Skip to main content
Log in

The Evolution of tRNA-Leu Genes in Animal Mitochondrial Genomes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Animal mitochondrial genomes usually have two transfer RNAs for leucine: one, with anticodon UAG, translates the four-codon family CUN, while the other, with anticodon UAA, translates the two-codon family UUR. These two genes must differ at the third anticodon position, but in some species the genes differ at many additional sites, indicating that these genes have been independent for a long time. Duplication and deletion of genes in mitochondrial genomes occur frequently during the evolution of the Metazoa. If a tRNA-Leu gene were duplicated and a substitution occurred in the anticodon, this would effectively turn one type of tRNA into the other. The original copy of the second tRNA type might then be lost by a deletion elsewhere in the genome. There are several groups of species in which the two tRNA-Leu genes occur next to one another (or very close) on the genome, which suggests that tandem duplication has occurred. Here we use RNA-specific phylogenetic methods to determine evolutionary trees for both genes. We present evidence that the process of duplication, anticodon mutation, and deletion of tRNA-Leu genes has occurred at least five times during the evolution of the metazoa—once in the common ancestor of all protostomes, once in the common ancestor of echinoderms and hemichordates, once in the hermit crab, and twice independently in mollusks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. JL Boore DV Lavrov WM Brown (1998) ArticleTitleGene translocation links insects and crustaceans. Nature 392 667–668 Occurrence Handle10.1038/33577 Occurrence Handle1:CAS:528:DyaK1cXjtVWmuro%3D Occurrence Handle9565028

    Article  CAS  PubMed  Google Scholar 

  2. Boore JL (2000) Mitochondrial gene arrangement source guide. Available at http://www.jgi.doe.gov/Mitochondrial_Genomics.html

  3. P Cantatore MN Gadaleta M Roberti C Saccone AC Wilson (1987) ArticleTitleDuplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature 329 853–855 Occurrence Handle10.1038/329853a0 Occurrence Handle1:CAS:528:DyaL2sXmtlSmsr4%3D Occurrence Handle3670390

    Article  CAS  PubMed  Google Scholar 

  4. J Castresana G Feldmaier-Fuchs S Yokobori N Satoh S Pääbo (1998) ArticleTitleThe mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria. Genetics 150 1115–1123 Occurrence Handle1:CAS:528:DyaK1cXnsFCntLo%3D Occurrence Handle9799263

    CAS  PubMed  Google Scholar 

  5. MJ Hickerson CW Cunningham (2000) ArticleTitleDramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Cristacea, Anomura). Mol Biol Evol 17 639–644 Occurrence Handle1:CAS:528:DC%2BD3cXisVSgtLo%3D Occurrence Handle10742054

    CAS  PubMed  Google Scholar 

  6. PG Higgs (1998) ArticleTitleCompensatory neutral mutations and the evolution of RNA. Genetica 102/103 91–101 Occurrence Handle10.1023/A:1017059530664 Occurrence Handle1:CAS:528:DyaK1cXlslGktr8%3D

    Article  CAS  Google Scholar 

  7. PG Higgs (2000) ArticleTitleRNA secondary structure: Physical and computational aspects. Q Rev Biophys 33 199–253 Occurrence Handle10.1017/S0033583500003620 Occurrence Handle1:CAS:528:DC%2BD3MXntFGmur0%3D Occurrence Handle11191843

    Article  CAS  PubMed  Google Scholar 

  8. C Hudelot V Gowri-Shankar H Jow M Rattray PG Higgs (2003) ArticleTitleRNA-based phylogenetic methods: Application to mammalian mitochondrial sequences. Mol Phyl Evol

    Google Scholar 

  9. D Jameson AP Gibson C Hudelot PG Higgs (2003) ArticleTitleOGRe: A relational database for comparative analysis of mitochondrial genomes. Nucleic Acids Res 31 202–206 Occurrence Handle10.1093/nar/gkg077 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSntbg%3D Occurrence Handle12519982

    Article  CAS  PubMed  Google Scholar 

  10. H Jow C Hudelot M Rattray PG Higgs (2002) ArticleTitleBayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol 19 1591–1601 Occurrence Handle1:STN:280:DC%2BD38vkt12jtg%3D%3D Occurrence Handle12200486

    CAS  PubMed  Google Scholar 

  11. CG Kurland (1992) ArticleTitleEvolution of mitochondrial genomes and the genetic code. BioEssays 14 709–714 Occurrence Handle1:CAS:528:DyaK3sXjtlKhsg%3D%3D Occurrence Handle1365884

    CAS  PubMed  Google Scholar 

  12. DC Larkin AM Williams SA Martinis GE Fox (2002) ArticleTitleIdentification of essential domains for Escherichia coli tRNA(leu) aminoacylation and amino acid editing using minimalist RNA molecules. Nucleic Acids Res 30 2103–2113 Occurrence Handle10.1093/nar/30.10.2103 Occurrence Handle1:CAS:528:DC%2BD38XktFyksbo%3D Occurrence Handle12000830

    Article  CAS  PubMed  Google Scholar 

  13. TM Lowe SR Eddy (1997) ArticleTitletRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 955–964 Occurrence Handle1:CAS:528:DyaK2sXhvVahtrk%3D Occurrence Handle9023104

    CAS  PubMed  Google Scholar 

  14. Nicholas, KB and Nicholas Jr, HB (1997) GeneDoc: A tool for editing and annotating multiple sequence alignments. 25 (http://www.psc.edu/biomed/genedoc)

  15. L Ribas de Pouplana P Schimmel (2001) ArticleTitleAminoacyl-tRNA synthetases: Potential markers of genetic code development. Trends Biochem Sci 26 591–596 Occurrence Handle10.1016/S0968-0004(01)01932-6 Occurrence Handle1:CAS:528:DC%2BD3MXnt1WjsbY%3D Occurrence Handle11590011

    Article  CAS  PubMed  Google Scholar 

  16. NJ Savill DC Hoyle PG Higgs (2001) ArticleTitleRNA sequence evolution with secondary structure constraints: Comparison of substitution rate models using maximum likelihood methods. Genetics 157 399–411 Occurrence Handle1:CAS:528:DC%2BD3MXhtFKhtbY%3D Occurrence Handle11139520

    CAS  PubMed  Google Scholar 

  17. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24 487–4882

    Google Scholar 

  18. CS Wilding PJ Mill J Grahame (1999) ArticleTitlePartial sequence of the mitochondrial genome of Littorina saxatilis: Relevance to gastropod phylogenetics. J Mol Evol 48 348–359 Occurrence Handle1:CAS:528:DyaK1MXhs1yls74%3D Occurrence Handle10093225

    CAS  PubMed  Google Scholar 

  19. Z Yang (1994) ArticleTitleMaximum likelihood phylogenetic estimation from DNA sequence with variable rates over sites: Approximate methods. J Mol Evol 39 306–314 Occurrence Handle7932792

    PubMed  Google Scholar 

  20. S Yokobori T Ueda G Feldmaier-Fuchs S Pääbo R Ueshima A Kondow K Nishikawa K Watanabe (1999) ArticleTitleComplete DNA sequence of the mitochondrial genomes of the ascidian Halocynthia roretzi (Chordata, Urochordata). Genetics 153 1851–1862 Occurrence Handle1:CAS:528:DC%2BD3cXhvV2ktQ%3D%3D Occurrence Handle10581290

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

P. Higgs is supported by the Canada Research Chairs organization. D. Jameson and M. Rattray are supported by the Biotechnology and Biological Sciences Research Council and H. Jow is supported by the Engineering and Physical Science Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul G. Higgs.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Higgs, P.G., Jameson, D., Jow, H. et al. The Evolution of tRNA-Leu Genes in Animal Mitochondrial Genomes . J Mol Evol 57, 435–445 (2003). https://doi.org/10.1007/s00239-003-2494-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2494-6

Keywords

Navigation