RNA secondary structure and compensatory evolution

Genes and Genetic Systems

Volumn 74, Issue 6, 1999, Pages 271-286

  Chen, Ying ^a   Carlini, David B ^a   Baines, John F ^a   Parsch, John ^a,c   Braverman, John M ^a,d   Tanda, Soichi ^b   Stephan, Wolfgang ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c HARVARD UNIVERSITY   (United States)

^d LE MOYNE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MESSENGER RNA PRECURSOR; RNA;

ARTICLE; CODON; DNA SEQUENCE; DROSOPHILA MELANOGASTER; EPISTASIS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; RNA BINDING; RNA SPLICING; RNA STRUCTURE;

ALCOHOL DEHYDROGENASE; ANIMALS; CODON; DROSOPHILA; EVOLUTION; GENETICS, POPULATION; MODELS, BIOLOGICAL; MUTATION; NUCLEIC ACID CONFORMATION; RNA; RNA SPLICING;

DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0033497101     PISSN: 13417568     EISSN: None     Source Type: Journal    
DOI: 10.1266/ggs.74.271     Document Type: Article

References (109)

1. Akashi, H. (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136, 927-935.
2. Anderson, C. L., Carew, E. A. and Powell, J. R. (1993) Evolution of the Adh locus in the Drosophila willistoni group: the loss of an intron, and shift in codon usage. Mol. Biol. Evol. 10, 605-618.
3. Antezana, M. A. and Kreitman, M. (1999) The nonrandom location of synonymous codons suggests that reading frame-in-dependent forces have patterned codon preferences. J. Mol. Evol. 49, 36-43.
4. Aquadro, C. F., Desse, S. F., Bland, M. M., Langley, C. H. and Laurie-Ahlberg, C. C. (1986) Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics 114, 1165-1190.
5. Benyajati, C., Spoerel, N., Haymerle, H. and Ashburner, M. (1983) The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5' end in different developmental stages. Cell 33, 125-133.
6. Benyajati, C., Wang, N., Reddy, A., Weinberg, E. and Sofer, W. (1980) Alcohol dehydrogenase in Drosophila: isolation and characterization of messenger RNA and cDNA clone. Nucleic Acids Res. 8, 5649-5667.
7. Bernardi, G. and Bernardi, G. (1986) Compositional constraints and genome evolution. J. Mol. Evol. 24, 1-11
8. Bernardi, G., Olofsson, B., Filipski, J., Zerial, M., Salinas, J., Cuny, G., Meunier-Rotival, M. and Rodier, F. (1985) The mosaic genome of warm-blooded vertebrates. Science 228, 953-958.
9. Berry, A. and Kreitman, M. (1993) Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics 134, 869-893.
10. Bulmer, M. (1988) Are codon usage patterns in unicellular organisms determined by selection-mutation balance? J. Evol. Biol. 1, 15-26.
11. Carulli, J. P.; Drane, D. E., Hartl, D. L. and Ochman, H. (1993) Compositional heterogeneity and patterns of molecular evolution in the Drosophila genome. Genetics 134, 837-845.
12. Cate, J. H., Gooding, A. R., Podell, E., Zhou, K., Golden, B. L., Kundrot, C. E., T. R., C. and Doudna, J. A. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 273, 1678-1685.
13. Choudhary, M. and Laurie, C. C. (1991) Use of in vitro mutagenesis to analyze the difference in Adh expression associated with the allozyme polymorphism in Drosophila melanogaster. Genetics 129, 481-488.
14. Comeron, J. M., Kreitman, M. and Aguadé, M. (1999) Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151, 239-249.
15. Coyne, J. A., Barton, N. H. and Turelli, M. (1997) A critique of Sewall Wright's shifting balance theory of evolution. Evolution 51, 643-671.
16. Csank, C., Taylor, F. M. and Martindale, D. W. (1990) Nuclear pre-mRNA introns: analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. Nucleic Acids Res. 18, 5133-5141.
17. D'Orval, B. C., Carafa, Y. D., Sirand-Pugnet, P., Gallego, M., Brody, E. and Marie, J. (1991) RNA secondary structure repression of a muscle-specific exon in HeLa cell nuclear extracts. Science 252, 1823-1828.
18. Eng, F. J. and Warner, J. R. (1991) Structural basis for the regulation of splicing of a yeast messenger RNA. Cell 65, 797-804.
19. Eperon, L. P., Estibeiro, J. P. and Eperon, I. C. (1986) The role of nucleotide sequences in splice site selection in eukaryotic premessenger RNA. Nature 324, 280-282.
20. Eperon, L. P., Graham, I. R., Griffiths, A. D. and Eperon, I. C. (1988) Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase? Cell 54, 393-401.
21. Eyre-Walker, A. (1996) Synonymous codon bias is related to gene length in Escherichia coli: selection for translational accuracy? Mol. Biol. Evol. 13, 864-872.
22. Fletcher, T. S., Ayala, F. J., Thatcher, D. R. and Chambers, G. K. (1978) Structural analysis of the ADHs electromorph of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 75, 5609-5612.
23. Fox, G. E. and Woese, C. R. (1975) 5S rRNA secondary structure. Nature 256, 505-507.
24. Fu, X. Y. and Manley, J. L. (1987) Factors influencing alternative splice site utilization in vivo. Mol. Cell Biol. 7, 738-748.
25. Gallie, D. R. (1991) The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes & Dev. 5, 2108-2116.
26. Goguel, V. and Rosbash, M. (1993) Splice site choice and splicing efficiency are positively influenced by pre-mRNA intramolecular base pairing in yeast. Cell 72, 893-901.
27. Golding, B. (1994) Using maximum likelihood to infer selection from phylogenies. In : Non-neutral Evolution: Theories and Molecular data (ed. : B. Golding), pp. 126-139, Chapman and Hall, New York.
28. Goodall, G. J. and Filipowicz, W. (1989) The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58, 473-483.
29. Grantham, R., Gautier, C., Gouy, M., Mercier, R. and Pave, A. (1980) Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8, 49-62.
30. Haldane, J. B. S. (1931) A mathematical theory of natural selection. Part VIII. Stable metapopulations. Proc. Cambridge. Philos. Soc. 27, 137-142.
31. Halfter, H. and Gallwitz, D. (1988) Impairment of yeast pre-mRNA splicing by potential secondary structure-forming sequences near the conserved branchpoint sequence. Nucleic Acids Res. 16, 10413-10423.
32. Han, K. and Kim, H. J. (1993) Prediction of common folding structures of homologous RNAs. Nucleic Acids Res. 21, 1251-1257.
33. Hedrick, P. W., Jain, S. and Holden, L. (1978) Multilocus systems in evolution. Evol. Biol. 11, 101-182.
34. Huynen, M. A. and Hogeweg, P. (1994) Pattern generation in molecular evolution: exploitation of the variation in RNA landscapes. J. Mol. Evol. 39, 71-79.
35. Huynen, M. A., Konings, D. A. M. and Hogeweg, P. (1992) Equal G and C contents in histone genes indicate selection pressures on mRNA secondary structure. J. Mol. Evol. 34, 280-291.
36. Huynen, M. A., Konings, D. A. M. and Hogeweg, P. (1993) Multiple coding and the evolutionary properties of RNA secondary structure. J. Theor. Biol. 165, 251-267.
37. Ikemura, T. (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J. Mol. Biol. 146, 1-21.
38. Jaeger, J. A., Turner, D. H. and Zuker, M. (1990) Predicting optimal and suboptimal secondary structure for RNA. Methods Enzymol. 183, 281-306.
39. James, B. D., Olsen, G. J. and Pace, N. R. (1989) Phylogenetic comparative analysis of RNA secondary structure. Methods Enzymol 180, 227-239.
40. Kimura, M. (1991) Recent developments of the neutral theory viewed from the Wrightian tradition of theoretical population genetics. Proc. Natl. Acad. Sci. USA 88, 5969-5973.
41. Kimura, M. (1985) The role of compensatory neutral mutations in molecular evolution. J. Genet. 64, 7-19.
42. Kirby, D. A., Muse, S. V. and Stephan, W. (1995) Maintenance of pre-mRNA secondary structure by epistatic selection. Proc. Natl. Acad. Sci. USA 92, 9047-9051.
43. Kliman, R. M. and Hey, J. (1993) Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10, 1239-1258.
44. Ko, C. H., Brendel, V., Taylor, R. D. and Walbot, V. (1998) U-richness is a defining feature of plant introns and may function as an intron recognition signal in maize. Plant Mol. Biol. 36, 573-583.
45. Konings, D. A. and Gutell, R. R. (1995) A comparison of thermodynamic foldings with comparatively derived structures of 16S and 16S-like rRNAs. RNA 1, 559-574.
46. Konings, D. A., van Duijn, L. P., Voorma, H. O. and Hogeweg, P. (1987) Minimal energy foldings of eukaryotic mRNAs form a separate leader domain. J. Theor. Biol. 127, 63-78.
47. Kreitman, M. (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304, 412-417.
48. Langley, C. H., Ito, K. and Voelker, R. A. (1977) Linkage disequilibrium in natural populations of Drosophila melanogaster seasonal variation. Genetics 86, 447-454.
49. Laurie, C. C., Bridgham, J. T. and Choudhary, M. (1991) Associations between DNA sequence variation and variation in expression of the Adh gene in natural populations of Drosophila melanogaster. Genetics 129, 489-499.
50. Laurie, C. C. and Stam, L. F. (1994) The effect of an intronic polymorphism on alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 138, 379-385.
51. Laurie, C. C. and Stam, L. F. (1988) Quantitative analysis of RNA produced by Slow and Fast alleles of Adh in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 85, 5161-5165.
52. Leicht, B. G., Lyckegaard, E. M. S., Benedict, C. M. and Clark, A. G. (1993) Conservation of alternative splicing and genomic organization of the myosin alkali light-chain (Mlc1) gene among Drosophila species. Mol. Biol. Evol. 10, 769-790.
53. Leicht, B. G., Muse, S. V., Hanczyc, M. and Clark, A. G. (1995) Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. Genetics 139, 299-308.
54. Lewontin, R. C. (1985) Population genetics. Ann. Rev. Genet. 19, 81-102.
55. Libri, D., Piseri, A. and Fiszman, M. Y. (1991) Tissue-specific splicing in vivo of the beta-tropomyosin gene: dependence on an RNA secondary structure. Science 252, 1842-1845.
56. Lindsley, D. L. and Grell, R. H. (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst. Wash. Publ. 627.
57. Lindsley, D. L. and Sandier, L. (1977) The genetic analysis of meiosis in female Drosophila melanogaster. Philos. Trans. Royal. Soc. Lond. B Biol. Sci. 277, 295-312.
58. Mercot, H., DeFaye, D., Capy, P., Pla, E. and David, J. R. (1994) Alcohol tolerance, ADH activity, and ecological niche of Drosophila species. Evolution 48, 746-757.
59. Miyashita, N. and Langley, C. H. (1988) Molecular and phenotypic variation of the white locus region in Drosophila melanogaster. Genetics 120, 199-212.
60. Miyashita, N. T., Aguade, M. and Langley, C.H. (1993) Linkage disequilibrium in the white locus region of Drosophila melanogaster. Genet. Res. 62, 101-109.
61. Moriyama, E. N. and Gojobori, T. (1992) Rates of synonymous substitution and base composition of nuclear genes in Drosophila. Genetics 130, 855-864.
62. Moriyama, E. N. and Powell, J. R. (1997) Codon usage bias and tRNA abundance in Drosophila. J. Mol Evol. 45, 514-523.
63. Mount, S. M. (1982) A catalogue of splice junction sequences. Nucleic Acids Res. 10, 459-472.
64. Mount, S. M., Burks, C., Hertz, G., Stormo, G. D., White, O. and Fields, C. (1992) Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res. 20, 4255-4262.
65. Muse, S. V. (1995) Evolutionary analyses of DNA sequences subject to constraints of secondary structure. Genetics 139, 1429-1439.
66. Nakamura, Y., Gojobori, T. and Ikemura, T. (1998) Codon usage tabulated from the international sequence databases. Nucleic Acids Res. 26, 334.
67. Nelson, K. K. and Green, M. R. (1988) Splice site selection and ribonucleoprotein complex assembly during in vitro premRNA splicing. Genes & Dev. 2, 319-329.
68. Noller, H. F. and Woese, C. R. (1981) Secondary structure of 16S ribosomal RNA. Science 212, 403-411.
69. Oakeshott, J. G., Gibson, J. B., Anderson, P. R., Knibb, W. R., Anderson, D. G. and Chambers, G. K. (1982) Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents. Evolution 36, 86-96.
70. Ohshima, Y. and Gotoh, Y. (1987) Signals for the selection of a splice site in pre-mRNA. Computer analysis of splice junction sequences and like sequences. J. Mol. Biol. 195, 247-259.
71. Ohta, T. (1982) Linkage disequilibrium due to random genetic drift in finite subdivided populations. Proc. Natl. Acad. Sci. USA 79, 1940-1944.
72. Parsch, J., Braverman, J. M. and Stephan, W. (2000) Comparative sequence analysis and patterns of covariation in RNA secondary structures. Genetics 154, ....
73. Parsch, J., Stephan, W. and Tanda, S. (1999) A highly conserved sequence in the 3'-untranslated region of the Drosophila Adh gene plays a functional role in Adh expression. Genetics 151, 667-674.
74. Parsch, J. (1998) Mutational analysis of conserved sequence elements within the Drosophila alcohol dehydrogenase gene. University of Maryland, Ph. D. thesis.
75. Parsch, J., Stephan, W. and Tanda, S. (1998) Long-range base pairing in Drosophila and human mRNA sequences. Mol. Biol. Evol. 15, 820-826.
76. Parsch, J., Tanda, S. and Stephan, W. (1997) Site-directed mutations reveal long-range compensatory interactions in the Adh gene of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94, 928-933.
77. Pikielny, C. W. and Rosbash, M. (1985) mRNA splicing efficiency in yeast and the contribution of nonconserved sequences. Cell 41, 119-126.
78. Reed, R. and Maniatis, T. (1986) A role for exon sequences and splice-site proximity in splice-site selection. Cell 46, 681-690.
79. Robberson, B. L., Cote, G. J. and Berget, S. M. (1990) Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol. Cell Biol. 10, 84-94.
80. Rousset, F., Pelandakis, M. and Solignac, M. (1991) Evolution of compensatory substitutions through G.U intermediate state in Drosophila rRNA. Proc. Natl. Acad. Sci. USA 88, 10032-10036.
81. Sachs, A. B., Sarnow, P. and Hentze, M. W. (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89, 831-838.
82. Salinas, J., Matassi, G., Montero, L. M. and Bernardi, G. (1988) Compositional compartmentalization and compositional patterns in the nuclear genomes of plants. Nucleic Acids Res. 16, 4269-4285.
83. Savakis, C. M., Ashburner, M. and Willis, J. H. (1986) the expression of the gene coding for alcohol dehydrogenase during the development of Drosophila melanogaster. Dev. Biol. 114, 194-207.
84. Schaeffer, S. W. and Miller, E. L. (1993) Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics 135, 541-552.
85. Seffens, W. and Digby, D. (1999) mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res, 27, 1578-1584.
86. Shapiro, M. B. and Senapathy, P. (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res. 15, 7155-7174.
87. Sharp, P. M. and Li, W.-H. (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J. Mol. Evol. 24, 28-38.
88. Sharp, P. M. and Li, W.-H. (1989) On the rate of DNA sequence evolution in Drosophila. J. Mol. Evol. 28, 398-402.
89. Sharp, P. M. and Lloyd, A. T. (1993) Codon usage. In : An Atlas of Drosophila Genes: Sequences and Molecular Features (ed. : G. Maroni), pp. 378-397, Oxford University Press, New York.
90. Shaw, G. and Kamen, R. (1986) A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659-667.
91. Smith, C. W. J., Patton, J. G. and Nadal-Ginard, B. (1989) Alternative splicing in the control of gene expression. Annu. Rev. Genet. 23, 527-577.
92. Solnick, D. and Lee, S. I. (1987) Amount of RNA secondary structure required to induce an alternative splice. Mol. Cell Biol. 7, 3194-3198.
93. Sorensen, M. A., Kurland, C. G. and Pedersen, S. (1989) Codon usage determines translation rate in Escherichia coli. J. Mol. Biol. 207, 365-377.
94. Stam, L. F. and Laurie, C. C. (1996) Molecular dissection of a major gene effect on a quantitative trait: the level of alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 144, 1559-1564.
95. Starmer, W. T. and Sullivan, D. T. (1989) A shift in the third-codon-position nucleotide frequency in alcohol dehydrogenase genes in the genus Drosophila. Mol. Biol. Evol. 6, 546-552.
96. Stephan, W. ( 1996) The rate of compensatory evolution. Genetics 144, 419-426.
97. Stephan, W. and Kirby, D.A. (1993) RNA folding in Drosophila shows a distance effect for compensatory fitness interactions. Genetics 135, 97-103.
98. Walter, A. E., Turner, D. H., Kim, J., Lyttle, M. H., Muller, P., Mathews, D. H. and Zuker, M. (1994) Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. Proc. Natl. Acad. Sci. USA 91, 9218-9222.
99. Wells, S. E., Hillner, P. E., Vale, R. D. and Sachs, A. B. (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2, 135-140.
100. Wieringa, B., Hofer, E. and Weissmann, C. (1984) A minimal intron length but no specific internal sequence is required for splicing the large rabbit beta-globin intron. Cell 37, 915-925.
101. Wieringa, B., Meyer, F., Reiser, J. and Weissmann, C. (1983) Unusual splice sites revealed by mutagenic inactivation of an authentic splice site of the rabbit beta-globin gene. Nature 301, 38-43.
102. Wright, F. (1990) The 'effective number of codons' used in a gene. Gene 87, 23-29.
103. Wright, S. (1931) Evolution in Mendelian populations. Genetics 16, 97-156.
104. Wu, J. and Manley, J. L. (1989) Mammalian pre-mRNA branch site selection by U2 snRNP involves base pairing. Genes & Dev. 3, 1553-1561.
105. Yang, A. J., Kochogan, M., Burgstaller, P., Westhof, E. and Famulok, M. (1996) Structural basis of ligand discrimination by two related RNA aptamers resolved by NMR spectroscopy. Science 272, 1343-1347.
106. Zhuang, Y. and Weiner, A. M. (1989) A compensatory base change in human U2 snRNA can suppress a branch site mutation. Genes & Dev. 3, 1545-1552.
107. Zhuang, Y. and Weiner, A. M. (1986) A compensatory base change in U1 snRNA suppresses a 5' splice site mutation. Cell 46, 827-835.
108. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule. Science 244, 48-52.
109. Zuker, M., Jaeger, J. A. and Turner, D. H. (1991) A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res. 19, 2707-2714.