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Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants

Nature volume 408, pages 354–357 (2000)Cite this article

Abstract

A central component of the endosymbiotic theory for the bacterial origin of the mitochondrion is that many of its genes were transferred to the nucleus. Most of this transfer occurred early in mitochondrial evolution1; functional transfer of mitochondrial genes has ceased in animals2. Although mitochondrial gene transfer continues to occur in plants3, no comprehensive study of the frequency and timing of transfers during plant evolution has been conducted. Here we report frequent loss (26 times) and transfer to the nucleus of the mitochondrial gene rps10 among 277 diverse angiosperms. Characterization of nuclear rps10 genes from 16 out of 26 loss lineages implies that many independent, RNA-mediated rps10 transfers occurred during recent angiosperm evolution; each of the genes may represent a separate functional gene transfer. Thus, rps10 has been transferred to the nucleus at a surprisingly high rate during angiosperm evolution. The structures of several nuclear rps10 genes reveal diverse mechanisms by which transferred genes become activated, including parasitism of pre-existing nuclear genes for mitochondrial or cytoplasmic proteins, and activation without gain of a mitochondrial targeting sequence.

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Figure 1: Southern blot hybridizations of 51 angiosperms (out of 277 examined in total) with the indicated angiosperm probes.
Figure 2: Sporadic loss of the mitochondrial rps10 gene among the surveyed angiosperms.
Figure 3: Partial sequence comparisons of three chimaeric nuclear rps10 genes and structures of seven nuclear rps10 genes.
Figure 4: Import of RPS10 proteins into isolated mitochondria.
Figure 5: Maximum likelihood trees of mitochondrial and nuclear rps10 nucleotide sequences.

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References

  1. Gray, M. W. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141, 233–357 (1992).

    Article  CAS  Google Scholar 

  2. Boore, J. L. Animal mitochondrial genomes. Nucleic Acids Res. 27 , 1767–1780 (1999).

    Article  CAS  Google Scholar 

  3. Adams, K. L. et al. Intracellular gene transfer in action: Dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc. Natl Acad. Sci. USA 96, 13863 –13868 (1999).

    Article  CAS  ADS  Google Scholar 

  4. Wolfe, K. H., Li, W. -H. & Sharp, P. M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl Acad. Sci. USA 84, 9054–9058 (1987).

    Article  CAS  ADS  Google Scholar 

  5. Laroche, J., Li, P., Maggia, L. & Bousquet, J. Molecular evolution of angiosperm mitochondrial exons and introns. Proc. Natl Acad. Sci. USA 94, 5722–5727 ( 1997).

    Article  CAS  ADS  Google Scholar 

  6. Kadowaki, K., Kubo, N., Ozawa, K. & Hirai, A. Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals. EMBO J. 15, 6652–6661 (1996).

    Article  CAS  Google Scholar 

  7. Figueroa, P., Gómez, I., Holuigue, L., Araya, A. & Jordana, X. Transfer of rps14 from the mitochondrion to the nucleus in maize implied integration within a gene encoding the iron-sulphur subunit of succinate dehydrogenase and expression by alternative splicing. Plant J. 18, 601– 609 (1999).

    Article  CAS  Google Scholar 

  8. Kubo, N., Harada, K., Hirai, A. & Kadowaki, K. A single nuclear transcript encoding mitochondrial RPS14 and SDHB of rice is processed by alternative splicing: Common use of the same mitochondrial targeting signal for different proteins. Proc. Natl Acad. Sci. USA 96, 9207–9211 (1999).

    Article  CAS  ADS  Google Scholar 

  9. Wischmann, C. & Schuster, W. Transfer of rps10 from the mitochondrion to the nucleus in Arabidopsis thaliana: evidence for RNA-mediated transfer and exon shuffling at the integration site. FEBS Lett. 375, 152–156 (1995).

    Article  Google Scholar 

  10. Kubo, N. et al. Transfer of the mitochondrial rps10 gene to the nucleus in rice: acquisition of the 5′ untranslated region followed by gene duplication. Mol. Gen. Genet. 263, 733– 739 (2000).

    Article  CAS  Google Scholar 

  11. Nakagawa, T., Maeshima, M., Nakamura, K. & Asahi, T. Molecular cloning of a cDNA for the smallest nuclear-encoded subunit of sweet potato cytochrome c oxidase. Eur. J. Biochem. 191, 557–561 (1990).

    Article  CAS  Google Scholar 

  12. Morikami, A., Ehara, G. & Yuuki, K. Molecular cloning and characterization of cDNAs for the γ-subunit and ε-subunit of mitochondrial F1F0 ATP synthase from sweet potato. J. Biol. Chem. 268, 17205–17210 (1993).

    CAS  PubMed  Google Scholar 

  13. Braun, H.-P., Jansch, L., Kruft, V. & Schmitz, U. K. The ‘Hinge’ protein of cytochrome c reductase from potato lacks the acidic domain and has no cleavable presequence. FEBS Lett. 347, 90–94 (1994).

    Article  CAS  Google Scholar 

  14. Long, M., de Souza, S. J., Rosenberg, C. & Gilbert, W. Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor. Proc. Natl Acad. Sci. USA 93, 7727–7731 (1996).

    Article  CAS  ADS  Google Scholar 

  15. Herrmann, R. G. in Eukaryotism and Symbiosis (eds Schenk, H. E. A. et al.) 73–118 (Springer, Vienna, 1997).

    Book  Google Scholar 

  16. Figueroa, P. et al. The gene for mitochondrial ribosomal protein S14 has been transferred to the nucleus in Arabidopsis thaliana. Mol. Gen. Genet. 262, 139–144 (1999).

    Article  CAS  Google Scholar 

  17. Bensasson, D., Zhang, D.-X. & Hewitt, G. M. Frequent assimilation of mitochondrial DNA by grasshopper nuclear genomes. Mol. Biol. Evol. 17, 406 –415 (2000).

    Article  CAS  Google Scholar 

  18. Palmer, J. D. The mitochondrion that time forgot. Science 275, 790–791 (1997).

    Article  CAS  Google Scholar 

  19. Martin, W. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162–165 (1998).

    Article  CAS  ADS  Google Scholar 

  20. Gray, M. W. Evolution of organellar genomes. Curr. Opin. Genet. Dev. 9, 678–687 (1999).

    Article  CAS  Google Scholar 

  21. Swofford, D. L. PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods) 4.0B3 edn (Sinauer Associates, Sunderland, MA, 2000).

    Google Scholar 

  22. Strimmer, K. & von Haeseler, A. Quartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969 (1996).

    Article  CAS  Google Scholar 

  23. Day, D. A., Neuburger, M. & Douce, R. Biochemical characterization of chlorophyll-free mitochondria from pea leaves. Aust. J. Plant Phys. 12, 219–228 (1985).

    CAS  Google Scholar 

  24. Neuberger, M., Journet, E., Bligny, R., Carde, J. & Douce, R. Purification of plant mitochondria by isopycnic centrifugation in density gradients of percoll. Arch. Biochem. Biophys. 217, 312–323 (1982).

    Article  Google Scholar 

  25. Tanudji, M., Sjoling, S., Glaser, E. & Whelan, J. Signals required for the import and processing of the alternative oxidase into mitochondria. J. Biol. Chem. 274, 1286– 1293 (1999).

    Article  CAS  Google Scholar 

  26. Knox, C., Sass, E., Neupert, W. & Pines, O. Import into mitochondria, folding, and retrograde movement of fumarase in yeast. J. Biol. Chem. 273, 25587–25593 ( 1998).

    Article  CAS  Google Scholar 

  27. Soltis, P. S., Soltis, D. E. & Chase, M. W. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402–404 (1999).

    Article  CAS  ADS  Google Scholar 

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Acknowledgements

We thank W. Fischer, J. Logsdon, C. Parkinson, M. Rosenblueth, N. Schisler and K. Wolfe for reading the manuscript, and D. Swofford for allowing us to use a pre-release version of PAUP*. This study was supported by a United States Department of Agriculture graduate fellowship to K.L.A., grants to Y.L.Q. and J.D.P. from the NIH, and grants from the Australian Research Council to J.W.

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Author notes

  1. Yin-Long Qiu

    Present address: Department of Biology, University of Massachusetts, Amherst, Massachusetts, 01003, USA

Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington, 47405, Indiana, USA

    Keith L. Adams, Yin-Long Qiu & Jeffrey D. Palmer

  2. Biochemistry Department, University of Western Australia, 6907, Nedlands, Australia

    Daniel O. Daley & James Whelan

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Correspondence to Jeffrey D. Palmer.

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Adams, K., Daley, D., Qiu, YL. et al. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 408, 354–357 (2000). https://doi.org/10.1038/35042567

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