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Journal of Molecular Evolution

, Volume 59, Issue 4, pp 448–457 | Cite as

Hypervariable and Highly Divergent Intron–Exon Organizations in the Chordate Oikopleura dioica

  • Rolf B. Edvardsen
  • Emmanuelle Lerat
  • Anne Dorthea Maeland
  • Mette Flåt
  • Rita Tewari
  • Marit F. Jensen
  • Hans Lehrach
  • Richard Reinhardt
  • Hee-Chan Seo
  • Daniel ChourroutEmail author
Article

Abstract

Oikopleura dioica is a pelagic tunicate with a very small genome and a very short life cycle. In order to investigate the intron–exon organizations in Oikopleura, we have isolated and characterized ribosomal protein EF-1α, Hox, and α-tubulin genes. Their intron positions have been compared with those of the same genes from various invertebrates and vertebrates, including four species with entirely sequenced genomes. Oikopleura genes, like Caenorhabditis genes, have introns at a large number of nonconserved positions, which must originate from late insertions or intron sliding of ancient insertions. Both species exhibit hypervariable intron–exon organization within their α-tubulin gene family. This is due to localization of most nonconserved intron positions in single members of this gene family. The hypervariability and divergence of intron positions in Oikopleura and Caenorhabditis may be related to the predominance of short introns, the processing of which is not very dependent upon the exonic environment compared to large introns. Also, both species have an undermethylated genome, and the control of methylation-induced point mutations imposes a control on exon size, at least in vertebrate genes. That introns placed at such variable positions in Oikopleura or C. elegans may serve a specific purpose is not easy to infer from our current knowledge and hypotheses on intron functions. We propose that new introns are retained in species with very short life cycles, because illegitimate exchanges including gene conversion are repressed. We also speculate that introns placed at gene-specific positions may contribute to suppressing these exchanges and thereby favor their own persistence.

Keywords

Intron Conversion α-Tubulin Hox Ribosomal protein Urochordate Oikopleura 

Notes

Acknowledgments

André Adoutte has contributed important advice throughout the course of this work. We also thank David Liberles for suggestions on the phylogenetic analysis. We thank the personnel of the UoB/Sars sequencing facility and the Sars Centre Oikopleura culture facility for their continued assistance.

References

  1. Archibald, JM, O’Kelly, CJ, Doolittle, WF 2002The chaperonin genes of jakobid and jakobid-like flagellates: Implications for eukaryotic evolutionMol Biol Evol19422431PubMedGoogle Scholar
  2. Berget, SM 1995Exon recognition in vertebrate splicingJ Biol Chem27024112414PubMedGoogle Scholar
  3. Blencowe, BJ 2000Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseasesTrends Biochem Sci25106110CrossRefPubMedGoogle Scholar
  4. Cavalier-Smith, T 1991Intron phylogeny: A new hypothesisTrends Genet7145148PubMedGoogle Scholar
  5. Coghlan, A, Wolfe, KH 2002Fourfold faster rate of genome rearrangement in nematodes than in DrosophilaGenome Res12857867CrossRefPubMedGoogle Scholar
  6. Dehal, P, Satou, Y, Campbell, RK, Chapman, J, Degnan, B, Tomaso, A, Davidson, B, Di Gregorio, A, Gelpke, M, Goodstein, DM, Harafuji, N, Hastings, KE, Ho, I, Hotta, K, Huang, W, Kawashima, T, Lemaire, P, Martinez, D, Meinertzhagen, IA, Necula, S, Nonaka, M, Putnam, N, Rash, S, Saiga, H, Satake, M, Terry, A, Yamada, L, Wang, HG, Awazu, S, Azumi, K, Boore, J, Branno, M, Chin-Bow, S, DeSantis, R, Doyle, S, Francino, P, Keys, DN, Haga, S, Hayashi, H, Hino, K, Imai, KS, Inaba, K, Kano, S, Kobayashi, K, Kobayashi, M, Lee, BI, Makabe, KW, Manohar, C, Matassi, G, Medina, M, Mochizuki, Y, Mount, S, Morishita, T, Miura, S, Nakayama, A, Nishizaka, S, Nomoto, H, Ohta, F, Oishi, K, Rigoutsos, I, Sano, M, Sasaki, A, Sasakura, Y, Shoguchi, E, Shin-i, T, Spagnuolo, A, Stainier, D, Suzuki, MM, Tassy, O, Takatori, N, Tokuoka, M, Yagi, K, Yoshizaki, F, Wada, S, Zhang, C, Hyatt, PD, Larimer, F, Detter, C, Doggett, N, Glavina, T, Hawkins, T, Richardson, P, Lucas, S, Kohara, Y, Levine, M, Satoh, N, Rokhsar, DS 2002The draft genome of Ciona intestinalis: insights into chordate and vertebrate originsScience29821572167CrossRefPubMedGoogle Scholar
  7. Souza, SJ, Long, M, Schoenbach, L, Roy, SW, Gilbert, W 1996Intron positions correlate with module boundaries in ancient proteinsProc Natl Acad Sci USA931463214636CrossRefPubMedGoogle Scholar
  8. Drouin, G 2002Characterization of the gene conversions between the multigene family members of the yeast genomeJ Mol Evol551423CrossRefPubMedGoogle Scholar
  9. Duret, L 2001Why do genes have introns? Recombination might add a new piece to the puzzleTrends Genet17172175CrossRefPubMedGoogle Scholar
  10. Duret, L, Bucher, P 1997Searching for regulatory elements in human noncoding sequencesCurr Opin Struct Biol7399406CrossRefPubMedGoogle Scholar
  11. Galtier, N, Gouy, M, Gautier, C 1996SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogenyComput Appl Biosci12543548PubMedGoogle Scholar
  12. Gilbert, W, Souza, SJ, Long, M 1997Origin of genesProc Natl Acad Sci USA9476987703CrossRefPubMedGoogle Scholar
  13. Gilbert, W, Marchionni, M, McKnight, G 1986On the antiquity of intronsCell46151153CrossRefPubMedGoogle Scholar
  14. Hanke, J, Brett, D, Zastrow, I, Aydin, A, Delbruck, S, Lehmann, G, Luft, F, Reich, J, Bork, P 1999Alternative splicing of human genes: more the rule than the exception?Trends Genet15389390CrossRefPubMedGoogle Scholar
  15. Hentze, MW, Kulozik, AE 1999A perfect message: RNA surveillance and nonsense-mediated decayCell96307310CrossRefPubMedGoogle Scholar
  16. Jeanmougin, F, Thompson, JD, Gouy, M, Higgins, DG, Gibson, TJ 1998Multiple sequence alignment with Clustal XTrends Biochem Sci23403405CrossRefPubMedGoogle Scholar
  17. Kent, WJ, Zahler, AM 2000Conservation, regulation, synteny, and introns in a large-scale C. briggsaeC. elegans genomic alignmentGenome Res1011151125CrossRefPubMedGoogle Scholar
  18. Kricker, MC, Drake, JW, Radman, M 1992Duplication-targeted DNA methylation and mutagenesis in the evolution of eukaryotic chromosomesProc Natl Acad Sci USA8910751079PubMedGoogle Scholar
  19. Lerat, E, Capy, P, Biemont, C 2002Codon usage by transposable elements and their host genes in five speciesJ Mol Evol54625637CrossRefPubMedGoogle Scholar
  20. Li, WH 1993Unbiased estimation of the rates of synonymous and nonsynonymous substitutionJ Mol Evol369699PubMedGoogle Scholar
  21. Lim, LP, Burge, CB 2001A computational analysis of sequence features involved in recognition of short intronsProc Natl Acad Sci USA981119311198CrossRefPubMedGoogle Scholar
  22. Logsdon, JM,Jr 1998The recent origins of spliceosomal introns revisitedCurr Opin Genet Dev8637648CrossRefPubMedGoogle Scholar
  23. Lykke-Andersen, J 2001mRNA quality control: Marking the message for life or deathCurr Biol118891CrossRefPubMedGoogle Scholar
  24. Lynch, M 2002Intron evolution as a population-genetic processProc Natl Acad Sci USA9961186123CrossRefPubMedGoogle Scholar
  25. Lynch, M, Kewalramani, A 2003Messenger RNA surveillance and the evolutionary proliferation of intronsMol Biol Evol20563571CrossRefPubMedGoogle Scholar
  26. Lynch, M, Richardson, AO 2002The evolution of spliceosomal intronsCurr Opin Genet Dev12701710CrossRefPubMedGoogle Scholar
  27. Mange, A, Prudhomme, JC 1999Comparison of Bombyx mori and Helicoverpa armigera cytoplasmic actin genes provides clues to the evolution of actin genes in insectsMol Biol Evol16165172PubMedGoogle Scholar
  28. Maxwell, ES, Fourier, MJ 1995The small nucleolar RNAsAnnu Rev Biochem64897934CrossRefPubMedGoogle Scholar
  29. Nixon, JE, Wang, A, Morrison, HG, McArthur, AG, Sogin, ML, Loftus, BJ, Samuelson, J 2002A spliceosomal intron in Giardia lambliaProc Natl Acad Sci USA9937013705CrossRefPubMedGoogle Scholar
  30. Robertson, HM 1998Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron lossGenome Res8449463PubMedGoogle Scholar
  31. Robertson, HM 2000The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and lossesGenome Res10192203CrossRefPubMedGoogle Scholar
  32. Rogozin, IB, Lyons-Weiler, J, Koonin, EV 2000Intron sliding in conserved gene familiesTrends Genet16430432CrossRefPubMedGoogle Scholar
  33. Sawyer, S 1989Statistical tests for detecting gene conversionMol Biol Evol6526538Google Scholar
  34. Semple, C, Wolfe, KH 1999Gene duplication and gene conversion in the Caenorhabditis elegans genomeJ Mol Evol48555564PubMedGoogle Scholar
  35. Seo, HC, Kube, M, Edvardsen, RB, Jensen, MF, Beck, A, Spriet, E, Gorsky, G, Thompson, EM, Lehrach, H, Reinhardt, R, Chourrout, D 2001Miniature genome in the marine chordate Oikopleura dioicaScience2942506CrossRefPubMedGoogle Scholar
  36. Spada, F, Steen, H, Troedsson, C, Kallesoe, T, Spriet, E, Mann, M, Thompson, EM 2001Molecular patterning of the oikoplastic epithelium of the larvacean tunicate Oikopleura dioicaJ Biol Chem2762062420632CrossRefPubMedGoogle Scholar
  37. Thioulouse, J, Chessel, D, Dolédec, S, Olivier, JM 1997ADE-4: A multivariate analysis and graphical display softwareStat Comput77583CrossRefGoogle Scholar
  38. Thompson, JD, Higgins, DG, Gibson, TJ 1994CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choiceNucleic Acids Res2246734680PubMedGoogle Scholar
  39. Tweedie, S, Charlton, J, Clark, V, Bird, A 1997Methylation of genomes and genes at the invertebrate-vertebrate boundaryMol Cell Biol1714691475PubMedGoogle Scholar
  40. Venkatesh, B, Ning, Y, Brenner, S 1999Late changes in spliceosomal introns define clades in vertebrate evolutionProc Natl Acad Sci USA961026710271CrossRefPubMedGoogle Scholar
  41. Wada, H, Kobayashi, M, Sato, R, Satoh, N, Miyasaka, H, Shirayama, Y 2002Dynamic, insertion-deletion of introns in deuterostome EF-1 alpha genesJ Mol Evol54118128PubMedGoogle Scholar

Copyright information

© Springer 2004

Authors and Affiliations

  • Rolf B. Edvardsen
    • 1
  • Emmanuelle Lerat
    • 2
  • Anne Dorthea Maeland
    • 1
  • Mette Flåt
    • 1
  • Rita Tewari
    • 1
  • Marit F. Jensen
    • 1
  • Hans Lehrach
    • 3
  • Richard Reinhardt
    • 3
  • Hee-Chan Seo
    • 1
  • Daniel Chourrout
    • 1
    Email author
  1. 1.Sars Centre for Marine Molecular BiologyBergen High Technology CentreThormoehlensgt. 55Norway
  2. 2.Laboratoire de Biométrie et Biologie EvolutiveUniversité Lyon 1Villeurbanne CedexFrance
  3. 3.Max-Planck Institute for Molecular GeneticsBerlinGermany

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