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. 1996 Dec 2;15(23):6652–6661.

Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals.

K Kadowaki 1, N Kubo 1, K Ozawa 1, A Hirai 1
PMCID: PMC452489  PMID: 8978691

Abstract

We have cloned a gene for mitochondrial ribosomal protein S11 (RPS11), which is encoded in lower plants by the mitochondrial genome, in higher plants by the nuclear genome, demonstrating genetic information transfer from the mitochondrial genome to the nucleus during flowering plant evolution. The sequence s11-1 encodes an N-terminal extension as well as an organelle-derived RPS11 region. Surprisingly, the N-terminal region has high amino acid sequence similarity with the presequence of the beta-subunit of ATP synthase from plant mitochondria, suggesting a common lineage of the presequences. The deduced N-terminal region of s11-2, a second nuclear-encoded homolog of rps11, shows high sequence similarity with the putative presequence of cytochrome oxidase subunit Vb. The sharing of the N-terminal region together with its 5' flanking untranslated nucleotide sequence in different proteins strongly suggests an involvement of duplication/recombination for targeting signal acquisition after gene migration. A remnant of ancestral rps11 sequence, transcribed and subjected to RNA editing, is found in the mitochondrial genome, indicating that inactivation of mitochondrial rps11 gene expression was initiated at the translational level prior to termination of transcription.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Baker A., Schatz G. Sequences from a prokaryotic genome or the mouse dihydrofolate reductase gene can restore the import of a truncated precursor protein into yeast mitochondria. Proc Natl Acad Sci U S A. 1987 May;84(10):3117–3121. doi: 10.1073/pnas.84.10.3117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bedwell D., Davis G., Gosink M., Post L., Nomura M., Kestler H., Zengel J. M., Lindahl L. Nucleotide sequence of the alpha ribosomal protein operon of Escherichia coli. Nucleic Acids Res. 1985 Jun 11;13(11):3891–3903. doi: 10.1093/nar/13.11.3891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boutry M., Chua N. H. A nuclear gene encoding the beta subunit of the mitochondrial ATP synthase in Nicotiana plumbaginifolia. EMBO J. 1985 Sep;4(9):2159–2165. doi: 10.1002/j.1460-2075.1985.tb03910.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  6. Brennicke A., Grohmann L., Hiesel R., Knoop V., Schuster W. The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett. 1993 Jun 28;325(1-2):140–145. doi: 10.1016/0014-5793(93)81430-8. [DOI] [PubMed] [Google Scholar]
  7. Chye M. L., Tan C. T. Isolation and nucleotide sequence of a cDNA clone encoding the beta subunit of mitochondrial ATP synthase from Hevea brasiliensis. Plant Mol Biol. 1992 Feb;18(3):611–612. doi: 10.1007/BF00040680. [DOI] [PubMed] [Google Scholar]
  8. Covello P. S., Gray M. W. Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J. 1992 Nov;11(11):3815–3820. doi: 10.1002/j.1460-2075.1992.tb05473.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gay N. J., Walker J. E. Two genes encoding the bovine mitochondrial ATP synthase proteolipid specify precursors with different import sequences and are expressed in a tissue-specific manner. EMBO J. 1985 Dec 16;4(13A):3519–3524. doi: 10.1002/j.1460-2075.1985.tb04111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gray M. W. Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol. 1989;5:25–50. doi: 10.1146/annurev.cb.05.110189.000325. [DOI] [PubMed] [Google Scholar]
  11. Gray M. W. The endosymbiont hypothesis revisited. Int Rev Cytol. 1992;141:233–357. doi: 10.1016/s0074-7696(08)62068-9. [DOI] [PubMed] [Google Scholar]
  12. Grohmann L., Brennicke A., Schuster W. The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome in Oenothera. Nucleic Acids Res. 1992 Nov 11;20(21):5641–5646. doi: 10.1093/nar/20.21.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hartl F. U., Pfanner N., Nicholson D. W., Neupert W. Mitochondrial protein import. Biochim Biophys Acta. 1989 Jan 18;988(1):1–45. doi: 10.1016/0304-4157(89)90002-6. [DOI] [PubMed] [Google Scholar]
  14. Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet. 1989 Jun;217(2-3):185–194. doi: 10.1007/BF02464880. [DOI] [PubMed] [Google Scholar]
  15. Kubo N., Ozawa K., Hino T., Kadowaki K. A ribosomal protein L2 gene is transcribed, spliced, and edited at one site in rice mitochondria. Plant Mol Biol. 1996 Jul;31(4):853–862. doi: 10.1007/BF00019472. [DOI] [PubMed] [Google Scholar]
  16. Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
  17. Maarse A. C., Van Loon A. P., Riezman H., Gregor I., Schatz G., Grivell L. A. Subunit IV of yeast cytochrome c oxidase: cloning and nucleotide sequencing of the gene and partial amino acid sequencing of the mature protein. EMBO J. 1984 Dec 1;3(12):2831–2837. doi: 10.1002/j.1460-2075.1984.tb02216.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nugent J. M., Palmer J. D. RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell. 1991 Aug 9;66(3):473–481. doi: 10.1016/0092-8674(81)90011-8. [DOI] [PubMed] [Google Scholar]
  19. Oda K., Yamato K., Ohta E., Nakamura Y., Takemura M., Nozato N., Akashi K., Kanegae T., Ogura Y., Kohchi T. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol. 1992 Jan 5;223(1):1–7. doi: 10.1016/0022-2836(92)90708-r. [DOI] [PubMed] [Google Scholar]
  20. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sakamoto M., Shimada H., Fujimura T. Nucleotide sequence of a cDNA encoding a beta subunit of the mitochondrial ATPase from rice (Oryza sativa). Plant Mol Biol. 1992 Oct;20(1):171–174. doi: 10.1007/BF00029164. [DOI] [PubMed] [Google Scholar]
  22. Stern D. B., Newton K. J. Isolation of plant mitochondrial RNA. Methods Enzymol. 1986;118:488–496. doi: 10.1016/0076-6879(86)18095-5. [DOI] [PubMed] [Google Scholar]
  23. Takemura M., Oda K., Yamato K., Ohta E., Nakamura Y., Nozato N., Akashi K., Ohyama K. Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. Nucleic Acids Res. 1992 Jun 25;20(12):3199–3205. doi: 10.1093/nar/20.12.3199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tamm L. K. Membrane insertion and lateral mobility of synthetic amphiphilic signal peptides in lipid model membranes. Biochim Biophys Acta. 1991 Jul 22;1071(2):123–148. doi: 10.1016/0304-4157(91)90021-n. [DOI] [PubMed] [Google Scholar]
  25. Terpstra P., Zanders E., Butow R. A. The association of var1 with the 38 S mitochondrial ribosomal subunit in yeast. J Biol Chem. 1979 Dec 25;254(24):12653–12661. [PubMed] [Google Scholar]
  26. Vassarotti A., Stroud R., Douglas M. Independent mutations at the amino terminus of a protein act as surrogate signals for mitochondrial import. EMBO J. 1987 Mar;6(3):705–711. doi: 10.1002/j.1460-2075.1987.tb04811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Walbot V. RNA editing fixes problems in plant mitochondrial transcripts. Trends Genet. 1991 Feb;7(2):37–39. doi: 10.1016/0168-9525(91)90225-F. [DOI] [PubMed] [Google Scholar]
  28. Winning B. M., Bathgate B., Purdue P. E., Leaver C. J. Nucleotide sequence of a cDNA encoding the beta subunit of the mitochondrial ATP synthase from Zea mays. Nucleic Acids Res. 1990 Oct 11;18(19):5885–5885. doi: 10.1093/nar/18.19.5885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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. 1995 Oct 30;374(2):152–156. doi: 10.1016/0014-5793(95)01100-s. [DOI] [PubMed] [Google Scholar]
  30. Wolff G., Plante I., Lang B. F., Kück U., Burger G. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization. J Mol Biol. 1994 Mar 18;237(1):75–86. doi: 10.1006/jmbi.1994.1210. [DOI] [PubMed] [Google Scholar]
  31. Zeviani M., Sakoda S., Sherbany A. A., Nakase H., Rizzuto R., Samitt C. E., DiMauro S., Schon E. A. Sequence of cDNAs encoding subunit Vb of human and bovine cytochrome c oxidase. Gene. 1988 May 15;65(1):1–11. doi: 10.1016/0378-1119(88)90411-8. [DOI] [PubMed] [Google Scholar]

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