The effect of intron length on exon creation ratios during the evolution of mammalian genomes

RNA

Volumn 14, Issue 11, 2008, Pages 2261-2273

  Roy, Meenakshi ^a   Kim, Namshin ^a,c   Xing, Yi ^b   Lee, Christopher ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Alternative splicing; Evolution; Exon creation; Inclusion level; Intron length

Indexed keywords

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; EXON; GENOME ANALYSIS; HUMAN; INTRON; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; RNA SPLICING;

ALTERNATIVE SPLICING; ANIMALS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EXONS; EXPRESSED SEQUENCE TAGS; GENOME, HUMAN; HUMANS; INTRONS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; RNA SPLICE SITES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

MAMMALIA; PRIMATES;

EID: 55549118939     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1024908     Document Type: Article

References (56)

1. Alekseyenko, A., Kim, N., and Lee, C. 2007. Global analysis of exon creation vs. loss, and the role of alternative splicing, in 17 vertebrate genomes. RNA 13: 661-670.
2. Artamonova, I.I. and Gelfand, M.S. 2004. Evolution of the exon-intron structure and alternative splicing of the MAGE-A family of cancer/testis antigens. J. Mol. Evol. 59: 620-631.
3. Ast, G. 2004. How did alternative splicing evolve? Nat. Rev. Genet. 5: 773-782.
4. Baek, D. and Green, P. 2005. Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc. Natl. Acad. Sci. 102: 12813-12818.
5. Berget, S.M. 1995. Exon recognition in vertebrate splicing. J. Biol. Chem. 270: 2411-2414.
6. Black, D.L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72: 291-336.
7. Boue, S., Letunic, I., and Bork, P. 2003. Alternative splicing and evolution. BioEssays 25: 1031-1034.
8. Chamary, J.V. and Hurst, L.D. 2004. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: Evidence for selectively driven codon usage. Mol. Biol. Evol. 21: 1014-1023.
9. Cusack, B.P. and Wolfe, K.H. 2005. Changes in alternative splicing of human and mouse genes are accompanied by faster evolution of constitutive exons. Mol. Biol. Evol. 22: 2198-2208.
10. Deutsch, M. and Long, M. 1999. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 27: 3219-3228.
11. Dewey, C.N., Rogozin, I.B., and Koonin, E.V. 2006. Compensatory relationship between splice sites and exonic splicing signals depending on the length of vertebrate introns. BMC Genomics 7: 311. doi: 10.1186/1471-2164-7-311.
12. Duret, L., Mouchiroud, D., and Gautier, C. 1995. Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J. Mol. Evol. 40: 308-317.
13. Eng, L., Coutinho, G., Nahas, S., Yeo, G., Tanouye, R., Babaei, M., Dork, T., Burge, C., and Gatti, R.A. 2004. Nonclassical splicing mutations in the coding and noncoding regions of the ATM gene: Maximum entropy estimates of splice junction strengths. Hum. Mutat. 23: 67-76.
14. Fox-Walsh, K.L., Dou, Y., Lam, B.J., Hung, S.P., Baldi, P.F., and Hertel, K.J. 2005. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc. Natl. Acad. Sci. 102: 16176-16181.
15. Gazave, E., Marques-Bonet, T., Fernando, O., Charlesworth, B., and Navarro, A. 2007. Patterns and rates of intron divergence between humans and chimpanzees. Genome Biol. 8: R21. doi: 10.1186/gb-2007-8-2-r21.
16. Haddrill, P.R., Charlesworth, B., Halligan, D.L., and Andolfatto, P. 2005. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol. 6: R67. doi: 10.1186/gb-2005-6-8-r67.
17. Hsieh, S.J., Lin, C.Y., Liu, N.H., Chow, W.Y., and Tang, C.Y. 2006. GeneAlign: A coding exon prediction tool based on phylogenetical comparisons. Nucleic Acids Res. 34: W280-W284.
18. Irimia, M., Rukov, J.L., Penny, D., Garcia-Fernandez, J., Vinther, J., and Roy, S.W. 2007a. Widespread evolutionary conservation of alternatively spliced exons in Caenorhabditis. Mol. Biol. Evol. 25: 375-382.
19. Irimia, M., Rukov, J.L., Penny, D., and Roy, S.W. 2007b. Functional and evolutionary analysis of alternatively spliced genes is consistent with an early eukaryotic origin of alternative splicing. BMC Evol. Biol. 7: 188. doi: 10.1186/1471-2148-7-188.
20. Itoh, H., Washio, T., and Tomita, M. 2004. Computational comparative analyses of alternative splicing regulation using full-length cDNA of various eukaryotes. RNA 10: 1005-1018.
21. Jones, E., Oliphant, T., and Peterson, P. 2001. Scipy: Open source scientific tools for Python. http://www.scipy.org/.
22. Kaufmann, D., Kenner, O., Nurnberg, P., Vogel, W., and Bartelt, B. 2004. In NF1, CFTR, PER3, CARS and SYT7, alternatively included exons show higher conservation of surrounding intron sequences than constitutive exons. Eur. J. Hum. Genet. 12: 139-149.
23. Kim, N., Alekseyenko, A., Roy, M., and Lee, C. 2007a. The ASAP II database: Analysis and comparative genomics of alternative splicing in 15 animal species. Nucleic Acids Res. 35: D93-D98.
24. Kim, E., Magen, A., and Ast, G. 2007b. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res. 35: 125-131.
25. Kondrashov, F.A., Ogurtsov, A.Y., and Kondrashov, A.S. 2006. Selection in favor of nucleotides G and C diversifies evolution rates and levels of polymorphism at mammalian synonymous sites. J. Theor. Biol. 240: 616-626.
26. Kuhn, R.M., Karolchik, D., Zweig, A.S., Trumbower, H., Thomas, D.J., Thakkapallayil, A., Sugnet, C.W., Stanke, M., Smith, K.E., Siepel, A., et al. 2007. The UCSC genome browser database: Update 2007. Nucleic Acids Res. 35: D668-D673.
27. Lareau, L.F., Green, R.E., Bhatnagar, R.S., and Brenner, S.E. 2004. The evolving roles of alternative splicing. Curr. Opin. Struct. Biol. 14: 273-282.
28. Lev-Maor, G., Sorek, R., Shomron, N., and Ast, G. 2003. The birth of an alternatively spliced exon: 39 splice-site selection in Alu exons. Science 300: 1288-1291.
29. Lev-Maor, G., Goren, A., Sela, N., Kim, E., Keren, H., Doron-Faigenboim, A., Leibman-Barak, S., Pupko, T., and Ast, G. 2007. The "alternative" choice of constitutive exons throughout evolution. PLoS Genet. 3: e203. doi: 10.1371/journal.pgen.0030203.
30. Malko, D.B., Makeev, V.J., Mironov, A.A., and Gelfand, M.S. 2006. Evolution of exon-intron structure and alternative splicing in fruit flies and malarial mosquito genomes. Genome Res. 16: 505-509.
31. Marais, G., Nouvellet, P., Keightley, P.D., and Charlesworth, B. 2005. Intron size and exon evolution in Drosophila. Genetics 170: 481-485.
32. Modrek, B. and Lee, C. 2003. Alternative splicing in the human, mouse and rat genomes is associated with an increased rate of exon creation/loss. Nat. Genet. 34: 177-180.
33. Moriyama, E.N., Petrov, D.A., and Hartl, D.L. 1998. Genome size and intron size in Drosophila. Mol. Biol. Evol. 15: 770-773.
34. Nurtdinov, R.N., Neverov, A.D., Favorov, A.V., Mironov, A.A., and Gelfand, M.S. 2007. Conserved and species-specific alternative splicing in mammalian genomes. BMC Evol. Biol. 7: 249. doi: 10.1186/1471-2148-7-249.
35. Ovcharenko, I., Boffelli, D., and Loots, G.G. 2004. eShadow: A tool for comparing closely related sequences. Genome Res. 14: 1191-1198.
36. Pan, Q., Shai, O., Misquitta, C., Zhang, W., Saltzman, A.L., Mohammad, N., Babak, T., Siu, H., Hughes, T.R., Morris, Q.D., et al. 2004. Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Mol. Cell 16: 929-941.
37. Pan, Q., Saltzman, A.L., Kim, Y.K., Misquitta, C., Shai, O., Maquat, L.E., Frey, B.J., and Blencowe, B.J. 2006. Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes & Dev. 20: 153-158.
38. Plass, M. and Eyras, E. 2006. Differentiated evolutionary rates in alternative exons and the implications for splicing regulation. BMC Evol. Biol. 6: 50. doi: 10.1186/1471-2148-6-50.
39. Resch, A., Xing, Y., Alekseyenko, A., Modrek, B., and Lee, C. 2004. Evidence for a sub-population of conserved alternative splicing events under selection pressure for protein reading frame preservation. Nucleic Acids Res. 32: 1261-1269.
40. Romfo, C.M., Alvarez, C.J., van Heeckeren, W.J., Webb, C.J., and Wise, J.A. 2000. Evidence for splice site pairing via intron definition in Schizosaccharomyces pombe. Mol. Cell. Biol. 20: 7955-7970.
41. Singer, S.S., Mannel, D.N., Hehlgans, T., Brosius, J., and Schmitz, J. 2004. From "junk" to gene: Curriculum vitae of a primate receptor isoform gene. J. Mol. Biol. 341: 883-886.
42. Sorek, R. 2007. The birth of new exons: Mechanisms and evolutionary consequences. RNA 13: 1603-1608.
43. Sorek, R. and Ast, G. 2003. Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res. 13: 1631-1637.
44. Sorek, R., Ast, G., and Graur, D. 2002. Alu-containing exons are alternatively spliced. Genome Res. 12: 1060-1067.
45. Sorek, R., Shemesh, R., Cohen, Y., Basechess, O., Ast, G., and Shamir, R. 2004. A non-EST-based method for exon-skipping prediction. Genome Res. 14: 1617-1623.
46. Sterner, D.A., Carlo, T., and Berget, S.M. 1996. Architectural limits on split genes. Proc. Natl. Acad. Sci. 93: 15081-15085.
47. Sugnet, C.W., Srinivasan, K., Clark, T.A., O'Brien, G., Cline, M.S., Wang, H., Williams, A., Kulp, D., Blume, J.E., Haussler, D., et al. 2006. Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput. Biol. 2: e4. doi: 10.1371/journal.pcbi. 0020004.
48. Talerico, M. and Berget, S.M. 1994. Intron definition in splicing of small Drosophila introns. Mol. Cell. Biol. 14: 3434-3445.
49. Wang, W., Zheng, H., Yang, S., Yu, H., Li, J., Jiang, H., Su, J., Yang, L., Zhang, J., McDermott, J., et al. 2005. Origin and evolution of new exons in rodents. Genome Res. 15: 1258-1264.
50. Wang, Z., Xinshu, X., Nostrand, E.V., and Burge, C. 2006. General and specific functions of exonic splicing silencers in splicing control. Mol. Cell 23: 61-70.
51. Xing, Y. and Lee, C. 2005. Evidence of functional selection pressure for alternative splicing events that accelerate evolution of protein subsequences. Proc. Natl. Acad. Sci. 102: 13526-13531.
52. Xing, Y. and Lee, C. 2006. Alternative splicing and RNA selection pressure - Evolutionary consequences for eukaryotic genomes. Nat. Rev. Genet. 7: 499-509.
53. Xing, Y., Wang, Q., and Lee, C. 2006. Evolutionary divergence of exon flanks: A dissection ofmutability and selection. Genetics 173: 1787-1791.
54. Xu, Q., Modrek, B., and Lee, C. 2002. Genome-wide detection of tissue-specific alternative splicing in the human transcriptome. Nucleic Acids Res. 30: 3754-3766.
55. Yeo, G. and Burge, C. 2004. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol. 11: 377-394.
56. Zheng, C.L., Fu, X.D., and Gribskov, M. 2005. Characteristics and regulatory elements defining constitutive splicing and different modes of alternative splicing in human and mouse. RNA 11: 1777-1787.