Skip to main content
SpringerLink
Log in
Book cover

Protein Trafficking in Plant Cells pp 311–338Cite as

Mitochondrial protein import in plants

Signals, Sorting, Targeting, Processing and Regulation

  • Chapter

Abstract

Mitochondrial biogenesis requires a coordinated expression of both the nuclear and the organellar genomes and specific intracellular protein trafficking, processing and assembly machinery. Most mitochondrial proteins are synthesised as precursor proteins containing an N-terminal extension which functions as a targeting signal, which is proteolytically cleaved off after import into mitochondria. We review our present knowledge on components and mechanisms involved in the mitochondrial protein import process in plants. This encompasses properties of targeting peptides, sorting of precursor proteins between mitochondria and chloroplasts, signal recognition, mechanism of translocation across the mitochondrial membranes and the role of cytosolic and organellar molecular chaperones in this process. The mitochondrial protein processing in plants is catalysed by the mitochondrial processing peptidase (MPP), which in contrast to other sources, is integrated into the bc1 complex of the respiratory chain. This is the most studied component of the plant import machinery characterised to date. What are the biochemical consequences of the integration of the MPP into an oligomeric protein complex and how are several hundred presequences of precursor proteins with no sequence similarities and no consensus for cleavage, specifically cleaved off by MPP? Finally we will address the emerging area of the control of protein import into mitochondria.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anastasi A, Knight CG, Barret AJ: Characterisation of the bacterial metalloendopeptidase pitrilysin by use of a continuous fluorsenecence assay. Biochem J 290: 601–607 (1993).

    PubMed  CAS  Google Scholar 

  2. Attardi G, Schatz G: Biogenesis of mitochondria: Assembly of the mitochondrial membrane systems. Ann Rev Cell Biol 4:289–333 (1988).

    Article  PubMed  CAS  Google Scholar 

  3. Atteia A, LGF: Identification of cDNA sequence and deduced amino acid sequence of the mitochondrial Rieske iron-sulfur protein from the green alga Chlamydomonas reinhardtii. Implications for protein targeting and subunit interaction. Eur J Biochem 237(3): 792–799 (1996).

    Article  PubMed  CAS  Google Scholar 

  4. Auld DS: Removal and replacement of metal ions in met-allopeptidase. In: Barret AJ (ed)’ Proteolytic enzymes: As-partic and Metallopeptidase’, pp. 228–242. Academic Press, New York (1995).

    Chapter  Google Scholar 

  5. Baker A, Leaver CJ: Isolation and sequence analysis of a cDNA encoding the ATP/ADP translocator of Zea mays L. Nucl. Acid Res 13: 5857–5867 (1985).

    Article  CAS  Google Scholar 

  6. Bauer MF, Sirrenberg C, Neupert W, Brunner M: Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria. Cell 87: 33–41 (1996).

    Article  PubMed  CAS  Google Scholar 

  7. Becker AB: An unusal active site identified in a family of zinc metalloendopeptidase. Proc Natl Acad Sci USA 88: 3835–3839 (1992).

    Article  Google Scholar 

  8. Becker AB, Roth RA: Insulysin and pitrilysin: insulin-degrading enzymes of mammals andbacteria. Methods En-zymol 248: 693–703 (1993).

    Google Scholar 

  9. Becker AB, Roth RA: Identification of glutamate-169 as the binding third zinc-residue in proteinase III, a member of the familiy of insulin-degrading enzymes. Biochem J 292:137–142 (1993).

    PubMed  CAS  Google Scholar 

  10. Bedwell D M, Strobel SA, Yun K, Jongeward GD, Emr SD: Sequence and structural requirements of a mitochondrial protein import signal defined by saturation cassette mutagenesis. Mol Cell Biol 9: 1014–1025 (1989).

    PubMed  CAS  Google Scholar 

  11. Berry EA, Huang L-S, DeRose VJ: Ubiquinol-cytochrome c oxidoreductase of higer plants. J Biol Chem 266: 9064–9077 (1991).

    PubMed  CAS  Google Scholar 

  12. Boemer U, Pfanner N, Dietmeier K: Identification of a third yeast mitochondrial Tom protein with tetratrico peptide repeats. FEBS Lett 382: 153–158 (1996).

    Article  Google Scholar 

  13. Bomer U, Rassow J, Zufall N, Pfanner N, Meijer M, Maarse AC: The preprotein translocase of the inner mitochondrial membrane: Evolutionary conservation of targeting and assembly of Timl7. J Mol Biol 262: 389–395 (1996).

    Article  PubMed  CAS  Google Scholar 

  14. Bohni PC, Daum G, Schatz G: Import of proteins into mitochondria: Partial purification of matrix-located protease involved in cleavage of mitochondrial precursor polypeptides. J Biol Chem 258: 4937–4943 (1983).

    PubMed  CAS  Google Scholar 

  15. Boumans H: The bc1 complex of the respiratory chain of Saccharomyces cerevisiae. Ph.D. thesis, University of Amsterdam (1997).

    Google Scholar 

  16. Bourguinon J, Vauclare P, Merand V, Forest E, Neuburger M, Douce R: Glycine decarboxylase complex from higher plants: Molecular cloning, tissue distribution and mass spectrometry analysis of the T-protein. Eur J Biochem 217: 377–386 (1993).

    Article  Google Scholar 

  17. Boutry M, Chua N-H: A nuclear gene encoding the beta subunit of the mitochondrial ATPsynthase in Nicotiana plumbaginifolia. EMBO J 4: 2159–2165 (1985).

    PubMed  CAS  Google Scholar 

  18. Boutry M, Nagy F, Poulsen C, Aoyagi K, Chua NH: Targeting of bacterial chloramphenicol acetyltransferase to mitochondria in transgenic plants. Nature 328: 340–342 (1987).

    Article  PubMed  CAS  Google Scholar 

  19. Bowler C, Alliotte T, DeLoose M, Van Montagu M, Inze D: The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J 8: 31–38 (1989).

    PubMed  CAS  Google Scholar 

  20. Braun H-P, Emmerman M, Kruft V, Schmitz UK. Cytochrome c1 from potato: a protein with a presequence for targeting to the mitochondrial intermembrane space. Mol Gen Genet 231: 217–225 (1992).

    PubMed  CAS  Google Scholar 

  21. Braun H-P, Emmerman M, Kruft V, Schmitz UK: The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J 11: 3219–3227 (1992).

    PubMed  CAS  Google Scholar 

  22. Braun H-P, Jansch L, Kruft V, Schmitz UK: 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  PubMed  CAS  Google Scholar 

  23. Braun H-P, Kruft V, Schmitz UK: Primary structure, cell-free synthesis and mitochondrial targeting of the 8.2 kDa protein of cytochrome c reductase from potato. Biochim et Biophys Acta 1188: 367–372 (1994).

    Article  Google Scholar 

  24. Braun H-P, Schmitz, UK: Molecular features and mitochondrial import pathway of the 14-Kilodalton subunit of cytochrome c reductase from potato. Plant Physiol 107: 1217–1223 (1995).

    Article  PubMed  CAS  Google Scholar 

  25. Braun H-P, Schmitz UK: Molecular structure of the 8.0 kDa sunubit of cytochrome c reductase from potato and its DY-dependent import into isolated mitochondria. Biochim Biophys Acta 1229: 181–186 (1995).

    Article  PubMed  Google Scholar 

  26. Braun HP et al.: The general mitochondrial processing peptidase from wheat is integrated into the cytochrome be1-complex of the respiratory chain. Planta 195: 396–402 (1995).

    Article  PubMed  CAS  Google Scholar 

  27. Braun HP, Schmitz UK: Are the’ core’ proteins of the mitochondrial bc1 complex evolutionary relics of a processing protease. Trends Biochem Sci 20: 171–175 (1995).

    Article  PubMed  CAS  Google Scholar 

  28. Brink S, Flugge U-I, Chaumont F, Boutry M, Emmermann M, Schmitz UK, Flügge UF: Preproteins of chloroplast envelope inner membrane contain targeting information for receptor-dependent import into fungal mitochondria. J Biol Chem 269: 16478–85 (1994).

    PubMed  CAS  Google Scholar 

  29. Carfi A, Pares S, Duée E, GAlleni M, Duez C, Frére JM, Dideberg O: The 3-D structure of a zinc metallo-b-Lactamse from Bacillus cereus reveals a new type of protein fold. EMBO J 14: 4914–4921 (1995).

    PubMed  CAS  Google Scholar 

  30. Chaumont F, Bernier B, Buxant R, Williams ME, Levings III, CS, Boutry M: Targeting the maize T-urfl 3 product into tobacco mitochondria confers methomyl sensitivity to mitochondrial respiration. Proc Natl Acad Sci USA 92: 1167–1171 (19??).

    Google Scholar 

  31. Chaumont F, O’Riordan V, Boutry M: Protein transport into mitochondria is conserved between plant and yeast species. J Biol Chem 265: 16856–16862 (1990).

    PubMed  CAS  Google Scholar 

  32. Chaumont F, deCastro Silva Filho M, Thomas D, Leterme S, Boutry M: Truncated presequences of mitochondrial F1-ATPase beta subunit from Nicotiana plumbaginifolia transport CAT and GUS proteins into mitochondria of transgenic tobacco. Plant Mol Biol 24: 631–641 (1994).

    Article  PubMed  CAS  Google Scholar 

  33. 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 18: 611–612 (1992).

    Article  PubMed  CAS  Google Scholar 

  34. Cognata UL, Lanschutze V, Willmitzer L, Muller-Rober B: Structure and expression of mitochondrial citrate synthase from higher plants. Plant Cell Physiol 37: 1022–1029 (1996).

    Article  PubMed  Google Scholar 

  35. Cohen P, Pierotti AR, Chesneau V, Foulon T, PA: N-Arginine dibasic convertase. Methods Enzym 248: 703–716 (1995).

    Article  CAS  Google Scholar 

  36. Covello PS, Gray MW: Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11:3815–3820 (1992).

    PubMed  CAS  Google Scholar 

  37. Criessen G, Edwards EA, Enard C, Welburn A, Mullineaux, P: Molecular characterisation of glutathionine reductase cD-NAs from pea (Pisum sativum L.). Plant J 2: 129–131 (1992).

    Google Scholar 

  38. Cruz-Hernandez A, Gomez-Lim MA: Alternative oxidase from mango (Mangifera indica L. is differentially regulated during fruit ripening. Planta 197: 569–576 (1995).

    Article  PubMed  CAS  Google Scholar 

  39. Cui J-Y, Mukai K, Seaki K, Matsubara H: Molecular cloning and nucleotide sequence of cDNAs encoding subunits I, II and IX of Euglena gracilis mitochondrial complex III. J Biochem 115:98–107 (1994).

    PubMed  CAS  Google Scholar 

  40. Cui X, Wise RP, Schnable PS: The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272: 1334–1336 (1996).

    Article  PubMed  CAS  Google Scholar 

  41. Cunillera N, Boronat A, Ferrer A: The Arabidopsis thaliana FPSlgene generrates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272: 15381–15388 (1997).

    Article  PubMed  CAS  Google Scholar 

  42. Dahlin C, Cline K: Developmental regulation of the plastid protein import apparatus.Plant Cell 3: 1131–1140 (1991).

    PubMed  CAS  Google Scholar 

  43. Dessi P: The characterisation of protein import pathways in plant mitochondria. Ph. D. thesis, University of Western Australia (submitted) (1998).

    Google Scholar 

  44. Dessi P, Smith MK, Day DA, Whelan J: Characterization of the import pathway of the FAd subunit of mitochondrial ATP synthase into isolated plant mitochondria. Arc Biochem Biophys 335: 358–368 (1996).

    Article  CAS  Google Scholar 

  45. Dessi P, Whelan J: Temporal regulation of in vitro import of precursor proteins into tobacco mitochondria. FEBS Lett 415: 173–178 (1997).

    Article  PubMed  CAS  Google Scholar 

  46. Dong JZ, Dunstan DI: Characterization of three heat shock protein genes and their developmental regulation during somatic embryogenesis in white spruce (Picea glauca). Planta 200: 85–91 (1996).

    Article  PubMed  CAS  Google Scholar 

  47. Doolittle RF: Similar amino acid sequences: chance or commmon ancestory? Science 214: 149–159 (1981).

    Article  PubMed  CAS  Google Scholar 

  48. Douce R: Mitochondria in higher plants-structure, function and biogenesis. Academic Press, London (1985).

    Google Scholar 

  49. Dudley P, Wood CK, Pratt AL, Moore AL: Developmental regulation of the plant mitochondrial matrix located hsp70 chaperone and its role in protein import. FEBS Lett 417: 321–324 (1997).

    Article  PubMed  CAS  Google Scholar 

  50. Emmerman M, Braun H-P, Schmitz UK: The ADP/ATP translocator from potato has a long N-terminal extension. Curr. Genet. 20: 405–410 (1991).

    Article  Google Scholar 

  51. Emmerman M, Braun H-P, Schmitz UK: Characterisation of the bifunctional cytochrome c reductase processing peptidase complex from potato mitochondria. J Biol Chem 268: 18936–18942 (1993).

    Google Scholar 

  52. Emmerman M, Braun H-P, Schmitz UK: The mitochondrial processing peptidase from potato: a self-processing enzyme encoded by two differentially expressed genes. Mol Gen Genet 245: 237–245 (1994).

    Article  Google Scholar 

  53. Emmerman M, Braun H-P, Schmitz UK: Characterization of the bifunctional cytochrome c reductase-processing peptidase complex from potato mitochondria. J Biol Chem 268: 18936–18942 (1993).

    Google Scholar 

  54. Emmermann M, Braun HP, Schmitz UK: The two high molecular weight subunits of cytochrome C reductase from potato are immunologically related to the mitochondrial processing enhancing protein, biochim. biophys. Acta 1142: 306–310 (1993).

    CAS  Google Scholar 

  55. Emmermann M, Braun HP, Schmitz UK: The mitochondrial processing peptidase from potato: A self-processing enzyme encoded by two differentially expressed genes. Mol Gen Gen 245: 237–245 (1994).

    CAS  Google Scholar 

  56. Eriksson A, Sjoling S, Glaser E: The ubiquinol cytochrome c oxidoreductase complex of spinach leaf mitochondria is involved in both respiration and protein processing. Biochim Biophys Acta 1186: 221–231 (1994).

    Article  CAS  Google Scholar 

  57. Eriksson, A, Sjoling S, Glaser E.: Characterization of the bifunctional mitochondrial processing peptidase (MPP)/bc-1 complex in Spinacia oleracea. J Bioenerg Biomem 28: 285–292 (1995).

    Article  Google Scholar 

  58. Eriksson AC: Functional and structural studies on the integral mitochondrial processing peptidase/bc1 complex from Spinacia oleracea. Ph.D. thesis, Stockholm University (1996).

    Google Scholar 

  59. Eriksson AC, Sjoling S, Glaser E.: Molecular, biochemical and physiological aspects of plant respiration. In: Lambers H, Van der Plas LHW (eds) pp. 299–306 SPB Academic Publishing bv The Hague. (1992).

    Google Scholar 

  60. Eriksson AC, Sjoling S, Glaser E: A general processing proteinase of spinach leaf mitochondria is involved in both respiration and protein processing. In: Brennike AK, (ed) Plant Mitochondria., VCH Verlags (1993).

    Google Scholar 

  61. Filipowicz W, Hohn T.: Post transcriptional control of gene expression in plants. Plant Mol Biol 32 (1996).

    Google Scholar 

  62. Finnegan PM, Whelan J, Millar AH, Zhang Q, Smith MK, Wiskich JT, Day DA: Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase.Plant Physiol 114: 455–466 (1997).

    Article  PubMed  CAS  Google Scholar 

  63. Franzen L-G, Rochaix J-D, Von Heijne G: Chloroplast transit peptides from the green algae Chlamydomonas reinhardtii share features with both mitochondrial and higher plant chloroplast presequences. FEBS Lett 260: 165–168 (1990).

    Article  PubMed  CAS  Google Scholar 

  64. Gavel Y, Von Heijne G: Cleavage-site motifs in mitochondrial targeting peptides. Protein Engineering 4: 33–38 (1990).

    Article  PubMed  CAS  Google Scholar 

  65. Gietl C, Lehnerer M, Olsen O.: Mitochondrial malate dehydrogenase from watermelon:sequence of cDNA clones and primary structure of the higher-plant precursor protein. Plant Mol Biol 14: 1019–1030 (1990).

    Article  PubMed  CAS  Google Scholar 

  66. Glaser E, Eriksson A, Sjoling S: Bifunctional role of the bc1complex in plants: Mitochondrial bc1 complex catalyses both electron transport and protein processing. FEBSLett. 346: 83–87 (1994).

    Article  CAS  Google Scholar 

  67. Glick B, Schatz G.: Import of proteins into mitochondria. Annu Rev Genet 25: 21–44 (1991).

    Article  PubMed  CAS  Google Scholar 

  68. Gray MW: Origin and evolution of organelle genomes. Curr Opinions Genet Develop 3: 884–890 (1993).

    Article  CAS  Google Scholar 

  69. Grof CPL et al.: Mitochondrial pyruvate dehydrogenase: Molecular cloning of the Ela subunit and expression analysis. Plant Physiol 108:1623–1629 (1995).

    Article  PubMed  CAS  Google Scholar 

  70. Grohmann L, Rasmusson AG, Heiser VL, Thieck O, Brennicke A: The NADH-binding subunit of the respiratory chain complex I is nuclear encoded in plants and identified only in mitochondria. Plant J 10: 793–803 (1996).

    Article  PubMed  CAS  Google Scholar 

  71. Gruhler A, et al.: N-terminal hydrophobic sorting signals of preproteins confer mitochondrial Hsp70 independence for import into mitochondria. J Biol Chem 272: 17410–17415 (1997).

    Article  PubMed  CAS  Google Scholar 

  72. Hachiya N, Alam R, Sakasegawa Y, Sakaguchi M, Mihara K., Omura, T: A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator forprecursor proteins. EMBO J 12: 1579–1586 (1993).

    PubMed  CAS  Google Scholar 

  73. Hachiya N, Komiya T, Alam R, Iwahashi J, Sakaguchi M, Omura T, Mihara, K: MSF, anovel cytoplasmic chaper-one which functions in precursor targeting to mitochondria. EMBO J13: 5146–5154 (1994).

    PubMed  CAS  Google Scholar 

  74. Hachiya N, Mihara K, Suda K, Horst M, Schatz G, Lithgow T: Reconstitution of the initial steps of mitochondrial protein import. Nature 376: 705–709 (1995).

    Article  PubMed  CAS  Google Scholar 

  75. Hallermayer G, Zimmermann R, Neupert W: Kinetic studies on the transport of cytoplasmically synthesized proteins into the mitochondria in intact cells of Neurospora crassa. Eur J Biochem 81: 523–532 (1977).

    Article  PubMed  CAS  Google Scholar 

  76. Hammen PK, Waltner M, Hahnemann B, Heard TS, Weiner H.: The role of positive charges and structural segments in the presequence of rat liver aldehyde dehydrogenase in import into mitochondria. J Biol Chem 271: 21041–21048 (1996).

    Article  PubMed  CAS  Google Scholar 

  77. Hartl F-U, Pfanner N, Nicholson DW and Neupert W: Mitochondrial protein import. Biochim Biophys Acta 988(1): 1–45 (1989).

    Article  PubMed  CAS  Google Scholar 

  78. Hashimoto H, Nishi R, Umeda M, Uchimiya H, Kato A: Isolation and characterisation of a rice cDNA clone encoding ATP/ADP translocator. Plant Mol Biol 22: 163–164 (1993).

    Article  PubMed  CAS  Google Scholar 

  79. Hawlitschek G, Schneider H, Schmidt B, Tropschug M, Hartl F-U, Neupert W: Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancingprotein. Cell 53: 795–806 (1988).

    Article  PubMed  CAS  Google Scholar 

  80. Hay den C, Harmey MA: Matrix protease of Vicia faba mitochondria. In: Lambers H, Van der Plas LHW (eds) Molecular, biochemical and physiological aspects of plantrespiration., SPB Publishing, The Hague, pp. 413–418 (1992).

    Google Scholar 

  81. Heins L, Schmitz UK: A receptor for protein import into potato mitochondria. Plant J 9: 829–839 (1996).

    Article  PubMed  CAS  Google Scholar 

  82. Heiser V, Brennicke A, Grohmann L: The plant mitochondrial 22 KDa (PSST) subunit of respiratory chain complex I is encoded by a nuclear gene with enhanced transcript levels in flowers. Plant Mol Biol 31:1195–1204 (1996).

    Article  PubMed  CAS  Google Scholar 

  83. Hemon P, Robbins MP, Cullimore JV: Targeting of gluthamine synthetase to the mitochondria of transgenic tobacco. Plant Mol Biol 15: 895–904 (1993).

    Article  Google Scholar 

  84. Hendrick JP, Hodges PE, and Rosenberg LE: Survey of amino-terminal proteolytic cleavage sites in mitochondrial precursor proteins leader peptides cleaved by two matrix proteases share a three-amino acid motif. Proc Natl Acad Sci USA 86: 4056–4060 (1989).

    Article  PubMed  CAS  Google Scholar 

  85. Hiser C, Kapranov P, Mcintosh L: Genetic modification of respiratory capacity in potato. Plant Physiol 110: 277–286 (1996).

    Article  PubMed  CAS  Google Scholar 

  86. Horst M, Azem A, Schatz G, Glick BS: What is the driving force for protein import into mitochondria? Biochim Biophys Acta 1318: 71–78 (1997).

    Article  PubMed  CAS  Google Scholar 

  87. Horwich AL, Kalousek F, Fenton WA, Pollock RA, Rosenberg LE: Targeting of pre-ornithine transcarbamylase to mitochondria definition of critical regions and residues in the leader peptide. Cell 44: 451–460 (1986).

    Article  PubMed  CAS  Google Scholar 

  88. Horwich AL, Kalousek F, Rosenberg LE: Arginine in the leader peptide is required for both import and proteolytic cleavage of a mitochondrial precursor. Proc Natl Acad Sci USA 82: 4930–4933 (1985).

    Article  PubMed  CAS  Google Scholar 

  89. Huang J, Struck F, Matzinger DF, Levings CSI: Flower-enhanced expression of a nuclear-encoded mitochondrial respiratory protein is associated with changes in mitochondrion number. Plant Cell 6: 439–448 (1994).

    PubMed  CAS  Google Scholar 

  90. Huang JT, Struck F, Matzinger DF, Levings CSI: Functional analysis in yeast of cDNAcoding for the mitochondrial Rieske iron-sulfur protein of higher plants. Proc Natl Acad Sci USA 88: 10716–10720 (1991).

    Article  PubMed  CAS  Google Scholar 

  91. Hugosson M, Boman H, Glaser E: Antibacterial peptides and mitochondrial presequences affect mitochondrial coupling, respiration and protein import. Eur J Biochem 223: 1027–1033 (1994).

    Article  PubMed  CAS  Google Scholar 

  92. Hugosson M, Nurani G, Glaser E, Franzén LG: Peculiar properties of the PsaF photosystem I protein from the green alga Chlamydomonas reinhardtii: Presequence independent import of the PsaF protein into both chloroplasts and mitochondria. Plant Mol Biol 28: 525–535 (1995).

    Article  PubMed  CAS  Google Scholar 

  93. Hurt EC, Allison DS, Müller U, Schatz G: Amino-terminal deletions in the presequence of an imported mitochondrial protein block the targeting fnction and poteolytic ceavage o the pesequence a the crboxyl-trminus. J Biol Chem 262: 1420–1424 (1987).

    PubMed  CAS  Google Scholar 

  94. Hurt EC, Soltanifar N, Goldschmidt-Clermont M, Rochaix J-D, Schatz G: The cleavable pre-sequence of an imported chloroplast protein directs attached polypeptides into yeast mitochondria. EMBO J 5: 1343–1350 (1986).

    PubMed  CAS  Google Scholar 

  95. Iacobazzi V, Palmieri F: Nucleotide sequence of a cDNA encoding the ADP/ATP carrier from wheat (Triticum turgidum). Plant Physiol 107: 1473 (1995).

    Article  PubMed  CAS  Google Scholar 

  96. Jansch L, Kruft V, Schmitz UK, Braun H-P: Cytochrome c reductase from potato does not comprise three core proteins but contain an additional low molecular mass subunit. Eur J Biochem 228: 878–885 (1995).

    Article  PubMed  CAS  Google Scholar 

  97. Kadokawi 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).

    Google Scholar 

  98. Kim Y., Oliver DJ: Molecular cloning, transcriptional characterisation and sequencing of cDNA encoding the H-protein of the mitochondrial glycine decarboxylase complex in peas. J Biol Chem 265: 848–853 (1990).

    PubMed  CAS  Google Scholar 

  99. Kimura T, Takeda S, Asahi T, Nakamura K: Primary structure of a precursor for the d-subunit of sweet potato mitochondrial F1-ATPase deduced from full length cDNA. J Biol Chem 265: 6079–6085 (1990).

    PubMed  CAS  Google Scholar 

  100. Kimura T, Takeda S, Kyozuka J, Asahi T, Shimamoto K, Nakamura K: The presequenceof a precursor for the d-subunit of sweet potato mitochondrial F1ATPase is not sufficient for the transport of b-glucuronidase (GUS) into mitochondria in tobacco, rice and yeast cells. Plant Cell Physiol 34: 345–355 (1993).

    PubMed  CAS  Google Scholar 

  101. Knack G, Kloppstech K: cDNA sequence of a heat-inducible protein of chenopodium sharing homology with other heat-shock proteins. Nucl Acids Res 17: 5380 (1989).

    Article  PubMed  CAS  Google Scholar 

  102. Knorpp C, Hugosson M, Sjoling S, Eriksson AC, Glaser, E: Tissue-specific differences of the mitochondrial protein import machinery: In vitro import, process and degradation of the pre-F-1-beta subunit of the ATP synthase in spinach leaf and root mitochondria. Plant Mol Biol 26: 571–579 (1994).

    Article  PubMed  CAS  Google Scholar 

  103. Knorpp C, Szigyarto C, Glaser E: Evidence for a novel ATP-dependent membrane-associated protease in spinach leaf mitochondria. Biochem J 310: 527–531 (1995).

    PubMed  CAS  Google Scholar 

  104. Komiya, T, Sakaguchi, M, Mihara K: Cytoplasmic chaper-ones determine the targeting pathway of precursor proteins to mitochondria. EMBO J 15: 399–407 (1996).

    PubMed  CAS  Google Scholar 

  105. Kopriva S, Bauwe H: P-protein of Glycine decarboxylase from Flaveria pringlei. Plant Physiol 104: 1079–1080 (1994).

    Article  PubMed  CAS  Google Scholar 

  106. Kopriva S, Bauwe H: T-protein of glycine decarboxylase from Solanum tuberosum. Plant Physiol 104: 1079–1080 (1994).

    Article  PubMed  CAS  Google Scholar 

  107. Kopriva S, Bauwe H: Serine hydroxymethyltransferase from Solanum tuberosum. Plant Physiol 107: 271–272 (1995).

    Article  PubMed  CAS  Google Scholar 

  108. Kopriva S, Turner SR, Rawsthorne S, Bauwe H: T-protein of the glycine decarboxylase multienzyme complex: evidence for partial similarity to formyltetrahydrofolate synthetase. Plant Mol Biol 27: 1215–1220 (1995).

    Article  PubMed  CAS  Google Scholar 

  109. Kraus JP, Hodges PE, Williamson CL, Horwich AL, Kalousek F, Williams KR, Rosenberg LE: A cDNA clone for the precursor of rat mitochondrial ornithine transcarbamy-lase: comparison of rat and human leader sequences and conservation of catalytic sites. Nucl Acid Res 13: 943–52 (1985).

    Article  CAS  Google Scholar 

  110. Kulhman P, Palmer JD: Isolation, expression and evolution of the gene encoding mitochondrial elongation factor Tu in Arabidopsis thaliana. Plant Mol Biol 29: 1057–1070 (1985).

    Article  Google Scholar 

  111. Kumar AM and Soll D: Arabidopsis alternative oxidase sustains Eschericia coli respiration. Proc Natl Acad Sci USA 89: 10842–10846 (199

    Article  PubMed  CAS  Google Scholar 

  112. Lafayette PR, Nagao RT, O’Grady K, Vierling E, Key JL. Molecular characterisation of cDNA encoding low-molecular-weight shock protein of soybean. Plant Mol Biol 30: 159–169 (1996).

    Article  PubMed  CAS  Google Scholar 

  113. Laloi, M, Klein, M, Riesmeier, JW, and Muller-Rober, B: A plant cold-induced uncoupler protein. Nature 389: 135–136 (1997).

    Article  PubMed  CAS  Google Scholar 

  114. Landschutze, V, Muller-Rober B, and Willmitzer L: Mitochondrial citrate synthase from potato predominant expression in mature leaves and young flower buds. Planta 196: 756–764 (1995).

    Article  PubMed  CAS  Google Scholar 

  115. Larsen KS, Auld DS: Characterisation of an inhibitory metal binding site in carboxypeptidase A. Biochemistry 30: 2613–2618 (1991).

    Article  PubMed  CAS  Google Scholar 

  116. Lenne C, Block MA, Garin J, Douce R: Sequence and expression of the mRNA encoding HSP22, the mitochondrial small heat-shock protein in pea leaves. Biochem J 311: 80–813 (1995).

    Google Scholar 

  117. Lermontova I, KE, Mock H-P, Grimm B: Cloning and characterisation of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci USA 94: 8895–8900 (1997).

    Article  PubMed  CAS  Google Scholar 

  118. Lill R, Nargang FE, Neupert W: Biogenesis of mitochondrial proteins. Curr Opinion Cell Biol 8: 505–512 (1996).

    Article  PubMed  CAS  Google Scholar 

  119. Lin C-T, Lin M-T, Shaw J-F: Cloning and characterisation of a cDNA for manganese superoxidase dismutase. J Agric Food Chem 45: 521–525 (1997).

    Article  CAS  Google Scholar 

  120. Lithgow T, Cuezva JM, Silver PA: Highways for protein delivery to the mitochondria. Trends Biochem Sci 22: 110–113 (1997).

    Article  PubMed  CAS  Google Scholar 

  121. Lithgow T, Hoj PB, Hoogenraad NJ: Do cytosolic factors prevent promiscuity at the membrane surface? FEBS Lett 329: 1–4 (1993).

    Article  PubMed  CAS  Google Scholar 

  122. Lithgow T, Ryan M, Anderson RL, Hoj PB, Hoogenraad NJ: A constitutive form of heat-shock protein 70 is located in the outer membranes of mitochondria from rat liver. FEBS Lett 332:277–281 (1993).

    Article  PubMed  CAS  Google Scholar 

  123. Ljungdahl PO, Pennoyer JD, Robertson DE, Trumpower BL: Purification of highly active cytochrome bc1 complexes from phylogenetically diverse species by single chromatographic procedure. Biochim Biophys Acta 891: 227–241 (1987).

    Article  PubMed  CAS  Google Scholar 

  124. Luethy MH, Miernyk JA, Randal DD: The nucleotide and deduced amino acid sequence ofa cDNA encoding the E1 b subunit of the Arabidopsis thaliana mitochondrial pyruvate dehydrogenase complex. Biochim et Biophys Acta 1187: 95–98 (1994).

    Article  CAS  Google Scholar 

  125. Martin J, Mahlke K, Pfanner N: Role of an energized inner membrane in mitochondrial protein import delta-psi drives the movement of presequences. J Biol Chem 266: 18051–18057 (1991).

    PubMed  CAS  Google Scholar 

  126. Matocha MF, Waterman MR: Discriminatory processing of the precursor forms of cytochrome P-450scc and adrenodoxin by adrenocortical and heart mitochondria. J Biol Chem 259: 8672–8678 (1994).

    Google Scholar 

  127. McAda PC, Douglas MG: A neutral metallo endoprotease involved in processing of the F1-ATPase subunit precursor in mitochondria. J Biol Chem 6: 3177–3182 (1982).

    Google Scholar 

  128. McBride HM, Goping IS, Shore GC: The human mitochondrial import receptor, Htom20p, prevents a cryptic matrix targeting sequence from gaining access to the protein translocation machinery. J Cell Biol 134: 307–313 (1996).

    Article  PubMed  CAS  Google Scholar 

  129. McBride HM, Silvius JR, Shore GC: Insertion of an uncharged polypeptide into the mitochondrial inner membrane does not require a trans-bilayer electrochemical potential-effects of positive charges. Biochim Biophys Acta 1237: 162–168 (1995).

    Article  PubMed  Google Scholar 

  130. Miao Z, Gaynor JJ: Molecular cloning, characterisation and expression of Mn-superoxide dismutase from the rubber tree (Hevea brasiliens). Plant Mol Biol 23: 267–277 (1993).

    Article  PubMed  CAS  Google Scholar 

  131. Mihara K, Omura T: Cytosolic factors in mitochondrial protein import. Experientia 52: 1063–1068 (1996).

    Article  PubMed  CAS  Google Scholar 

  132. Moller IM, Lin W: Membrane-bound NAD(P)H dehydrogenases in higher plant cells. Ann Rev Plant Physiol 37: 309–334 (1986).

    Article  Google Scholar 

  133. Mooney B, Harmey MA: The occurrence of hsp70 in the outer membrane of plant mitochondria. Biochem Biophys Res Comm 218: 309–313 (1996).

    Article  PubMed  CAS  Google Scholar 

  134. Moore AL, Siedow JN: The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059: 121–140 (1991).

    Article  PubMed  CAS  Google Scholar 

  135. Morikami A, Aiso K, Asahi T, Nakamura K: The delta’-subunit of higher plant six-subunit mitochondrial F1-ATPase is homologous to the delta-subunit of animal mitochondrial Fl-ATPase. J Biol Chem 267: 72–76 (1992).

    PubMed  CAS  Google Scholar 

  136. Mozo T, Fischer K, Flügge UI, Schmitz UK: The N-terminal extension of the ADP/ATP translocator is not involved in targeting to plant mitochondria in vivo. Plant J 7: 1015–1020 (1995).

    Article  PubMed  CAS  Google Scholar 

  137. Murakami K and Mori M: Purified presequence binding factor pbf forms an import-competent complex with a purified mitochondrial precursor protein. EMBO J 9: 3201–3208 (1990).

    PubMed  CAS  Google Scholar 

  138. Nagakawa Y, Meashima M, Nakamura K, Asahi T: Molecular cloning of a cDNA for the smallest nuclear-encoded subunit of sweet potato cytochrome c oxidase: analysis with the cDNA of the structure and import into mitochondria of the subunit. Eur J Biochem 191: 557–561 (1990).

    Article  Google Scholar 

  139. Nast G, Muller-Rober B: Molecular characterisation of potato fumarate hydratase and functional expression in Escherichia coli. Plant Physiol 112: 1219–1227 (1996).

    Article  PubMed  CAS  Google Scholar 

  140. Neumann D, Emmerman M, Thierfelder J-M, zurNeiden U, Clericus M, Braun H-P, Novel L, Schmitz UK: HSP68 — a DnaK like heat-stress protein of plant mitochondria. Planta 190:32–43 (1993).

    Article  PubMed  CAS  Google Scholar 

  141. Neupert W: Protein import into mitochondria. Ann Rev Biochem 66: 863–917(1997).

    Article  PubMed  CAS  Google Scholar 

  142. Niidome T, Kitada S, Shimokata K, Ogishima T, and Ito A: Arginine residues in the extension peptide are required for cleavage of a precursor by mitochondrial processing peptidase. J Biol Chem 269: 24719–24722 (1994).

    PubMed  CAS  Google Scholar 

  143. Nugent JM, Palmer JD: RNA-mediated transfer of the gene coxll from the mitochondrion to the nucleus during flowering plant evolution. Cell 66: 473–481 (1991).

    Article  PubMed  CAS  Google Scholar 

  144. Nurani G, Eriksson M, Knorpp C, Glaser E, Franzén L-G: Homologous and heterologous protein import into mitochondria from Chlamydomonas reinhardtii. Plant Mol Biol 35: 973–980 (1997).

    Article  PubMed  CAS  Google Scholar 

  145. Nurani G, Franzen L-G: Isolation and characterisation of the mitochondrial ATP synthase from Chlamydomonas reinhardtii. cDNA sequence and deduced protein sequence of the a subunit. Plant Mol Biol 31:1105–1116 (1996).

    Article  PubMed  CAS  Google Scholar 

  146. Ogishima T, Niidome T, Shimokata K, Kitada S, Ito A: Analysis of elements in the substrate required for processing by mitochondrial processing peptidase. J Biol Chem 270: 30322–30326 (1995).

    Article  PubMed  CAS  Google Scholar 

  147. Ogishima T, Okada Y, Omura, T: Import and processing of the precursor of cytochrome P-450(SCC) by bovine adrenal cortex mitochondria. J Biochem. 98: 781–91 (1985).

    PubMed  CAS  Google Scholar 

  148. Ou W-J, Ito A, Okazaki H, Omura T: Purification and characterisation of a processing peptidase from rat liver mitochondria. J Biochem 103: 589–595 (1989).

    Google Scholar 

  149. Ou W-J, Kumamoto T, Mihara K, Kitada S, Niidome T, Ito A, Omura T: Structural requirement for recognition of the precursor proteins by the mitochondrial processing peptidase. J Biol Chem 269: 24673–24678 (1994).

    PubMed  CAS  Google Scholar 

  150. Perkins SJ, Weiss H: Low-resolution structural studies of mitochondrial ubiquinol:cytochrome c reductase in detergent solutions by neutron scattering. J Mol Biol 168: 847–866 (1983).

    Article  PubMed  CAS  Google Scholar 

  151. Perlman RK, Gehm BD, Kuo WL, Rosner MR: Functional analysis of conserved residues in the active site of insulin-degrading enzyme. J Biol Chem 268: 21538–21544 (1993).

    PubMed  CAS  Google Scholar 

  152. Perryman RA, Mooney B, Harmey MA: Identification of a 42-kDa plant mitochondrial outer membrane protein, MOM42, involved in the import of precursor proteins into plant mitochondria. Arch Biochem Biophys 316: 659–664 (1995).

    Article  PubMed  CAS  Google Scholar 

  153. Pfanner N, Neupert W: Transport of proteins into mitochondria a potassium diffusion potential is able to drive the import of Adp-Atp carrier. EMBO J 4: 2819–2826 (1985).

    PubMed  CAS  Google Scholar 

  154. Poeydomenge O, Marold M, Boudet AM, Grima-Pettenati J: Nucleotide sequence of a cDNA encoding mitochondrial malate dehydrogenase from Eucalyptus. Plant Physiol 107: 1455–1456 (1995).

    Article  PubMed  CAS  Google Scholar 

  155. Prasad TK, Stewart CR: cDNA clones encoding Arabidopsis thaliana and Zea mays mitochondrial chaperonin hsp60 and gene expression during seed germination and heat shock. Plant Mol Biol 18: 873–885 (1992).

    Article  PubMed  CAS  Google Scholar 

  156. Rawlings N, Barrett AJ: Homologous of insulinase, a new superfamily of metallopeptidase. Biochem J 275: 389–391.

    Google Scholar 

  157. Rawlings ND, Barrett AJ: Evolutionary families of metallopeptidase. Methods Enzymol 248: 183–228 (1995).

    Article  PubMed  CAS  Google Scholar 

  158. Rawlings ND, Barrett AJ: Classification of peptidases by comparisons of primary and tertiary structures, in 11th ICOP conference. Turku, Finland, IOS Press (1997).

    Google Scholar 

  159. Rebeille F, Macherel D, Mouillon J-M, Garin R, Douce R: Folate biosynthesis in higher plants: purification and molecular cloning of a bifunctional 6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase/7,8-dihydropteroate synthase localized in mitochondria. EMBO J 16:947–957 (1997).

    Article  PubMed  CAS  Google Scholar 

  160. Rhoads DM, Mcintosh L: Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc Natl Acad Sci USA 88: 2122–2126 (1991).

    Article  PubMed  CAS  Google Scholar 

  161. Roise D: Recognition and binding of mitochondrial prese-quences during the import of proteins into mitochondria. J Bioener Biomem 29: 19–27 (1977).

    Article  Google Scholar 

  162. Roise D, Schatz G: Mitochondrial presequences. J Biol Chem 263:4509–4511 (1998).

    Google Scholar 

  163. Saisho D, Nambara E, Naito S, Tsutsumi N, Hirai A, Nakamozo M: Characterisation of the gene family for alternative oxidase from Arabidopsis thaliana. Plant Mol Biol 35: 585–596 (1997).

    Article  PubMed  CAS  Google Scholar 

  164. Sakamoto A, Nosaka Y, and Tanaka K: Cloning and sequence analysis of a complementary DNA for manganese-superoxide dismutase from rice (Oryza sativa L.). Plant Physiol 103: 1477–1478 (1993).

    Article  PubMed  CAS  Google Scholar 

  165. Schägger H, Link TA, Engel WD, Von Jagow G: Isolation of the eleven protein subunits of the bc1 complex from beef heart. Methods Enzymol 126: 224–237 (1986).

    Article  PubMed  Google Scholar 

  166. Schatz G, Butow RA: How are protein imported into mitochondria. Cell 32: 316–318 (1983).

    Article  PubMed  CAS  Google Scholar 

  167. Schatz G, Dobberstein B: Common principles of protein translocation across membranes. Science 271: 1519–1526 (1996).

    Article  PubMed  CAS  Google Scholar 

  168. Schmitt ME, Trumpower BL: Subunit 6 regulates half of the sites reactivity of the dimeric cytochrome bc1 complex Saccharomyces cerevisiae. J Biol Chem 265: 17005–17011 (1990).

    PubMed  CAS  Google Scholar 

  169. Schneider G, Sjöling S, Wallin E, Wrede P, Glaser E, Von Heijne G: Feature-extraction from endopeptidase cleavage sites in mitochondrial targeting peptides. Proteins 30: 49–60 (1988).

    Article  Google Scholar 

  170. Schoppink P: Yeast ubiquinol: Cytochrome c Oxidoreductase. Ph. D. Thesis, Universiteit Van Amsterdam (1989).

    Google Scholar 

  171. Schulte U, Arretz M, Schneider H, Tropschug M, Wachter E, Neupert W, Weiss H: A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature 339: 147–149 (1989).

    Article  PubMed  CAS  Google Scholar 

  172. Schuster W, Kloska S, Brennicke A: An adenine nucleotide translocator gene from Arabidopsis thaliana. Biochim Biophys. Acta 1172: 205–208 (1993).

    CAS  Google Scholar 

  173. Sharpe JA, Day D: Structure, evolution and expression of the mitochondrial ADP/ATP translocator gene from Chlamydomonas reinhardtii. Mol Gen Genet 237: 134–144 (1993).

    Article  PubMed  CAS  Google Scholar 

  174. Silva Filho MD, Wieers MC, Flügge UI, Chaumont F, Boutry M: Mitochondrial and chloroplast targeting sequences in tandem modify protein import specificity in plant organelles. Plant Mol Biol 30: 769–780 (1996).

    Article  Google Scholar 

  175. Silva-Filho MD, Wieers MC, Flügge UI, Chaumont F, Boutry, M: Different in vitro and in vivo targeting properties of the transit peptide of a chloroplast envelope inner membrane protein. J Biol Chem 272: 15264–15269 (1997).

    Article  PubMed  CAS  Google Scholar 

  176. Sjoling S, Eriksson A, Glaser E: A helical element in the C-terminal domain of the N. plumbaginifolia F-1-beta pre-sequence is important for recognition by the mitochondrial processing peptidase. J Biol Chem 269: 32059–32062 (1994).

    PubMed  CAS  Google Scholar 

  177. Sjoling S, Glaser E: Mitochondrial processing peptidase integrated into be 1 complexof the respiratory chain in spinach. Proteolysis and protein turnover. Turku, Finland, IOS Press (1996).

    Google Scholar 

  178. Sjoling S, Glaser E: Characteristics of mitochondrial targeting peptides in plants. Trends Plant Sci 7: 1–4 (1998).

    Google Scholar 

  179. Sjöling S, Waltner M, Kalousek F, Glaser E, Weiner H: Studies on protein processing for membrane-bound spinach leaf mitochondrial processing peptidase integrated into the cytochrome bc-1 complex and the soluble rat liver matrix mitochondrial processing peptidase. Eur J Biochem 242: 114–121 (1996).

    Article  PubMed  Google Scholar 

  180. Smith AG, Santana MA, Wallace-Cook ADM, JM, R, Labbe-Bois R: Isolation of a cDNA encoding chloroplast ferrochelatase from Arabidopsis thaliana by functional complementation of a yeast mutant. J Biol Chem 269: 13405–13413 (1994).

    PubMed  CAS  Google Scholar 

  181. Smith MK, DA Day, Whelan J: Isolation of a novel soybean gene encoding a mitochondrial ATP synthase subunit. Arc Biochem Biophys 313: 235–340 (1994).

    Article  CAS  Google Scholar 

  182. Song M-C, Shimokata K, Kitada S, Ogishima T, Ito A: Role of basic amino acids in cleavage of synthetic peptide substrates by mitochondrial processing peptidase. J Biochem 120: 1163–1166 (1996).

    Article  PubMed  CAS  Google Scholar 

  183. Srinivasan R, Oliver DJ: H-protein of the glycine decarboxylase multienzyme complex. Complementary DNA encoding the protein from Arabidopsis thaliana. Plant Physiol 98: 1518–1519 (1992).

    Article  PubMed  CAS  Google Scholar 

  184. Sulli C, Oliver DJ: Cloning of the delta-prime subunit of the mitochondrial Fl-ATPase from peas. Plant Sci 91: 149–156 (1993).

    Article  CAS  Google Scholar 

  185. Surpin M., Chory J: The co-ordinatio of nuclear and organellar genome in eukaryotic cells. Essays Biochem 32: 113–125 (1997).

    PubMed  CAS  Google Scholar 

  186. Szigyarto C, Dessi P, Smith MK, Knorpp C, Harmey MA, Day DA, Glaser E, Whelan J: A matrix-located processing peptidase of plant mitochondria. Plant Mol Biol 36: 171–181 (1991).

    Article  Google Scholar 

  187. Taniguchi M, Sawaki H, Sasakawa H, Hase T, Sugiyama T: Cloning and sequence analysis of a cDNA encoding aspartate aminotransferase isozyme from Panicum miliaceum L., a C4 plant. Eur J Biochem 204: 611–620 (1992).

    Article  PubMed  CAS  Google Scholar 

  188. Taniguchi M, Sugiyama T: Isolation, characterisation and expression of cDNA clones encoding a mitochondrial malate translocator from Panicum miliaceum L. Plant Mol Biol 30: 51–64 (1996).

    Article  PubMed  CAS  Google Scholar 

  189. Terada K, Kanazawa M, Yano M, Hanson B, Hoogenraad N, Mori M: Participating of the import receptor Tom20 in protein import into mammalian mitochondria: Analyses in vitro and in cultured cells. FEBS Lett 403: 309–312 (1997).

    Article  PubMed  CAS  Google Scholar 

  190. Tohru K, Masao S, Katsuyoshi M: Cytosolic chaperones determine the targeting pathway of precursor proteins to mitochondria. EMBO J 15: 399–407 (1996).

    Google Scholar 

  191. Trumpower BL: Cytochrome bc1 complexes of microorganisms. Microbiol Rev 54: 101–129 (1990).

    PubMed  CAS  Google Scholar 

  192. Tsugeki R, Mori H, Nishimura M.: Purification, cDNA cloning and northern blot analysis of mitochondrial chaperonin 60 from pumpkin cotyledons. Eur J Biochem 209: 453–458 (1992).

    Article  PubMed  CAS  Google Scholar 

  193. Turner SR, Ireland R, Morgan C, Rawsthorne S: Identification and localization of multiple forms of serine hydrox-ymethylase in pea (Pisum sativum) and characterisation of a cDNA encoding a mitochondrial isoform. J Biol Chem 267: 13528–13534 (1992).

    Google Scholar 

  194. Turner SR, Ireland R, Rawsthorne S: Purification and primary amino acid sequence of the L subunit of glycine decarboxylase. J Biol Chem 267: 7745–7750 (1992).

    PubMed  CAS  Google Scholar 

  195. Turner SR, Ireland R, Rawsthorne S: Cloning and characterisation of the P subunit of glycine decarboxylase from pea (Pisum sativum). J Biol Chem 267: 5355–5360 (1992).

    PubMed  CAS  Google Scholar 

  196. Unger EA, Hamd JM, Cashmore AR, Vasconcelos AC: Isolation of a cDNA encoding mitochondrial citrate synthase from Arabidopsis thaliana. Plant Mol Biol 13: 411–418 (1989).

    Article  PubMed  CAS  Google Scholar 

  197. Vanlerberghe GC, Mcintosh L: Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene in tobacco. Plant Physiol 105: 867–874 (1994).

    Article  PubMed  CAS  Google Scholar 

  198. Vianello A, Braidot E, Petrussa E, Macri F: ATP synthesis driven by a-keto acid-stimulated alternative oxidase in pea leaf mitochondria. Plant Cell Physiol 38: 1368–1374 (1997).

    Article  CAS  Google Scholar 

  199. Visioli G, Meastri E, Marmiroli N.: Differential display-mediated isolation of a genomic sequence for a putative mitochondrial LMW HSP specifically expressed in codition of induced thermotolerance in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 34: 517–527 (1997).

    Article  PubMed  CAS  Google Scholar 

  200. Von Heijne G.: Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5: 1335–1342 (1986).

    Google Scholar 

  201. Von Heijne G, Steppuhn J, Herrmann RG: Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535–546 (1989).

    Article  Google Scholar 

  202. Von Stedingk E, Glaser E: The molecular chaperone mhsp72 is partially associated with the inner mitochondrial membrane both in normal and heat stressed Spinacia oleracea. Biochem Mol Biol Int 35: 1307–1314 (1995).

    Google Scholar 

  203. Von Stedingk E, Pavlov P, Grinkevich V, Glaser E: Mitochondrial protein import:modification of sulfhydryl groups of the inner mitochondrial membrane import machinery in Solanum tuberosum inhibits protein import. Plant Mol Biol 35:809–820 (1997).

    Article  Google Scholar 

  204. Wadsworth GJ, Gebhardt JS, Matthews BF: Characterisation of a soybean cDNA clone encoding the mitochondrial isozyme of aspartate aminotransferase, AAT4. Plant Mol Biol 27: 1085–1095 (1995).

    Article  PubMed  CAS  Google Scholar 

  205. Waegemann K, Soll J: Phosphorylation of the transit sequence of chloroplast proteins. J Biol Chem 271: 6545–6554 (1996).

    Article  PubMed  CAS  Google Scholar 

  206. Walters AJ, Watts FZ Moore AL: Bioenergetic aspectsw of protein targeting to plant mitochondria. In: Lambers H, Van der Plas LHW (eds), Molecular, biochemical and physiological aspects of plant respiration. SPB Academic Publishing, The Hague (1992).

    Google Scholar 

  207. Waltner M, Hammen PK, Weiner H: Influence of the mature portion of a precursor protein on the mitochondrial signal sequence. J Biol Chem 271: 21226–21230 (1996).

    Article  PubMed  CAS  Google Scholar 

  208. Waltner M, Weiner H: Conversion of a nonprocessed mitochondrial precursor protein into one that is processed by the mitochondrial processing peptidase. J Biol Chem 270: 2631 1–26317 (1995).

    Article  Google Scholar 

  209. Watts FZ, Walters AJ, Moore AL: Characterisation of pHSPl, a cDNA clone encoding a mitochondrial HSP70 from Pisum sativum. Plant Mol Biol 18: 23–32 (1992).

    Article  PubMed  CAS  Google Scholar 

  210. Weiss H, Kolb H: Isolation of mitochondrial succinate: Ubiquinone reductase, cytochrome c reducatse and cytochrome c oxidase from Neurospora crassa using nonionic detergent. Eur J Biochem 99: 139–149 (1979).

    Article  PubMed  CAS  Google Scholar 

  211. Whelan J, Glaser E: Protein import into plant mitochondria. Plant Mol Biol 33: 771–789 (1997).

    Article  PubMed  CAS  Google Scholar 

  212. Whelan J, Hugosson, M, Glaser E, Day DA: Studies on the import and processing of the alternative oxidase precursor by isolated soybean mitochondria. Plant Mol Biol 27: 769–778 (1995).

    Article  PubMed  CAS  Google Scholar 

  213. Whelan J, Knorpp C, Harmey MA and Glaser E: Specificity of leaf mitochondrial and chloroplast processing systems for nuclear-encoded precursor proteins. Plant Mol Biol 16: 283–92 (1991).

    Article  PubMed  CAS  Google Scholar 

  214. Whelan J, O’Mahony P, Harmey MA: Processing of precursor proteins by plant mitochondria. Arc Biochem Biophys 279:281–285 (1990).

    Article  CAS  Google Scholar 

  215. Whelan J, Smith MK, Yu JW, Badger MR, Price GD, Day DA: Cloning of an additional cDNA for the alternative oxidase in tobacco. Plant Physiol 107: 1469–1470 (1995).

    Article  PubMed  CAS  Google Scholar 

  216. Whelan J, Tanudji MR, Smith MK, Day DA: Evidence for a link between translocation and processing during protein import into soybean mitochondria. Biochim Biophys Acta 1312:48–54 (1996).

    Article  PubMed  Google Scholar 

  217. Whelan JM, Mcintosh L, Day DA: Sequencing of a cDNA alternative oxidase cDNA clone. Plant Physiol 103: 1481 (1993).

    Google Scholar 

  218. White JA, Scandalios JG: Isolation and characterization of a cDNA for mitochondrial manganese superoxide dismutase (SOD-3) of maize and its relation to other manganese superoxide dismutases. Biochim Biophys. Acta 951: 61–70 (1988).

    CAS  Google Scholar 

  219. White JA, Scandalios JG: Deletion analysis of the maize mitochondrial superoxide dismutase transit peptide. Proc Natl Acad Sci USA 86: 3534–3538 (1989).

    Article  PubMed  CAS  Google Scholar 

  220. Winning BM, Bathgate B, Purdue PE, Leaver CJ: Nucleotide sequence of a cDNA encoding the beta subunit of mitochondrial ATP synthase from Zea mays. Nucl Acid Res 18: 5885 (1990).

    Google Scholar 

  221. Winning BM, Bourguignon J, Leaver CJ: Plant mitochondrial NAD+ dependent malic enzymes: cDNA cloning, deduced primary stucture and the 59-and 62-Kda subunits, import, gene complexity and expression analysis. J Biol Chem 269: 4780–4786 (1994).

    PubMed  CAS  Google Scholar 

  222. Winning BM, Day CD, Sarah CJ, Leaver CJ: Nulceotide sequence of two cDNAs encoding the adenine nucleotide translocator from Zea mays L. Plant Mol Biol 17: 305–307 (1991).

    Article  PubMed  CAS  Google Scholar 

  223. Winning BM, Sarah CJ, Purdue PE, Day CD, Leaver CJ: The adenine nucleotide translocator of higher plants is synthesized as a large precursor that is processed upon import into mitochondria. Plant J. 2: 763–773 (1997).

    Google Scholar 

  224. Wischmann C, Schuster W: Transfer of rps 10 from mitochondrion to the nucleus in Arabidopsis thaliana: evidence or RNA-mediated transfer and exon shuffling at the integration site.FEBS Lett. 374: 152–156 (1995).

    Article  PubMed  CAS  Google Scholar 

  225. Witt U, Luhrs R, Buck F, Lembke K, Gruneberg-Seiler M, Abel W: Mitochondrial malate dehydrogenase in Brassica napus: altered protein patterns in different nuclear mitochondrial combinations. Plant Mol Biol 35: 1015–1021 (1997).

    Article  PubMed  CAS  Google Scholar 

  226. Wong-Vega L, Burke JJ, Allen RD: Isolation and sequence analysis of a cDNA that encodes pea manganese superoxi-dase dismutase. Plant Mol Biol 17: 1271–1274 (1991).

    Article  PubMed  CAS  Google Scholar 

  227. Xia D, Yu C-A, Kim H, Xia J-Z, Kachurin A M, Zhang L, Yu L, Deisenhofer J: Crystal structure of the cytochrome bc1complex from bovine heart mitochondria. Science 277: 60–66.

    Google Scholar 

  228. Yaffe MP, Ohta S and Schatz G: A yeast mutant temperature-sensitive for mitochondrial assembly is deficient in a mitochondrial assembly is deficient in a mitochondrial protease activity that cleaves imported precursor polypeptides. EMBO J 4: 2069–2074 (1985).

    PubMed  CAS  Google Scholar 

  229. Yang M, Jensen RE, Yaffe MP, Oppliger W, Schatz G: Import of proteins into yeast mitochondria the purified matrix processing protease contains two subunits which are encoded by the nuclear Mas 1 and Mas2 genes. EMBO J 7: 3857–3862 (1988).

    PubMed  CAS  Google Scholar 

  230. Zhou J, Bai Y, Weiner H: Proteolysis prevents in vivo chimeric fusion protein import into yeast mitochondria: Cytosolic cleavage and subcellular distribution. J Biol Chem 270: 16689–16693 (1995).

    Article  PubMed  CAS  Google Scholar 

  231. Zhou YH, Ragan MA: Characterization of the nuclear gene encoding mitochondrial aconitase in the marine red alga Gracilaria verrucosa. Plant Mol Biol 28(4): 635–646 (1995).

    Article  PubMed  CAS  Google Scholar 

  232. Zwizinski C, Neupert W: Precursor proteins are transported into mitochondria in the absence of proteolytic cleavage of the additional sequences. J Biol Chem 258: 13340–13346 (1983).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Arrhenius Laboratories for Natural Sciences, Stockholm University, S-106, Stockholm, 91, Sweden

    Elzbieta Glaser & Sara Sjöling

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

    Marcel Tanudji & James Whelan

Authors
  1. Elzbieta Glaser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sara Sjöling
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcel Tanudji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James Whelan
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Jürgen Soll

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Glaser, E., Sjöling, S., Tanudji, M., Whelan, J. (1998). Mitochondrial protein import in plants. In: Soll, J. (eds) Protein Trafficking in Plant Cells. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5298-3_16

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-5298-3_16

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-6229-9

  • Online ISBN: 978-94-011-5298-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation