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Plant Molecular Biology

, Volume 45, Issue 3, pp 317–325 | Cite as

Protein import into plant mitochondria: precursor proteins differ in ATP and membrane potential requirements

  • Marcel Tanudji
  • Patrick Dessi
  • Monika Murcha
  • James Whelan
Article

Abstract

The import pathways of the alternative oxidase and the FAd subunit of the ATP synthase from soybean were characterised. The FAd precursor does not require extramitochondrial ATP for import and this was shown to be a characteristic of the mature protein. The alternative oxidase and FAd precursors were shown to differ in their requirement for a membrane potential. The membrane potential was modified using malonate, a competitive inhibitor to complex II. The alternative oxidase could be imported at higher malonate concentrations compared to the FAd. This difference could not be ascribed to the number of positive charges in each presequence as would be predicted from similar studies in fungi.

ATP energy requirements membrane potential mitochondrial protein import 

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References

  1. Adam, A., Endres, M., Sirrenberg, C., Lottspeich, F., Neupert, W. and Brunner, M. 1999.Tim9, a new component of the TIM22-54 translocase in mitochondria. EMBO J. 18: 313–319.Google Scholar
  2. Attimonelli, M., Altamura, N., Benne, R., Boyen, C., Brennicke, A. et al. 1999. Mitbase: a comprehensive and integrated mitochondrial DNA database. Nucl. Acids Res. 27: 128–133.Google Scholar
  3. Chaumont, F., Silva Filho, M.D.C., Thomas, D., Leterme, S. and Boutry, M. 1994. Truncated presequences of mitochondrial F1-ATPase β subunit from Nicotiana plumbaginifolia transport CAT and GUS proteins into mitochondria of transgenic tobacco. Plant Mol. Biol. 24: 631–641.Google Scholar
  4. Day, D.A., Neuburger, M. and Douce, R. 1985. Biochemical characterization of chlorophyll-free mitochondria from pea leaves. Aust. J. Plant Physiol. 12: 219–228.Google Scholar
  5. Dessi, P., Smith, M.K., Day, D.A. and Whelan, J. 1996. Characterization of the import pathway of the FA d subunit of mitochondrial ATP synthase into isolated plant mitochondria. Arch. Biochem. Biophys. 335: 358–368.Google Scholar
  6. Finnegan, P.M., Whelan, J., Millar, A.H., Zhang, Q., Smith, M.K., Wiskich, J.T. and Day, D.A. 1997. Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiol. 114: 455–466.Google Scholar
  7. Folsch, H., Gaume, B., Brunner, M., Neupert, M. and Stuart, R.A. 1998. C-to N-terminal translocation of preproteins into mitochondria. EMBO J. 17: 6508–6515.Google Scholar
  8. Glaser, E. and Dessi, P. 1999. Integration of the mitochondrial processing peptidase into the cytochrome bc1 complex in plants. J. Bioenerg. Biomembr. 31: 259–274.Google Scholar
  9. Glaser, E., Sjoling, S., Tanudji, M. and Whelan, J. 1998. Mitochondrial protein import in plants: signals, sorting, targeting, processing and regulation. Plant Mol. Biol. 38: 311–338.Google Scholar
  10. Hartl, F.U., Pfanner, N., Nicholson, D.W. and Neupert, W. 1989. Mitochondrial protein import. Biochim. Biophys. Acta 988: 1–45.Google Scholar
  11. Jansch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. 1996. New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J. 9: 357–368.Google Scholar
  12. Koehler, C.M., Merchant, S., Oppliger, W., Schmid, K., Jarosch, E., Dolfini, L., Junne, T., Schatz, G. and Tokatlidis, K. 1998. Tim9p, an essential partner subunit of Tim 10p for the import of mitochondrial carrier proteins. EMBO J. 17: 6477–6486.Google Scholar
  13. Lain, B., Iriarte, A. and Martinez-Carrion, M. 1994. Dependence of the folding and import of the precursor to mitochondrial aspartate aminotransferase on the nature of the cell-free translation system. J. Biol. Chem. 269: 15588–15596.Google Scholar
  14. Martin, J., Mahlke, K. and Pfanner, N. 1991. Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences. J. Biol. Chem. 266: 18051–18057.Google Scholar
  15. Millar, A.H., Atkin, O.K., Lambers, H., Wiskich, J.T. and Day, D.A. 1995. A critique of the use of inhibitors to estimate partitioning of electrons between mitochondrial respiratory pathways in plants. Physiol. Plant. 95: 523–532.Google Scholar
  16. Nett, J.H., Schagger, H. and Trumpower, B.L. 1998. Processing of the presequence of the Schizosaccharomyces pombe Rieske iron-sulfur protein occurs in a single step and can be converted to two-step processing by mutation of a single proline to serine in the presequence.J. Biol. Chem. 273: 8652–8658.Google Scholar
  17. Neupert, W. 1997. Protein import into mitochondria. Annu. Rev. Biochem. 66: 863–917.Google Scholar
  18. Pfanner, N., Craig, E.A. and Honlinger, A. 1997. Mitochondrial preprotein translocase. Annu. Rev. Cell Devel. Biol. 13: 25–51.Google Scholar
  19. Rojo, E.E., Guiard, B., Neupert, W. and Stuart, R.A. 1998. Sorting of D-lactate dehydrogenase to the inner membrane of mitochondria. J. Biol. Chem. 273: 8040–8047.Google Scholar
  20. Siedow, J.N. and Umbach, A.L. 1995. Plant mitochondrial electron transfer and molecular biology.Plant Cell 7: 821–831.Google Scholar
  21. Smith, M.K., Day, D.A. and Whelan, J. 1994. Isolation of a novel soybean gene encoding a mitochondrial ATP synthase subunit. Arch. Biochem. Biophys. 313: 235–240.Google Scholar
  22. Straffon, A.F.L., Prescott, M., Nagley, P. and Devenish, R.J. 1998. The assembly of yeast mitochondrial ATP synthase: subunit depletion in vivo suggests ordered assembly of the stalk subunits b, OSCP and d. Biochim. Biophys. Acta 1371: 157–162.Google Scholar
  23. Sztul, E.S., Hendrick, J.P., Kraus, J.P., Wall, D., Kalousek, F. and Rosenberg, L.E. 1987. Import of rat ornithine transcarbamylase precursor into mitochondria: two-step processing of the leader peptide. J. Cell Biol. 105: 2631–2640.Google Scholar
  24. Tanudji, M., Djajanegara, I.N., Daley, D.O., McCabe, T.C., Finnegan, P.M., Day, D.A. and Whelan, J. 1999a. The multiple alternative oxidase proteins of soybean. Aust. J. Plant Physiol. 26: 337–344.Google Scholar
  25. Tanudji, M., Sjoling, S., Glaser, E. and Whelan, J. 1999b. Signals required for the import and processing of the alternative oxidase into mitochondria. J. Biol. Chem. 274: 1286–1293Google Scholar
  26. Wachter, C., Schatz, G. and Glick, B.S. 1994. Protein import into mitochondria: the requirement for external ATP is precursor-specific whereas intramitochondrial ATP is universally needed for translocation into the matrix. Mol. Biol. Cell 5: 465–474.Google Scholar
  27. Whelan, J., McIntosh, L. and Day, D.A. 1993. Sequencing of a soybean alternative oxidase cDNA clone. Plant Physiol. 103: 1481.Google Scholar
  28. Whelan, J., Tanudji, M.R., Smith, M.K. and Day, D.A. 1996. Evidence for a link between translocation and processing during protein import into soybean mitochondria. Biochim. Biophys. Acta 1312: 48–54.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Marcel Tanudji
    • 1
  • Patrick Dessi
    • 1
  • Monika Murcha
    • 1
  • James Whelan
    • 1
  1. 1.Department of BiochemistryUniversity of Western AustraliaNedlandsAustralia

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