMA, J. GLEASON and A. CACCONE, 2003 Analysis of a shift in codon usage in Drosophila. J. Mol. Evol. 57: S214-S225.
75. ROCHA, E. P., and A. DANCHIN, 2002 Base composition bias might result from competition for metabolic resources. Trends Genet. 18: 291-294.
76. RODRÍGUEZ-TRELLES, F., R. TARRIO and F. J. AYALA, 1999 Switch in codon bias and increased rates of amino acid substitution in the Drosophila saltans species group. Genetics 153: 339-350.
77. RODRÍGUEZ-TRELLES, F., R. TARRIO and F. J. AYALA, 2000a Fluctuating mutation bias and the evolution of base composition in Drosophila. J. Mol. Evol. 50: 1-10.
78. RODRÍGUEZ-TRELLES, F., R. TARRIO and F. J. AYALA, 2000b Evidence for a high ancestral GC content in Drosophila. Mol. Biol. Evol. 17: 1710-1717.
79. SAVITSKY, M., T. KAHN, E. POMERANTSEVA and P. GEORGIEV, 2003 Transvection at the end of the truncated chromosome in Drosophila melanogaster. Genetics 163: 1375-1387.
80. SCHÜBELER, D., D. SCALZO, C. KOOPERBERG, B. VAN STEENSEL, J. DELROW et al., 2002 Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat. Genet. 32: 438-442.
81. SHARP, P. M., M. AVEROF, A. T. LLOYD, G. MATASSI and J. F. PEDEN, 1995 DNA sequence evolution: the sounds of silence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 349: 241-247.
82. SINGER, C. E., and B. N. AMES, 1970 Sunlight ultraviolet and bacterial DNA base ratios. Science 170: 822-825.
83. SINGER, G. A., and D. A. HICKEY, 2000 Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol. Biol. Evol. 17: 1581-1588.
84. SMITH, N. G., and A. EYRE-WALKER, 2002 The compositional evolution of the murid genome. J. Mol. Evol. 55: 197-201.
85. SUEOKA, N., 1962 On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl. Acad. Sci. USA 48: 582-592.
86. SUEOKA, N., 1964 On the evolution of informational macromolecules, pp. 479-496 in Evolving Genes and Proteins, edited by V. BRYSON and H. J. VOGEL. Academic Press, New York.
87. TAKANO, T. S., 1998 Rate variation of DNA sequence evolution in the Drosophila lineages. Genetics 149: 959-970.
88. TAKANO-SHIMIZU, T., 1999 Local recombination and mutation effects on molecular evolution in Drosophila. Genetics 153: 1285-1296.
89. TAKANO-SHIMIZU, T., 2001 Local changes in GC/AT substitution biases and in crossover frequencies on Drosophila chromosomes. Mol. Biol. Evol. 18: 606-619.
90. TENZEN, T., T. YAMAGATA, T. FUKAGAWA, K. SUGAYA, A. ANDO et al., 1997 Precise switching of DNA replication timing in the GC content transition area in the human major histocompatibility complex. Mol. Cell. Biol. 17: 4043-4050.
91. WATANABE, Y., A. FUJIYAMA, Y. ICHIBA, M. HATTORI, T. YADA et al., 2002 Chromosome-wide assessment of replication timing for human chromosomes 11q and 21q: disease-related genes in timing-switch regions. Hum. Mol. Genet. 11: 13-21.
92. WEBSTER, M. T., N. G. SMITH and H. ELLEGREN, 2003 Compositional evolution of noncoding DNA in the human and chimpanzee genomes. Mol. Biol. Evol. 20: 278-286.
93. WHEELER, D. L., T. BARRETT, D. A. BENSON, S. H. BRYANT, K. CANESE et al., 2005 Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 33: D39-D45.
94. WOLFE, K. H., P. M. SHARP and W. H. LI, 1989 Mutation rates differ among regions of the mammalian genome. Nature 337: 283-285.
95. WOOTTON, J. C., and S. FEDERHEN, 1996 Analysis of compositionally biased regions in sequence databases. Methods Enzymol. 266: 554-571.
96. YANG, Z., 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.