Journal of Molecular Evolution

, Volume 67, Issue 3, pp 278–290 | Cite as

Oscheius tipulae as an Example of eEF1A Gene Diversity in Nematodes

Article
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Abstract

We characterized four eEF1A genes in the alternative rhabditid nematode model organism Oscheius tipulae. This is twice the copy number of eEF1A genes in C. elegans, C. briggsae, and, probably, many other free-living and parasitic nematodes. The introns show features remarkably different from those of other metazoan eEF1A genes. Most of the introns in the eEF1A genes are specific to O. tipulae and are not shared with any of the other genes described in metazoans. Most of the introns are phase 0 (inserted between two codons), and few are inserted in protosplice sites (introns inserted between the nucleotide sequence A/CAG and G/A). Two of these phase 0 introns are conserved in sequence in two or more of the four eEF1A gene copies, and are inserted in the same position in the genes. Neither of these characteristics has been detected in any of the nematode eEF1A genes characterized to date. The coding sequences were also compared with other eEF1A cDNAs from 11 different nematodes to determine the variability of these genes within the phylum Nematoda. Parsimony and distance trees yielded similar topologies, which were similar to those created using other molecular markers. The presence of more than one copy of the eEF1A gene with nearly identical coding regions makes it difficult to define the orthologous cDNAs. As shown by our data on O. tipulae, careful and extensive examination of intron positions in the eEF1A gene across the phylum is necessary to define their potential for use as valid phylogenetic markers.

Keywords

eEF1A Nematoda Oscheius tipulae Caenorhabditis elegans Intron evolution 
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Notes

Acknowledgments

We would like to thank Dr. Marie Anne Félix for the kind gift of the cDNA library of Oscheius tipulae (strain CEW1). We would also like to thank Drs. Jeffrey J. Shaw (Department of Parasitology, University of São Paulo) and Thomas Blumenthal (Department of Molecular, Cellular, and Developmental Biology, University of Colorado at Boulder) for commentary on the first draft of the manuscript. This work was supported by grants from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, The State of São Paulo Research Foundation). R.N.A. was a FAPESP graduate fellow.

Supplementary material

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References

  1. Abdallah B, Hourdry J, Krieg PA, Denis H, Mazabraud A (1991) Germ cell-specific expression of a gene encoding eukaryotic translation elongation factor 1 alpha (eEF-1 alpha) and generation of eEF-1 alpha retropseudogenes in Xenopus laevis. Proc Natl Acad Sci USA 88:9277–9281PubMedCrossRefGoogle Scholar
  2. Ahn IY, Winter CE (2005) Determination of DNA base composition by small scale acrylamide-CsCl gradient centrifugation. J Biochem Biophys Methods 63:155–160PubMedCrossRefGoogle Scholar
  3. Ahn IY, Winter CE (2006) The genome of Oscheius tipulae: determination of size, complexity and structure by DNA reassociation using fluorescent dye. Genome 49:1007–1015PubMedCrossRefGoogle Scholar
  4. Andersen GR, Pedersen L, Valente L, Chatterjee I, Kinzy TG, Kjeldgaard M, Nyborg J (2000) Structural basis for nucleotide exchange and competition with tRNA in the yeast elongation factor complex eEF1A:eEF1Balpha. Mol Cell 6:1261–1266PubMedCrossRefGoogle Scholar
  5. Bieri T, Blasiar D, Ozersky P et al (2007) WormBase: new content and better access. Nucleic Acids Res (Database Issue):D506–D510Google Scholar
  6. Blaxter ML (2003) Nematoda: genes, genomes and the evolution of parasitism. Adv Parasitol 54:101–195PubMedCrossRefGoogle Scholar
  7. Blumenthal T, Steward K (1997) RNA processing and gene structure. In: Riddle D, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II. Cold Spring Harbor Laboratory Press, Woodbury, NY, pp 117–146Google Scholar
  8. Carr-Schmid A, Durko N, Cavallius J, Merrick WC, Kinzy TG (1999) Mutations in a GTP-binding motif of eukaryotic elongation factor 1A reduce both translational fidelity and the requirement for nucleotide exchange. J Biol Chem 274:30297–30302PubMedCrossRefGoogle Scholar
  9. Cho S, Mitchell A, Regier JC, Mitter C, Poole RW, Friedlander TP, Zhao S (1995) A highly conserved nuclear gene for low-level phylogenetics: elongation factor-1 alpha recovers morphology-based tree for heliothine moths. Mol Biol Evol 12:650–656PubMedGoogle Scholar
  10. Coghlan A, Wolfe KH (2004) Origins of recently gained introns in Caenorhabditis. Proc Natl Acad Sci USA 101:11362–11367PubMedCrossRefGoogle Scholar
  11. Cutter AD, Wasmuth JD, Blaxter ML (2006) The evolution of biased codon and amino acid usage in Nematode genomes. Mol Biol Evol 23:2303–2315PubMedCrossRefGoogle Scholar
  12. De Ley P (2006) A quick tour of nematode diversity and the backbone of nematode phylogeny, The C. elegans Research Community, editor. WormBook, doi/10.1895/wormbook.1.41.1/ Available at: http://www.wormbook.org
  13. Deschamps S, Morales J, Mazabraud A, le Maire M, Denis H, Brown DD (1991) Two forms of elongation factor 1 alpha (EF-1 alpha O and 42Sp50), present in oocytes, but absent in somatic cells of Xenopus laevis. J Cell Biol 114:1109–1111PubMedCrossRefGoogle Scholar
  14. Dever TE, Glynias MJ, Merrick WC (1987) GTP-binding domain: three consensus sequence elements with distinct spacing. Proc Natl Acad Sci USA 84:1814–1818PubMedCrossRefGoogle Scholar
  15. Dibb NJ, Newman AJ (1989) Evidence that introns arose at protosplice sites. EMBO J 8:2015–2021PubMedGoogle Scholar
  16. Dichtel-Danjoy ML, Félix MA (2004) Phenotypic neighborhood and micro-evolvability. Trends Genet 20:268–276PubMedCrossRefGoogle Scholar
  17. Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487PubMedCrossRefGoogle Scholar
  18. Evans D, Zorio D, MacMorris M, Winter CE, Lea K, Blumenthal T (1997) Operons and SL2 trans-splicing exist in nematodes outside the genus Caenorhabditis. Proc Natl Acad Sci USA 94:9751–9756PubMedCrossRefGoogle Scholar
  19. Farrer T, Roller AB, Kent WJ, Zahler AM (2002) Analysis of the role of Caenorhabditis elegans GC-AG introns in regulated splicing. Nucleic Acids Res 30:3360–3367PubMedCrossRefGoogle Scholar
  20. Fedorov A, Roy S, Fedorova L, Gilbert W (2003) Mystery of intron gain. Genome Res 13:2236–2241PubMedCrossRefGoogle Scholar
  21. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13PubMedCrossRefGoogle Scholar
  22. Félix MA (2006) Oscheius tipulae. In: The C. elegans Research Community, (ed) WormBook, doi/10.1895/wormbook.1.119.1. Available at: http://www.wormbook.org
  23. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: multiple sequence alignments in PostScript. Bioinformatics 15:305–308PubMedCrossRefGoogle Scholar
  24. Guiliano DB, Blaxter ML (2006) Operon conservation and the evolution of trans-splicing in the phylum Nematoda. PLoS Biol 2:1871–1882Google Scholar
  25. Hashimoto T, Nakamura Y, Kamaishi T, Adachi J, Nakamura F, Okamoto K, Hasegawa M (1995) Phylogenetic place of kinetoplastid protozoa inferred from a protein phylogeny of elongation factor 1 alpha. Mol Biochem Parasitol 70:181–185PubMedCrossRefGoogle Scholar
  26. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  27. Jordal BH (2002) Elongation factor 1 α resolves the monophyly of the haplodiploid ambrosia beetles Xyleborini (Coleoptera: Curculionidae). Insect Mol Biol 11:453–465PubMedCrossRefGoogle Scholar
  28. Kent WJ, Zahler AM (2000) Conservation, regulation, synteny, and introns in a large-scale C. briggsae-C. elegans genomic alignment. Genome Res 10:1115–1125PubMedCrossRefGoogle Scholar
  29. Kim DW, Uetsuki T, Kaziro Y, Yamaguchi N, Sugano S (1990) Use of the human elongation factor 1 alpha promoter as a versatile and efficient expression system. Gene 91:217–223PubMedCrossRefGoogle Scholar
  30. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 101:9003–9008PubMedCrossRefGoogle Scholar
  31. Lee S, Francoeur AM, Liu S, Wang E (1992) Tissue-specific expression in mammalian brain, heart, and muscle of S1, a member of the elongation factor–1 alpha gene family. J Biol Chem 267:24064–24068PubMedGoogle Scholar
  32. Lee S, Wolfraim LA, Wang E (1993) Differential expression of S1 and elongation factor-1 alpha during rat development. J Biol Chem 268:24453–24459PubMedGoogle Scholar
  33. Linney E, Hardison NL, Lonze BE, Lyons S, DiNapoli L (1999) Transgene expression in zebrafish: a comparison of retroviral-vector and DNA-injection approaches. Dev Biol 213:207–216PubMedCrossRefGoogle Scholar
  34. Liu G, Edmonds BT, Condeelis J (1996) pH, EF-1alpha and the cytoskeleton. Trends Cell Biol 6:168–171PubMedCrossRefGoogle Scholar
  35. Llopart A, Comeron JM, Brunet FG, Lachaise D, Long M (2002) Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci USA 99:8121–8126PubMedCrossRefGoogle Scholar
  36. Long M, de Souza SJ, Rosenberg C, Gilbert W (1998) Relationship between “protosplice sites” and intron phases: evidence from dicodon analysis. Proc Natl Acad Sci USA 95:219–223PubMedCrossRefGoogle Scholar
  37. Madsen HO, Poulsen K, Dahl O, Clark BF, Hjorth JP (1990) Retropseudogenes constitute the major part of the human elongation factor 1 alpha gene family. Nucleic Acids Res 18:1513–1516PubMedCrossRefGoogle Scholar
  38. McInerney JO (1998) GCUA (General Codon Usage Analysis). Bioinformatics 14:372–373PubMedCrossRefGoogle Scholar
  39. Mitreva M, Blaxter ML, Bird DM, McCarter JP (2005) Comparative genomics of nematodes. Trends Genet 21:573–581PubMedCrossRefGoogle Scholar
  40. Mitreva M, Wendl MC, Martin J, Wylie T, Yin Y, Larson A, Parkinson J, Waterston RH, McCarter JP (2006) Codon usage patterns in Nematoda: analysis based on over 25 million codons in thirty-two species. Genome Biol 7:R75PubMedCrossRefGoogle Scholar
  41. Negrutskii BS, El’skaya N (1998) Eukaryotic translation elongation factor 1 alpha: structure, expression, functions, and possible role in aminoacyl-tRNA channeling. Prog Nucleic Acid Res Mol Biol 60:47–78PubMedCrossRefGoogle Scholar
  42. Peden JF (1999) Analysis of codon usage. PhD thesis. University of Nottingham, UKGoogle Scholar
  43. Qiu WG, Schisler N, Stoltzfus A (2004) The evolutionary gain of spliceosomal introns: sequence and phase preferences. Mol Biol Evol 21:1252–1263PubMedCrossRefGoogle Scholar
  44. Ridgley EL, Xiong ZH, Kaur KJ, Ruben L (1996) Genomic organization and expression of elongation factor-1 alpha genes in Trypanosoma brucei. Mol Biochem Parasitol 79:119–123PubMedCrossRefGoogle Scholar
  45. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  46. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  47. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467PubMedCrossRefGoogle Scholar
  48. Shepherd JC, Walldorf U, Hug P, Gehring W (1989) Fruit flies with additional expression of the elongation factor EF-1 alpha live longer. Proc Natl Acad Sci USA 86:7520–7521PubMedCrossRefGoogle Scholar
  49. Slobin LI (1980) The role of eucaryotic factor Tu in protein synthesis. The measurement of the elongation factor Tu content of rabbit reticulocytes and other mammalian cells by a sensitive radioimmunoassay. Eur J Biochem 110:555–563PubMedCrossRefGoogle Scholar
  50. Stiernagle T (1999) Maintenance of C. elegans. In: Hope IA (ed) C. elegans—a practical approach. Oxford University Press, Oxford, UK, pp 51–67Google Scholar
  51. Sulston J, Hodgkin J (1988) Methods. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Woodbury, NY, pp 587–606Google Scholar
  52. Sverdlov AV, Rogozin IB, Babenko VN, Koonin EV (2003) Evidence of splice signal migration from exon to intron during intron evolution. Curr Biol 13:2170–2174PubMedCrossRefGoogle Scholar
  53. Waterston RH, Sulston JE, Coulson AR (1997) The genome. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II. Cold Spring Harbor Laboratory Press, Woodbury, NY, pp 23–45Google Scholar
  54. Winter CE, Penha C, Blumenthal T (1996) Comparison of a vitellogenin gene between two distantly related rhabditid nematode species. Mol Biol Evol 13:674–684PubMedGoogle Scholar
  55. Wylie T, Martin JC, Dante M, Mitreva MD, Clifton SW, Chinwalla A, Waterston RH, Wilson RK, McCarter JP (2004) Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res (Database Issue):D423–D426Google Scholar
  56. Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 347:494–496PubMedCrossRefGoogle Scholar
  57. Zhaxybayeva O, Gogarten JP (2003) Spliceosomal introns: new insights into their evolution. Curr Biol 13:R764–R766PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Departmento de ParasitologiaInstituto de Ciências Biomédicas/Universidade de São PauloSao PauloBrazil

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