Evolutionary history of exon shuffling

Abstract

Exon shuffling has been characterized as one of the major evolutionary forces shaping both the genome and the proteome of eukaryotes. This mechanism was particularly important in the creation of multidomain proteins during animal evolution, bringing a number of functional genetic novelties. Here, genome information from a variety of eukaryotic species was used to address several issues related to the evolutionary history of exon shuffling. By comparing all protein sequences within each species, we were able to characterize exon shuffling signatures throughout metazoans. Intron phase (the position of the intron regarding the codon) and exon symmetry (the pattern of flanking introns for a given exon or block of adjacent exons) were features used to evaluate exon shuffling. We confirmed previous observations that exon shuffling mediated by phase 1 introns (1-1 exon shuffling) is the predominant kind in multicellular animals. Evidence is provided that such pattern was achieved since the early steps of animal evolution, supported by a detectable presence of 1-1 shuffling units in Trichoplax adhaerens and a considerable prevalence of them in Nematostella vectensis. In contrast, Monosiga brevicollis, one of the closest relatives of metazoans, and Arabidopsis thaliana, showed no evidence of 1-1 exon or domain shuffling above what it would be expected by chance. Instead, exon shuffling events are less abundant and predominantly mediated by phase 0 introns (0-0 exon shuffling) in those non-metazoan species. Moreover, an intermediate pattern of 1-1 and 0-0 exon shuffling was observed for the placozoan T. adhaerens, a primitive animal. Finally, characterization of flanking intron phases around domain borders allowed us to identify a common set of symmetric 1-1 domains that have been shuffled throughout the metazoan lineage.

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References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  2. Aouacheria A, Cluzel C, Lethias C, Gouy M, Garrone R, Exposito JY (2004) Invertebrate data predict an early emergence of vertebrate fibrillar collagen clades and anti-incest model. J Biol Chem 279:47711–47719

    Article  CAS  PubMed  Google Scholar 

  3. Cancherini DV, França GS, de Souza SJ (2010) The role of exon shuffling in shaping protein-protein interaction networks. BMC Genomics 11(Suppl 5):S11

    Article  PubMed  Google Scholar 

  4. de Souza SJ (2003) The emergence of a synthetic theory of intron evolution. Genetica 118:117–121

    Article  PubMed  Google Scholar 

  5. de Souza SJ, Long M, Klein JR, Roy S, Lin S, Gilbert W (1998) Toward 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

    Article  PubMed  Google Scholar 

  6. Dellaporta SL, Xu A, Sagasser S, Moreno MA, Buss L, Schierwater B (2006) Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proc Natl Acad Sci USA 103:8751–8756

    Article  CAS  PubMed  Google Scholar 

  7. Eickbush TH (1999) Exon shuffling in retrospect. Science 283:1465–1467

    Article  CAS  PubMed  Google Scholar 

  8. Elrouby N, Bureau TE (2010) Bs1, a new chimeric gene formed by retrotransposon-mediated exon shuffling in maize. Plant Physiol 153:1413–1424

    Article  CAS  PubMed  Google Scholar 

  9. Fedorov A, Suboch G, Bujakov M, Fedorova L (1992) Analysis of nonuniformity in intron phase distribution. Nucleic Acids Res 20:2553–2557

    Article  CAS  PubMed  Google Scholar 

  10. Fedorov A, Cao X, Saxonov S, de Souza SJ, Roy SW, Gilbert W (2001) Intron distribution difference for 276 ancient and 131 modern genes suggests the existence of ancient introns. Proc Natl Acad Sci USA 98:13177–13182

    Article  CAS  PubMed  Google Scholar 

  11. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:281–288

    Article  Google Scholar 

  12. Gilbert W (1978) Why genes in pieces? Nature 271:501

    Article  CAS  PubMed  Google Scholar 

  13. Han J, Batey S, Nickson AA, Teichmann SA, Clarke J (2007) The folding and evolution of multidomain proteins. Nat Rev Mol Cell Biol 8:319–330

    Google Scholar 

  14. Hynes RO (2012) The evolution of metazoan extracellular matrix. J Cell Biol 196:671–679

    Article  CAS  PubMed  Google Scholar 

  15. Kaessmann H, Zöllner S, Nekrutenko A, Li WH (2002) Signatures of domain shuffling in the human genome. Genome Res 12:1642–1650

    Article  CAS  PubMed  Google Scholar 

  16. Kawashima T, Kawashima S, Tanaka C, Murai M, Yoneda M, Putnam NH, Rokhsar DS, Kanehisa M, Satoh N, Wada H (2009) Domain shuffling and the evolution of vertebrates. Genome Res 19:1393–1403

    Article  CAS  PubMed  Google Scholar 

  17. King N, Westbrook MJ, Young SL et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788

    Article  CAS  PubMed  Google Scholar 

  18. Liu M, Grigoriev A (2004) Protein domains correlate strongly with exons in multiple eukaryote genomes: evidence of exon shuffling? Trends Genet 20:399–403

    Article  PubMed  Google Scholar 

  19. Liu M, Walch H, Wu S, Grigoriev A (2005) Significant expansion of exon-bordering domains during animal proteome evolution. Nucleic Acids Res 33:95–105

    Article  CAS  PubMed  Google Scholar 

  20. Long M, Langley CH (1993) Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 293:91–95

    Article  Google Scholar 

  21. Long M, Rosenberg C, Gilbert W (1995) Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci USA 95:219–223

    Article  Google Scholar 

  22. Long M, de Souza SJ, Rosenberg C, Gilbert W (1996) Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor. Proc Natl Acad Sci USA 93:7727–7731

    Article  CAS  PubMed  Google Scholar 

  23. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002

    Article  CAS  PubMed  Google Scholar 

  24. Nguyen HD, Yoshihama M, Kenmochi N (2006) Phase distribution of spliceosomal introns: implications for intron origin. BMC Evol Biol 6:69

    Article  PubMed  Google Scholar 

  25. Patthy L (1987) Intron-dependent evolution: preferred types of exons and introns. FEBS Lett 214:1–7

    Article  CAS  PubMed  Google Scholar 

  26. Patthy L (1996) Exon shuffling and other ways of module exchange. Matrix Biol 15:301–310

    Article  CAS  PubMed  Google Scholar 

  27. Patthy L (1999) Genome evolution and the evolution of exon suffling- a review. Gene 238:103–114

    Article  CAS  PubMed  Google Scholar 

  28. Patthy L (2003) Modular assembly of genes and the evolution of new functions. Genetica 118:217–231

    Article  CAS  PubMed  Google Scholar 

  29. Putnam NH, Srivastava M, Hellsten U et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94

    Article  CAS  PubMed  Google Scholar 

  30. Qiu W, Schisler N, Stoltzfus A (2004) The evolutionary gain of spliceosomal introns: sequence and phase preferences. Mol Biol Evol 21:1252–1263

    Article  CAS  PubMed  Google Scholar 

  31. Saxonov S, Gilbert W (2003) The universe of exons revisited. Genetica 118:267–278

    Article  CAS  PubMed  Google Scholar 

  32. Smedley D, Haider S, Ballester B, Holland R, London D, Thorisson G, Kasprzyk A (2009) Biomart—biological queries made easy. BMC Genomics 10:22

    Article  PubMed  Google Scholar 

  33. Srivastava M, Begovic E, Chapman J et al (2008) The Trichoplax adhaerens genome and the nature of placozoans. Nature 454:955–960

    Article  CAS  PubMed  Google Scholar 

  34. Stajich JE, Dietrich FS, Roy SW (2007) Comparative genomic analysis of fungal genomes reveals intron-rich ancestors. Genome Biol 8:R223

    Article  PubMed  Google Scholar 

  35. Tyler S (2003) Epithelium—the primary building block for metazoan complexity. Integr Comp Biol 43:55–63

    Article  PubMed  Google Scholar 

  36. Vibranovski MD, Sakabe NJ, de Oliveira RS, de Souza SJ (2005) Signs of ancient and modern exon shuffling are correlated to the distribution of ancient and modern domains along proteins. J Mol Evol 61:341–350

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Gustavo S. França and Douglas V. Cancherini were supported by FAPESP scholarships.

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Correspondence to Sandro J. de Souza.

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França, G.S., Cancherini, D.V. & de Souza, S.J. Evolutionary history of exon shuffling. Genetica 140, 249–257 (2012). https://doi.org/10.1007/s10709-012-9676-3

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Keywords

  • Exon shuffling
  • Metazoan evolution
  • Protein domains
  • Introns