The evolution of spliceosomal introns: patterns, puzzles and progress (original) (raw)

• Cannone, J. J. et al. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. MBC Bioinformatics 3, 2 (2002).
  Google Scholar
• Bonen, L. & Vogel, J. The ins and outs of group II introns. Trends Genet. 17, 322–331 (2001).
  Article CAS PubMed Google Scholar
• Lambowitz, A. M. & Zimmerly, S. Mobile group II introns. Annu. Rev. Genet. 38, 1–35 (2004).
  Article CAS PubMed Google Scholar
• Jurica, M. S. & Moore, M. J. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell 12, 5–14 (2003).
  Article CAS PubMed Google Scholar
• Cech, T. R. The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44, 207–210. (1986).
  Article CAS PubMed Google Scholar
• Rogers, J. H. How were introns inserted into nuclear genes? Trends Genet. 5, 213–216 (1989). Two of the five current models of intron creation are proposed in this speculative piece.
  Article CAS PubMed Google Scholar
• Sharp, P. A. Five easy pieces. Science 254, 663 (1991).
  Article CAS PubMed Google Scholar
• Cavalier-Smith, T. Intron phylogeny: a new hypothesis. Trends Genet. 7, 145–148 (1991). An important statement of the idea that introns might be descended from type II introns that are transferred from early eukaryotic organelles.
  Article CAS PubMed Google Scholar
• Stoltzfus, A. On the possibility of constructive neutral evolution. J. Mol. Evol. 49, 169–181 (1999).
  Article CAS PubMed Google Scholar
• Llopart, A., Comeron, J. M., Brunet, F. G., Lachaise, D. & Long, M. Intron presence–absence polymorphism in Drosophila driven by positive Darwinian selection. Proc. Natl Acad. Sci. USA 99, 8121–8126 (2002). The sole known cases of polymorphic intron absence–presence within a species, notably in a gene with a fascinating evolutionary history.
  Article CAS PubMed PubMed Central Google Scholar
• Iwamoto, M., Maekawa, M., Saito, A., Higo, H. & Higo, K. Evolutionary relationship of plant catalase genes inferred from intron–exon structures: isozyme divergence after the separation of monocots and dicots. Theor. Appl. Genet. 97, 9–19 (1998). The first convincing case of intron gain in which the source of the intron, an inserted SINE element, is clear.
  Article CAS Google Scholar
• Iwamoto, M., Nagashima, H., Nagamine, T., Higo, H. & Higo, K. p-SINE1-like intron of the CatA catalase homologs and phylogenetic relationships among AA-genome Oryza and related species. Theor. Appl. Genet. 98, 853–861 (1999).
  Article CAS Google Scholar
• Hankeln, T., Friedl, H., Ebersberger, I., Martin, J. & Schmidt, E. R. A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain. Gene 205, 151–160 (1997).
  Article CAS PubMed Google Scholar
• Dawkins, R. The Selfish Gene (Oxford Univ. Press, 1976).
  Google Scholar
• Orgel, L. E. & Crick, F. H. Selfish DNA: the ultimate parasite. Nature 284, 604–607 (1980).
  Article CAS PubMed Google Scholar
• Doolittle, W. F. & Sapienza, C. Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601–603 (1981). Along with reference 15, this article contains early statements of the idea of genome evolution by insertion of selfish elements and differential selection on such elements between species of different complexity.
  Article Google Scholar
• Gilbert, W. The exon theory of genes. Cold Spring Harbor Symp. Quant. Biol. 52, 901–905 (1987).
  Article CAS PubMed Google Scholar
• Britten, R. J. & Davidson, E. H. Gene regulation for higher cells: a theory. Science 165, 349–357 (1969).
  Article CAS PubMed Google Scholar
• Britten, R. J. & Davidson, E. H. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q. Rev. Biol. 46, 111–138 (1971).
  Article CAS PubMed Google Scholar
• Lynch, M. Intron evolution as a population-genetic process. Proc. Natl Acad. Sci. USA 99, 6118–6123 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Lynch, M. & Conery, J. The origins of genome complexity. Science 302, 1401–1404 (2002).
  Article CAS Google Scholar
• Gilbert, W. Why genes in pieces? Nature 271, 501 (1978).
  Article CAS PubMed Google Scholar
• Doolittle, W. F. Genes in pieces – were they ever together? Nature 272, 581–582 (1978).
  Article Google Scholar
• Blake, C. C. F. Do genes in pieces imply proteins in pieces? Nature 273, 267 (1978). References 22–24 provide the backbone of the IE theory.
  Article Google Scholar
• Perler, F. et al. The evolution of genes — the chicken preproinsulin gene. Cell 20, 555–566 (1980).
  Article CAS PubMed Google Scholar
• Go, M. Correlation of DNA exonic regions with protein structural units in haemoglobin. Nature 291, 90–92 (1981).
  Article CAS PubMed Google Scholar
• Stone, E. M., Rothblum, K. N. & Schwartz, R. J. Intron-dependent evolution of chicken glyceraldehyde phosphate dehydrogenase gene. Nature 313, 498–500 (1985).
  Article CAS PubMed Google Scholar
• Straus, D. & Gilbert, W. Genetic engineering in the Precambrian: structure of the chicken triosephosphate isomerase gene. Mol. Cell Biol. 5, 3497–3506 (1985).
  Article CAS PubMed PubMed Central Google Scholar
• Long, M., Rosenberg, C. & Gilbert, W. Intron phase correlations and the evolution of the intron/exon structure of genes. Proc. Natl Acad. Sci. USA 92, 12495–12499 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• De Souza, S. J., Long, M., Schoenbach, L., Roy, S. W. & Gilbert., W. Introns correlate with module boundaries in ancient proteins. Proc. Natl Acad. Sci. USA 93, 14632–14636 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• De Souza, S. J. et al. Towards a resolution of the introns early/late debate: only phase zero introns are correlated with the structure of ancient proteins. Proc. Natl Acad. Sci. USA 95, 5094–5099 (1998). An important early statement of the 'synthetic' or 'mixed' variant of the IE theory.
  Article CAS PubMed PubMed Central Google Scholar
• Roy, S. W., Nosaka, M., de Souza, S. J. & Gilbert, W. Centripetal modules and ancient introns. Gene 238, 85–91 (1999).
  Article CAS PubMed Google Scholar
• Fedorov, A. et al. Intron distribution difference for 276 ancient and 131 modern genes suggests the existence of ancient introns. Proc. Natl Acad. Sci. USA 98, 13177–13182 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Roy, S. W., Lewis, B. P., Fedorov, A. & Gilbert, W. Footprints of primordial introns on the eukaryotic genome. Trends Genet. 17, 496–498 (2001).
  Article CAS PubMed Google Scholar
• Fedorov, A., Roy, S., Cao, X. & Gilbert, W. Phylogenetically older introns strongly correlate with module boundaries in ancient proteins. Genome Res. 13, 1155–1157 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Roy, S. W., Fedorov, A. & Gilbert, W. The signal of ancient introns is obscured by intron density and homolog number. Proc. Natl Acad. Sci. USA 99, 15513–15517 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• De Souza, S. J. The emergence of a synthetic theory of intron evolution. Genetica 118, 117–121 (2003).
  Article CAS PubMed Google Scholar
• Roy, S. W. Recent evidence for the exon theory of genes. Genetica 118, 251–266 (2003).
  Article CAS PubMed Google Scholar
• Patthy, L. Genome evolution and the evolution of exon-shuffling — a review. Gene 238, 103–114 (1999). A comprehensive review of the known cases of exon shuffling.
  Article CAS PubMed Google Scholar
• Patthy, L. Modular assembly of genes and the evolution of new functions. Genetica 118, 217–231 (2003).
  Article CAS PubMed Google Scholar
• Tonegawa, S., Maxam, A. M., Tizard, R., Bernard, O. & Gilbert, W. Sequence of a mouse germ-line gene for a variable region of an immunoglobulin light chain. Proc. Natl Acad. Sci. USA 75, 1485–1489 (1978).
  Article CAS PubMed PubMed Central Google Scholar
• Comeron, J. M. & Kreitman, M. The correlation between intron length and recombination in Drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156, 1175–1190 (2000).
  CAS PubMed PubMed Central Google Scholar
• Duret, L. Why do genes have introns? Recombination might add a new piece to the puzzle. Trends Genet. 17, 172–175 (2001).
  Article CAS PubMed Google Scholar
• Lynch, M. & Kewalramani, A. Messenger RNA surveillance and the evolutionary proliferation of introns. Mol. Biol. Evol. 20, 563–571 (2003).
  Article CAS PubMed Google Scholar
• Cavalier-Smith, T. Selfish DNA and the origin of introns. Nature 315, 283–284 (1985). An important early statement of the IL hypothesis.
  Article CAS PubMed Google Scholar
• Sharp, P. A. On the origin of RNA splicing and introns. Cell 42, 397–400 (1985).
  Article CAS PubMed Google Scholar
• Dibb, N. J. & Newman, A. J. Evidence that introns arose at proto-splice sites. EMBO J. 8, 2015–2021 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Palmer, J. D. & Logsdon, J. M. Jr. The recent origin of introns. Curr. Opin. Genet. Dev. 1, 470–477 (1991).
  Article CAS PubMed Google Scholar
• Stoltzfus, A., Spencer, D. F., Zuker, M., Logsdon, J. M. Jr & Doolittle, W. F. Testing the exon theory of genes: the evidence from protein structure. Science 265, 202–207 (1994).
  Article CAS PubMed Google Scholar
• Stoltzfus, A. Origin of introns — early or late? Nature 369, 526–527 (1994).
  Article CAS PubMed Google Scholar
• Logsdon, J. M. Jr et al. Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. Proc. Natl Acad. Sci. USA 92, 8507–8511 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Kwaitowski, J., Krawczyk, M., Kornacki, M., Bailey, K. & Ayala, F. J. Evidence against the exon theory of genes derived from the triose-phosphate isomerase gene. Proc. Natl Acad. Sci. USA 92, 8503–8506 (1995).
  Article Google Scholar
• Cho, G. & Doolittle, R. F. Intron distribution in ancient paralogs supports random insertion and not random loss. J. Mol. Evol. 44, 573–584 (1997).
  Article CAS PubMed Google Scholar
• Rzhetsky, A., Ayala, F. J., Hsu, L. C., Chang, C. & Yoshida, A. Exon/intron structure of aldehyde dehydrogenase genes supports the 'introns-late' theory. Proc. Natl Acad. Sci. USA 94, 6820–6825 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Logsdon, J. M. Jr. The recent origins of spliceosomal introns revisited. Curr. Opin. Genet. Dev. 8, 637–648 (1998).
  Article CAS PubMed Google Scholar
• Logsdon, J. M. Jr, Stoltzfus, A. & Doolittle, W. F. Molecular evolution: recent cases of spliceosomal intron gain? Curr. Biol. 8, R560–R563 (1998).
  Article CAS PubMed Google Scholar
• Fedoro v, A. F., Merican, A. F. & Gilbert, W. Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc. Natl Acad. Sci. USA 99, 16128–16133 (2002).
  Article CAS Google Scholar
• Rogozin, I. B., Wolf, Y. I., Sorokin, A. V., Mirkin, B. G. & Koonin, E. V. Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr. Biol. 13, 1512–1517 (2003).
  Article CAS PubMed Google Scholar
• Tarrio, R., Rodriguez-Trelles, F. & Ayala, F. J. A new Drosophila spliceosomal intron position is common in plants. Proc. Natl Acad. Sci. USA 100, 6580–6583 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Dibb, N. J. Proto-splice site model of intron origin. J. Theor. Biol. 151, 405–416 (1991).
  Article CAS PubMed Google Scholar
• Paquette, S. M., Bak, S & Feyereisen, R. Intron–exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. DNA Cell Biol. 19, 307–317 (2000).
  Article CAS PubMed Google Scholar
• Sverdlov, A. V., Rogozin, I. B., Babenko, V. N. & Koonin, E. V. Reconstruction of ancestral protosplice sites. Curr. Biol. 14, 1505–1508 (2004).
  Article CAS PubMed Google Scholar
• Coghlan, A. & Wolfe, K. H. Origins of recently gained introns in Caenorhabditis. Proc. Natl Acad. Sci. USA 101, 11362–11367 (2004). The first sequence analysis of a large number of putative recently gained introns. The results are interpreted by the authors as evidence for intron transposition, although the answer might not be so straightforward.
  Article CAS PubMed PubMed Central Google Scholar
• Qiu, W. G., Schisler, N. & Stoltzfus, A. The evolutionary gain of spliceosomal introns: sequence and phase preferences. Mol. Biol. Evol. 21, 1252–1263 (2004).
  Article CAS PubMed Google Scholar
• Tordai, H. & Patthy, L. Insertion of spliceosomal introns in proto-splice sites: the case of secretory signal peptides. FEBS Lett. 575, 109–111 (2004).
  Article CAS PubMed Google Scholar
• Sadusky, T., Newman, A. J. & Dibb, N. J. Exon junction sequences as cryptic splice sites: implications for intron origin. Curr. Biol. 14, 505–509 (2004).
  CAS PubMed Google Scholar
• Stoltzfus, A. Molecular evolution: introns fall into place. Curr. Biol. 14, R351–352 (2004).
  Article CAS PubMed Google Scholar
• Sverdlov, A. V., Rogozin, I. B., Babenko, V. N. & Koonin, E. V. Conservation versus parallel gains in intron evolution. Nucleic Acids Res. 33, 1741–1748 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Roy, S. W. & Gilbert, W. Complex early genes. Proc. Natl Acad. Sci. USA 102, 1986–1991 (2005). The reanalysis of data from reference 58, which indicates that intron loss, not gain, has dominated intron evolution.
  Article CAS PubMed PubMed Central Google Scholar
• Rogozin, I. B., Sverdlov, A. V., Babenko, V. N. & Koovin, E. V. Analysis of evolution of exon–intron structure in eukaryotic genes. Brief Bioinform. 6, 118–134.
• Roy, S. W., Fedorov, A. & Gilbert, W. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc. Natl Acad. Sci. USA 100, 7158–7162 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Cho, S., Jin, S. W., Cohen, A. & Ellis, R. E. A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res. 14, 1207–1220 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Kiontke, K. et al. Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc. Natl Acad. Sci. USA 101, 9003–9008 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Robertson, H. M. Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. Genome Res. 8, 449–463 (1998).
  Article CAS PubMed Google Scholar
• Wolf, Y. I., Kondrashov, F. A. & Koonin, E. V. Footprints of primordial introns on the eukaryotic genome: still no clear traces. Trends Genet. 17, 499–501 (2001).
  Article CAS PubMed Google Scholar
• Seo, H. C. et al. Miniature genome in the marine chordate Oikopleura dioica. Science 294, 2506 (2001).
  Article CAS PubMed Google Scholar
• Edvardsen, R. B. et al. Hypervariable and highly divergent intron–exon organizations in the chordate Oikopleura dioica. J. Mol. Evol. 59, 448–457 (2004).
  Article CAS PubMed Google Scholar
• Babenko, V. N., Rogozin, I. B., Mekhedov, S. L. & Koonin, E. V. Prevalence of intron gain over intron loss in the evolution of paralogous gene families. Nucleic Acids Res. 32, 3724–3733 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Embley, T. M. & Hirt, R. P. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 624–629 (1998).
  Article CAS PubMed Google Scholar
• Simpson, A. G. & Roger, A. J. Eukaryotic evolution: getting to the root of the problem. Curr. Biol. 12, R691–R693 (2002).
  Article CAS PubMed Google Scholar
• Sogin, M. L. Early evolution and the origin of eukaryotes. Curr. Opin. Genet. Dev. 1, 457–463 (1991).
  Article CAS PubMed Google Scholar
• Hashimoto, T. & Hasegawa, M. Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1α/Tu and 2/G. Adv. Biophys. 32, 73–120 (1996).
  Article CAS PubMed Google Scholar
• Stiller, J. W., Duffield, E. C. & Hall, B. D. Amitochondriate amoebae and the evolution of DNA-dependent RNA polymerase II. Proc. Natl Acad. Sci. USA 95, 11769–11774 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Biderre, C., Metenier, G. & Vivares, C. P. A small spliceosomal-type intron occurs in a ribosomal protein gene of the microsporidian Encephalitozoon cuniculi. Mol. Biochem. Parasitol. 94, 283–286 (1998).
  Article CAS PubMed Google Scholar
• Fast, N. M., Roger, A. J., Richardson, C. A. & Doolittle, W. F. U2 and U6 snRNA genes in the microsporidian Nosema locustae: evidence for a functional spliceosome. Nucleic Acids Res. 26, 3202–3207 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Fast, N. M. & Doolittle, W. F. Trichomonas vaginalis possesses a gene encoding the essential spliceosomal component, PRP8. Mol. Biochem. Parasitol. 99, 275–278 (1999).
  Article CAS PubMed Google Scholar
• Breckenridge, D. G, Watanabe, Y., Greenwood, S. J., Gray, M. W. & Schnare, M. N. U1 small nuclear RNA and spliceosomal introns in Euglena gracilis. Proc. Natl Acad. Sci. USA 96, 852–856 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Ismaili, N. et al. Characterization of a SR protein from Trypanosoma brucei with homology to RNA-binding _cis_-splicing proteins. Mol. Biochem. Parasitol. 102, 103–105 (1999).
  Article CAS PubMed Google Scholar
• Schnare, M. N. & Gray, M. W. Structural conservation and variation among U5 small nuclear RNAs from trypanosomatid protozoa. Biochim. Biophys. Acta. 1490, 362–366 (2000).
  Article CAS PubMed Google Scholar
• Dacks, J. B. & Doolittle, W. F. Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help. Cell 107, 419–425 (2001).
  Article CAS PubMed Google Scholar
• Edgcomb, V. P., Roger, A. J., Simpson, A. G., Kysela, D. T. & Sogin, M. L. Evolutionary relationships among 'jakobid' flagellates as indicated by α- and β-tubulin phylogenies. Mol. Biol. Evol. 18, 514–522 (2001).
  Article CAS PubMed Google Scholar
• Archibald, J. M., O'Kelly, C. J. & Doolittle, W. F. The chaperonin genes of jakobid and jakobid-like flagellates: implications for eukaryotic evolution. Mol. Biol. Evol. 19, 422–431 (2002).
  Article CAS PubMed Google Scholar
• Nixon, J. E. et al. A spliceosomal intron in Giardia lamblia. Proc. Natl Acad. Sci. USA 99, 3701–3705 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Simpson, A. G., MacQuarrie, E. K & Roger, A. J. Eukaryotic evolution: early origin of canonical introns. Nature 419, 270 (2002).
  Article CAS PubMed Google Scholar
• Collins, L. & Penny, D. Complex spliceosomal organization ancestral to extant eukaryotes. Mol. Biol. Evol. 22, 1053–1066 (2005). A demonstration of the presence of a sophisticated spliceosome in the common ancestor of all extant eukaryotes.
  Article CAS PubMed Google Scholar
• Vanacova, S., Yan, W., Carlton, J. M. & Johnson, P. J. Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 102, 4430–4435 (2005).
  Article CAS PubMed Google Scholar
• Anantharaman, V., Koonin, E. V. & Aravind, L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids. Res. 30, 1427–1464 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Ruvinsky, A., Eskesen, S. T., Eskesen, F. N. & Hurst, L. D. Can codon usage bias explain intron phase distributions and exon symmetry? J. Mol. Evol. 60, 99–104 (2005).
  Article CAS PubMed Google Scholar
• Long, M., de Souza, S. J., Rosenberg, C. & Gilbert, W. Relationship between 'proto-splice sites' and intron phases: evidence from dicodon analysis. Proc. Natl Acad. Sci. USA 95, 219–223 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Long, M. & Rosenberg, C. Testing the 'proto-splice sites' model of intron origin: evidence from analysis of intron phase correlations. Mol. Biol. Evol. 17, 1789–1796 (2000).
  Article CAS PubMed Google Scholar
• Bernstein, L. B., Mount, S. M. & Weiner, A. M. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell 32, 461–472 (1983).
  Article CAS PubMed Google Scholar
• Lewin, R. How mammalian RNA returns to its genome. Science 219, 1052–1054 (1983).
  Article CAS PubMed Google Scholar
• Weiner, A. M., Deininger, P. L. & Efstratiadis, A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu. Rev. Biochem. 55, 631–661 (1986).
  Article CAS PubMed Google Scholar
• Fink, G. R. Pseudogenes in yeast? Cell 49, 5–6 (1987).
  Article CAS PubMed Google Scholar
• Long, M. & Langley, C. H. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 260, 91–95 (1993).
  CAS PubMed Google Scholar
• Derr, L. K. The involvement of cellular recombination and repair genes in RNA-mediated recombination in Saccharomyces cerevisiae. Genetics 148, 937–945 (1998).
  CAS PubMed PubMed Central Google Scholar
• Kent, W. J. & Zahler, A. M. Conservation, regulation, synteny, and introns in a large-scale C. briggsae–C. elegans genomic alignment. Genome Res. 10, 1115–1125 (2000).
  Article CAS PubMed Google Scholar
• Fedorova, L. & Fedorov, A. Introns in gene evolution. Genetica 118, 123–131 (2003).
  Article CAS PubMed Google Scholar
• Nielsen, C. B., Friedman, B., Birren, B., Burge, C. B. & Galagan, J. E. Patterns of intron gain and loss in fungi. PLoS Biol. 2, e422 (2004).
  Article PubMed PubMed Central CAS Google Scholar
• Banyai, L. & Patthy, L. Evidence that human genes of modular proteins have retained significantly more ancestral introns than their fly or worm orthologues. FEBS Lett. 565, 127–132 (2004).
  Article CAS PubMed Google Scholar
• Sakurai, A. et al. On biased distribution of introns in various eukaryotes. Gene 300, 89–95 (2002).
  Article CAS PubMed Google Scholar
• Mourier, T. & Jeffares, D. C. Eukaryotic intron loss. Science 300, 1393 (2003).
  Article CAS PubMed Google Scholar
• Frugoli, J. A., McPeek, M. A., Thomas, T. L. & McClung, C. R. Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics 149, 355–365 (1998).
  CAS PubMed PubMed Central Google Scholar
• Wada, H. et al. Dynamic insertion-deletion of introns in deuterostome EF-1a genes. J. Mol. Evol. 54, 118–128 (2002).
  Article CAS PubMed Google Scholar
• Sverdlov, A. V., Babenko, V. N., Rogozin, I. B. & Koonin, E. V. Preferential loss and gain of introns in 3′ portions of genes suggests a reverse-transcription mechanism of intron loss. Gene 338, 85–91 (2004).
  Article CAS PubMed Google Scholar
• Roy, S. W. & Gilbert, W. The pattern of intron loss. Proc. Natl Acad. Sci. USA 102, 713–718 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Crick, F. H. Chromosome structure and function — future prospects. Eur. J. Biochem. 83, 1–3 (1978).
  Article CAS PubMed Google Scholar
• Crick, F. Split genes and RNA splicing. Science 204, 264–271 (1979).
  Article CAS PubMed Google Scholar
• Tsujimoto, Y. & Suzuki, Y. The DNA sequence of Bombyx-mori fibroin gene including the 5′ flanking, mRNA coding, entire intervening and fibroin protein coding regions. Cell 18, 591–600 (1979).
  Article CAS PubMed Google Scholar
• Giroux, M. J. et al. De novo synthesis of an intron by the maize transposable element Dissociation. Proc. Natl Acad. Sci. USA 91, 12150–12154 (1994). The authors show that a transposable element inserted into the Sh2 gene of maize is sometimes exactly spliced out of transcripts, supporting the idea that transposable element insertions could give rise to new introns in some cases.
  Article CAS PubMed PubMed Central Google Scholar
• Rogers, J. H. The role of introns in evolution. FEBS Lett. 268, 339–343 (1990).
  Article CAS PubMed Google Scholar
• Roy, S. W. The origin of recent introns: transposons? Genome Biol. 5, 251 (2004).
  Article PubMed PubMed Central Google Scholar
• Roy, S. W. & Gilbert, W. Rates of intron loss and gain: implications for early eukaryotic evolution. Proc. Natl Acad. Sci. USA 102, 5773–5778 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Guiliano, D. B. et al. Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes. Genome Biol. 3, research 0057 (2002).
  Article Google Scholar
• Gao, L. Z. & Innan, H. Very low gene duplication rate in the yeast genome. Science 306, 1367–1370 (2004).
  Article CAS PubMed Google Scholar
• Krzywinski, J. & Besansky, N. J. Frequent intron loss in the white gene: a cautionary tale for phylogeneticists. Mol. Biol. Evol. 19, 362–366 (2002).
  Article CAS PubMed Google Scholar
• Hentze, M. W. & Kulozik, A. E. A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96, 307–310 (1999).
  Article CAS PubMed Google Scholar
• Ast, G. How did alternative splicing evolve? Nature Rev. Genet. 5, 773–782 (2004).
  Article CAS PubMed Google Scholar
• Castillo-Davis, C. I., Mekhedov, S. L., Hartl, D. L., Koonin, E. V. & Kondrashov, F. A. Selection for short introns in highly expressed genes. Nature Genet. 31, 415–418 (2002).
  Article CAS PubMed Google Scholar
• Ometto, L., Stephan, W. & De Lorenzo, D. Insertion/deletion and nucleotide polymorphism data reveal constraints in Drosophila melanogaster introns and intergenic regions. Genetics 169, 1521–1527 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Prachumwat, A., DeVincentis, L. & Palopoli, M. F. Intron size correlates positively with recombination rate in Caenorhabditis elegans. Genetics 166, 1585–1590 (2004).
  Article CAS PubMed PubMed Central Google Scholar