Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Mitochondrial gene history and mRNA localization: is there a correlation?

Nature Reviews Genetics volume 4, pages 391–397 (2003)Cite this article

Abstract

Phylogenetic studies of the yeast mitochondrial proteome have shown a complex evolutionary scenario, in which proteins of bacterial origin form complexes with proteins of eukaryotic origin. Exciting new results from whole-genome microarray studies of subcellular mRNA localizations have shown that mRNAs that are of putative bacterial origin are mainly translated on polysomes that are associated with the mitochondrion, whereas those of eukaryotic origin are generally translated on free cytosolic polysomes. Understanding these newly discovered relationships promises insights into old questions about organelle origins and mRNA localization in the eukaryotic cell.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Aerobic respiration in mitochondria and Rickettsia.
Figure 2: The dual origin of the mitochondrial proteome.
Figure 3: Functional profile of the yeast mitochondrial proteome.
Figure 4: Yeast mitochondrial mRNAs — presequences and protein locations.
Figure 5: Yeast mitochondrial mRNAs: origins and polysome locations.

Similar content being viewed by others

References

  1. Saraste, M. Oxidative phosphorylation at the fin de siecle. Science 283, 1488–1492 (1999).

    Article  CAS  Google Scholar 

  2. Dillon, A. et al. Rates of behaviour and aging specified by mitochondrial function during development. Science 298, 2398–2401 (2002).

    Article  Google Scholar 

  3. Wallace, D. C. Mitochondrial diseases in man and mouse. Science 283, 1482–1487 (1999).

    Article  CAS  Google Scholar 

  4. Margulis, L. Symbiosis in Cell Evolution (Freeman, San Francisco, 1981).

    Google Scholar 

  5. Gray, M., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476–1481 (1999).

    Article  CAS  Google Scholar 

  6. Karlberg, O., Canbäck, B., Kurland, C. G. & Andersson, S. G. E. The dual origin of the yeast mitochondrial proteome. Yeast 17, 170–187 (2000).

    Article  CAS  Google Scholar 

  7. Marc et al. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3, 159–164 (2002).

  8. Farquhar, J., Bao, H. & Thiemans, M. Atmospheric influence on Earth's earliest sulfur cycle. Science 289, 765–769 (2000).

    Article  Google Scholar 

  9. Goodner, B. et al. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294, 2323–2328 (2001).

    Article  CAS  Google Scholar 

  10. Wood, D. W. et al. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294, 2317–2323 (2001).

    Article  CAS  Google Scholar 

  11. Kaneko, T. et al. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7, 331–338 (2000).

    Article  CAS  Google Scholar 

  12. DelVecchio, V. G. et al. The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc. Natl Acad. Sci. USA 99, 443–448 (2002).

    Article  CAS  Google Scholar 

  13. Andersson, S. G. E. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).

    Article  CAS  Google Scholar 

  14. Kurland, C. G. & Andersson, S. G. E. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786–820 (2000).

    Article  CAS  Google Scholar 

  15. Canbäck, B., Andersson, S. G. E. & Kurland, C. G. The global phylogeny of glycolytic enzymes. Proc. Natl Acad. Sci. USA 99, 6097–6102 (2002).

    Article  Google Scholar 

  16. Woischnik, M. & Moraes, C. T. Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res. 12, 885–893 (2002).

    Article  CAS  Google Scholar 

  17. Hodges, P. E., McKee, A. H., Davis, B. P., Payne, W. E. & Garrels, J. I. The Yeast Proteome Database (YPD): a model for the organization and presentation of genome-wide functional data. Nucleic Acids Res. 27, 69–73 (1999).

    Article  CAS  Google Scholar 

  18. Kumar, A. Subcellular localization of the yeast proteome. Genes Dev. 16, 707–719 (2002).

    Article  CAS  Google Scholar 

  19. Marx, S. et al. Structure of the bc1 complex from Seculamonas ecuadoriensis, a jakobid flagellate with an ancestral mitochondrial genome. Mol. Biol. Evol. 20, 145–153 (2003).

    Article  CAS  Google Scholar 

  20. Amiri, H., Karlberg, O. & Anderssson, S. G. E. Deep origin of plastid/parasite ATP/ADP translocases. J. Mol. Evol. 56, 137–150 (2003).

    Article  CAS  Google Scholar 

  21. Pfanner, N. & Geissler, A. Versatility of the mitochondrial import machinery. Nature Rev. Mol. Cell Biol. 2, 339–349 (2001).

    Article  CAS  Google Scholar 

  22. Geissler, A. et al. The mitochondrial presequence translocase: an essential role of Tim50 in directing preproteins to the import channel. Cell 111, 507–518 (2002).

    Article  CAS  Google Scholar 

  23. Lithgow, T. Targeting of proteins to mitochondria. FEBS Lett. 476, 22–26 (2000).

    Article  CAS  Google Scholar 

  24. Gratzer, S., Beilharz, T., Beddoe, T., Henry, M. F. & Lithgow, T. The mitochondrial protein targeting suppressor (mts1) mutation maps to the mRNA-binding domain of Np13p and affects translation on cytoplasmic polysomes. Mol. Microbiol. 35, 1277–1285 (2000).

    Article  CAS  Google Scholar 

  25. George, R., Walsh, P., Beddoe, T. & Lithgow, T. The nascent polypeptide-associated complex (NAC) promotes interaction of ribosomes with the mitochondrial surface in vivo. FEBS Lett. 516, 213–216. (2002).

    Article  CAS  Google Scholar 

  26. Margeot, A. et al. In Saccharomyces cerevisiae, ATP2 mRNA sorting to the vicinity of mitochondria is essential for respiratory function. EMBO J. 21, 6893–6904 (2002).

    Article  CAS  Google Scholar 

  27. Fujiki, M. & Verner, K. Coupling of cytosolic protein synthesis and mitochondrial protein import in yeast: evidence for co-translational import in vivo. J. Biol. Chem. 268, 1914–1920 (1993).

    CAS  PubMed  Google Scholar 

  28. Steinmetz, L. M. et al. Systematic screen for human disease genes in yeast. Nature Genet. 31, 400–404 (2002).

    Article  CAS  Google Scholar 

  29. Chinnery, P. F. & Turnbull, D. M. The epidemiology and treatment of mitochondrial disease. Am. J. Med. Genet. 106, 94–101 (2001).

    Article  CAS  Google Scholar 

  30. Yaffe, M. P. The machinery of mitochondria inheritance and behaviour. Science 283, 1493–1497 (1999).

    Article  CAS  Google Scholar 

  31. Juan, A. S., Brown, M. D. & Wallace, D. C. A mitochondrial DNA mutation at nucleotide pair 14459 of the NADH dehydrogenase subunit 6 gene associated with maternally inherited Leber hereditary optic neuropathy and dystonia. Proc. Natl Acad. Sci. USA 91, 6206–6210 (1994).

    Article  Google Scholar 

  32. Shoffner, J. M. et al. Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA (Lys) mutation. Cell 61, 931–937 (1990).

    Article  CAS  Google Scholar 

  33. Goto, Y., Nonaka, I. & Horai, S. A mutation in the tRNA (Leu)(UU) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348, 651–653 (1990).

    Article  CAS  Google Scholar 

  34. Bourgeron, T. et al. Mutation of a nuclear succcinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nature Genet. 11, 144–149 (1995).

    Article  CAS  Google Scholar 

  35. Loeffen, J. et al. The first nuclear-encoded complex I mutation in a patient with Leigh syndrome. Am. J. Hum. Genet. 63, 1594–1597 (1998).

    Article  Google Scholar 

  36. Tiranti, V. et al. Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am. J. Hum. Genet. 63, 1609–1621 (1998).

    Article  CAS  Google Scholar 

  37. Graham, B. H. et al. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nature Genet. 16, 226–234 (1997).

    Article  CAS  Google Scholar 

  38. Murdock, D. G., Boone, B. E., Esposito, L. A. & Wallace, D. C. Up-regulation of nuclear and mitochondrial genes in the skeletal muscle of mice lacking the heart/muscle isoform of the adenine nucleotide translocator. J. Biol. Chem. 174, 14429–14433 (1999).

    Article  Google Scholar 

  39. Esposito, L. A., Melov, S., Panov, A., Cottrell, B. A. & Wallace, D. C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl Acad. Sci. USA 96, 4820–4825 (1999).

    Article  CAS  Google Scholar 

  40. Petit, P. X., Susin, S. A., Zamzami, N., Mignotte, B. & Kroemer, G. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396, 7–13 (1996).

    Article  CAS  Google Scholar 

  41. Green, D. R. & Reed, J. C. Mitochondria and apoptosis. Science 281, 1309–1312 (1998).

    Article  CAS  Google Scholar 

  42. Susin, S. A. et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 387–389 (1999).

    Article  Google Scholar 

  43. Andersson, S. G. E. & Kurland, C. G. Origin of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2, 535–541 (1999).

    Article  CAS  Google Scholar 

  44. Martin, W. & Mueller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).

    Article  CAS  Google Scholar 

  45. Moreira, D. & Lopez-Garcia, P. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998).

    Article  CAS  Google Scholar 

  46. Brooks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999).

    Article  Google Scholar 

  47. Kump, L. R., Kasting, J. F. & Barley, M. E. Rise of atmospheric oxygen and the 'upside-down' Archaean mantle. Geol. Geochem. Geophys. 2 (2001).

  48. Catling, D. C., Zahnle, K. J. & McKay, C. P. Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839–843 (2001).

    Article  CAS  Google Scholar 

  49. Emanuelsson, O., Nielsen, H., Brunak, S. & von Heijne, G. Predicting subcellular localization of proteins based on their N–terminal amino acid sequence. J. Mol. Biol. 300, 1005–1016 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank all the members of the Department of Molecular Evolution at Uppsala University for providing a stimulating atmosphere.

Author information

Authors and Affiliations

  1. Department of Molecular Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18C, Uppsala, 752 36, Sweden

    E. Olof L. Karlberg & Siv G. E. Andersson

Authors
  1. E. Olof L. Karlberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siv G. E. Andersson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siv G. E. Andersson.

Related links

Related links

DATABASES

LocusLink

Ant1

Ant2

cytochrome b

cytochrome c1

ND6

Rieske iron-sulphur protein

OMIM

Leigh syndrome

mitochondrial myopathy

myoclonic epilepsy

SwissProt

Adh1

ANT1

Tim9

Tim10

Tim17

Tim22

Tim23

Tom20

Tom22

Tom40

Tom70

FURTHER INFORMATION

Saccharomyces Genome Database

Glossary

ANAEROBE

An organism that can grow in an oxygen-free environment.

CYANOBACTERIA

Photosynthetic bacteria, formerly called blue-green algae.

ENDOSYMBIONT

An organism that grows inside the cell of another organism. The relationship can be either mutualistic (both species benefit) or commensalistic (one species benefits, whereas the other is not affected).

FACULTATIVE INTRACELLULAR PARASITE

A parasite that is capable of growing both inside and outside of the cells of the infected host.

HORIZONTAL TRANSFER

The transfer of genetic material among cells that belong to different strains, species or genera.

KRUSKAL-WALLIS NON-PARAMETRIC TEST

A statistical test that is used to assess whether two (or more) populations have the same mean and distribution.

MATURASES

Enzymes that are involved in removing introns from mRNA.

POLYSOME

(Polyribosome). Many ribosomes that are connected by an mRNA molecule.

PROTISTS

Unicellular eukaryotes including protozoans, slime molds and certain algae.

VERTICAL DESCENT

The transfer of genetic material from an ancestor to its offspring — for example, by cell division.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karlberg, E., Andersson, S. Mitochondrial gene history and mRNA localization: is there a correlation?. Nat Rev Genet 4, 391–397 (2003). https://doi.org/10.1038/nrg1063

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg1063

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing