Journal of Molecular Evolution

, Volume 59, Issue 1, pp 90–96

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

Article

Abstract

Reduction of genome size and gene shortening have been observed in a number of parasitic and mutualistic intracellular symbionts. Reduction of coding capacity is also a unifying principle in the evolutionary history of mitochondria, but little is known about the evolution of gene length in mitochondria. The genes for cytochrome c oxidase subunits I–III, cytochrome b, and the large and small subunit rRNAs are, with very few exceptions, always found on the mitochondrial genome. These resident mitochondrial genes can therefore be used to test whether the reduction in gene lengths observed in a number of intracellular symbionts is also seen in mitochondria. Here we show that resident mitochondrial gene products are shorter than their corresponding counterparts in α-proteobacteria and, furthermore, that the reduction of mitochondrial genome size is correlated with a reduction in the length of the corresponding resident gene products. We show that relative genomic AT content, which has been identified as a factor influencing gene lengths in other systems, cannot explain gene length/genome size covariance observed in mitochondria. Our data are therefore in agreement with the idea that gene length evolves as a consequence of selection for smaller genomes, either to avoid accumulation of deleterious mutations or triggered by selection for a replication advantage.

Keywords

Mitochondrial genome size Gene length Gene length reduction Mitochondrial evolution Gene length/genome size covariation 

References

  1. Allen, JF 2003The function of genomes in bioenergetic organellesPhil Trans R Soc Lond B Biol Sci3581937CrossRefGoogle Scholar
  2. Allen, JF, Raven, JA 1996Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organellesJ Mol Evol42482492PubMedGoogle Scholar
  3. Andersson, GE, Kurland, CG 1991An extreme codon preference strategy: Codon reassignmentMol Biol Evol8530544PubMedGoogle Scholar
  4. Andersson, SG, Kurland, CG 1998Reductive evolution of resident genomesTrends Microbiol6263268CrossRefPubMedGoogle Scholar
  5. Andersson, SGE, Zomorodipour, A, Andersson, JO, Sicheritz-Ponten, T, Alsmark, UCM, Podowski, RM, Näslund, AK, Eriksson, A-S, Winkler, HH, Kurland, CG 1998The genome sequence of Rickettsia prowazekii and the origin of mitochondriaNature396133140CrossRefPubMedGoogle Scholar
  6. Berg, OG, Kurland, CG 2000Why mitochondrial genes are most often found in nucleiMol Biol Evol17951961PubMedGoogle Scholar
  7. Blanchard, JL, Lynch, M 2000Organellar genes: Why do they end up in the nucleus?Trends Genet16315320CrossRefPubMedGoogle Scholar
  8. Burt, A 1989Comparative methods using phylogenetically independent contrastsOxford Surv Evol Biol63353Google Scholar
  9. Busse, I, Preisfeld, A 2002Unusually expanded SSU ribosomal DNA of primary osmotrophic euglenids: Molecular evolution and phylogenetic inferenceJ Mol Evol55757767CrossRefPubMedGoogle Scholar
  10. Cavalier-Smith, T 2002Nucleomorphs: Enslaved algal nucleiCurr Opin Microbiol5612619CrossRefPubMedGoogle Scholar
  11. Charles, H, Mouchiroud, D, Lobry, J, Goncalves, I, Rahbe, Y 1999Gene size reduction in the bacterial aphid endosymbiont, BuchneraMol Biol Evol.18201822PubMedGoogle Scholar
  12. Doolittle, WF 1998You are what you eat: A gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomesTrends Genet14307311CrossRefPubMedGoogle Scholar
  13. Gillespie, DE, Salazar, NA, Rehkopf, DH, Feagin, JE 1999The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum have short A tailsNucleic Acids Res2724162422CrossRefPubMedGoogle Scholar
  14. Gray, MW, Lang, BF, Cedergren, R, Golding, GB, Lemieux, C, Sankoff, D, Turmel, M, Brossard, N, Delage, E, Littlejohn, TG, Plante, I, Rioux, P, Saint-Louis, D, Zhu, Y, Burger, G 1998Genome structure and gene content in protist mitochondrial DNAsNucleic Acids Res26865878CrossRefPubMedGoogle Scholar
  15. Gray, MW, Burger, G, Lang, BF 1999Mitochondrial evolutionScience28314761481CrossRefPubMedGoogle Scholar
  16. Howe, CJ, Barbrook, AC, Lockhart, PJ 2000Organelle genes—Do they jump or are they pushed?Trends Genet166566CrossRefPubMedGoogle Scholar
  17. Kurland, CG, Andersson, SG 2000Origin and evolution of the mitochondrial proteomeMicrobiol Mol Biol Rev64786820CrossRefPubMedGoogle Scholar
  18. Lang, BF, Gray, MW, Burger, G 1999Mitochondrial genome evolution and the origin of eukaryotesAnnu Rev Genet33351397CrossRefPubMedGoogle Scholar
  19. Lynch, M 1996Mutation accumulation in transfer RNAs: Molecular evidence for Muller’s ratchet in mitochondrial genomesMol Biol Evol13209220PubMedGoogle Scholar
  20. Marienfeld, J, Unseld, M, Brennicke, A 1999The mitochondrial genome of Arabidopsis is composed of both native and immigrant informationTrends Plant Sci12495502CrossRefGoogle Scholar
  21. Mira, AH, Ochman, H, Moran, NA 2001Deletional bias and the evolution of bacterial genomesTrends Genet17589596CrossRefPubMedGoogle Scholar
  22. Oliver, JL, Marin, A 1996A relationship between GC content and coding-sequence lengthJ Mol Evol43216223PubMedGoogle Scholar
  23. Palmer, JD, Adams, KL, Cho, Y, Parkinson, CL, Qiu, YL, Song, K 2000Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation ratesProc Natl Acad Sci USA9769606966CrossRefPubMedGoogle Scholar
  24. Secq, MPO-L, Fontaine, JM, Rousvoal, S, Kloareg, B, Goer, SL-D 2001The complete sequence of a brown algal mitochondrial genome, the ectocarpale Pylaiella littoralis (L.) KjellmJ Mol Evol538088PubMedGoogle Scholar
  25. Selosse, M, Albert, B, Godelle, B 2001Reducing the genome size of organelles favours gene transfer to the nucleusTrends Ecol Evol16135141CrossRefPubMedGoogle Scholar
  26. Shimko, N, Liu, L, Lang, BF, Burger, G 2001GOBASE: The organelle genome databaseNucleic Acids Res29128132CrossRefPubMedGoogle Scholar
  27. Thorness, PE, Fox, TD 1990Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiaeNature346376379CrossRefPubMedGoogle Scholar
  28. Vivares, CP, Gouy, M, Thomarat, F, Metenier, G 2002Functional and evolutionary analysis of a eukaryotic parasitic genomeCurr Opin Microbiol5499505CrossRefPubMedGoogle Scholar
  29. Wernegreen, JJ 2002Genome evolution in bacterial endosymbionts of insectsNat Rev Genet3850861CrossRefPubMedGoogle Scholar
  30. Wuyts, J, Peer, Y, Wacher, R 2001Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNANucleic Acids Res2950175028CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of BiologyUniversity of FribourgFribourgSwitzerland

Personalised recommendations