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.
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References
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).
Attardi G, Schatz G: Biogenesis of mitochondria: Assembly of the mitochondrial membrane systems. Ann Rev Cell Biol 4:289–333 (1988).
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).
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).
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).
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).
Becker AB: An unusal active site identified in a family of zinc metalloendopeptidase. Proc Natl Acad Sci USA 88: 3835–3839 (1992).
Becker AB, Roth RA: Insulysin and pitrilysin: insulin-degrading enzymes of mammals andbacteria. Methods En-zymol 248: 693–703 (1993).
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).
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).
Berry EA, Huang L-S, DeRose VJ: Ubiquinol-cytochrome c oxidoreductase of higer plants. J Biol Chem 266: 9064–9077 (1991).
Boemer U, Pfanner N, Dietmeier K: Identification of a third yeast mitochondrial Tom protein with tetratrico peptide repeats. FEBS Lett 382: 153–158 (1996).
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).
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).
Boumans H: The bc1 complex of the respiratory chain of Saccharomyces cerevisiae. Ph.D. thesis, University of Amsterdam (1997).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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??).
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).
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).
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).
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).
Cohen P, Pierotti AR, Chesneau V, Foulon T, PA: N-Arginine dibasic convertase. Methods Enzym 248: 703–716 (1995).
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).
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).
Cruz-Hernandez A, Gomez-Lim MA: Alternative oxidase from mango (Mangifera indica L. is differentially regulated during fruit ripening. Planta 197: 569–576 (1995).
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).
Cui X, Wise RP, Schnable PS: The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272: 1334–1336 (1996).
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).
Dahlin C, Cline K: Developmental regulation of the plastid protein import apparatus.Plant Cell 3: 1131–1140 (1991).
Dessi P: The characterisation of protein import pathways in plant mitochondria. Ph. D. thesis, University of Western Australia (submitted) (1998).
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).
Dessi P, Whelan J: Temporal regulation of in vitro import of precursor proteins into tobacco mitochondria. FEBS Lett 415: 173–178 (1997).
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).
Doolittle RF: Similar amino acid sequences: chance or commmon ancestory? Science 214: 149–159 (1981).
Douce R: Mitochondria in higher plants-structure, function and biogenesis. Academic Press, London (1985).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Eriksson AC: Functional and structural studies on the integral mitochondrial processing peptidase/bc1 complex from Spinacia oleracea. Ph.D. thesis, Stockholm University (1996).
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).
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).
Filipowicz W, Hohn T.: Post transcriptional control of gene expression in plants. Plant Mol Biol 32 (1996).
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).
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).
Gavel Y, Von Heijne G: Cleavage-site motifs in mitochondrial targeting peptides. Protein Engineering 4: 33–38 (1990).
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).
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).
Glick B, Schatz G.: Import of proteins into mitochondria. Annu Rev Genet 25: 21–44 (1991).
Gray MW: Origin and evolution of organelle genomes. Curr Opinions Genet Develop 3: 884–890 (1993).
Grof CPL et al.: Mitochondrial pyruvate dehydrogenase: Molecular cloning of the Ela subunit and expression analysis. Plant Physiol 108:1623–1629 (1995).
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).
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).
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).
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).
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).
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).
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).
Hartl F-U, Pfanner N, Nicholson DW and Neupert W: Mitochondrial protein import. Biochim Biophys Acta 988(1): 1–45 (1989).
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).
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).
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).
Heins L, Schmitz UK: A receptor for protein import into potato mitochondria. Plant J 9: 829–839 (1996).
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).
Hemon P, Robbins MP, Cullimore JV: Targeting of gluthamine synthetase to the mitochondria of transgenic tobacco. Plant Mol Biol 15: 895–904 (1993).
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).
Hiser C, Kapranov P, Mcintosh L: Genetic modification of respiratory capacity in potato. Plant Physiol 110: 277–286 (1996).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Iacobazzi V, Palmieri F: Nucleotide sequence of a cDNA encoding the ADP/ATP carrier from wheat (Triticum turgidum). Plant Physiol 107: 1473 (1995).
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).
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).
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).
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).
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).
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).
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).
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).
Komiya, T, Sakaguchi, M, Mihara K: Cytoplasmic chaper-ones determine the targeting pathway of precursor proteins to mitochondria. EMBO J 15: 399–407 (1996).
Kopriva S, Bauwe H: P-protein of Glycine decarboxylase from Flaveria pringlei. Plant Physiol 104: 1079–1080 (1994).
Kopriva S, Bauwe H: T-protein of glycine decarboxylase from Solanum tuberosum. Plant Physiol 104: 1079–1080 (1994).
Kopriva S, Bauwe H: Serine hydroxymethyltransferase from Solanum tuberosum. Plant Physiol 107: 271–272 (1995).
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).
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).
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).
Kumar AM and Soll D: Arabidopsis alternative oxidase sustains Eschericia coli respiration. Proc Natl Acad Sci USA 89: 10842–10846 (199
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).
Laloi, M, Klein, M, Riesmeier, JW, and Muller-Rober, B: A plant cold-induced uncoupler protein. Nature 389: 135–136 (1997).
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).
Larsen KS, Auld DS: Characterisation of an inhibitory metal binding site in carboxypeptidase A. Biochemistry 30: 2613–2618 (1991).
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).
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).
Lill R, Nargang FE, Neupert W: Biogenesis of mitochondrial proteins. Curr Opinion Cell Biol 8: 505–512 (1996).
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).
Lithgow T, Cuezva JM, Silver PA: Highways for protein delivery to the mitochondria. Trends Biochem Sci 22: 110–113 (1997).
Lithgow T, Hoj PB, Hoogenraad NJ: Do cytosolic factors prevent promiscuity at the membrane surface? FEBS Lett 329: 1–4 (1993).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Mihara K, Omura T: Cytosolic factors in mitochondrial protein import. Experientia 52: 1063–1068 (1996).
Moller IM, Lin W: Membrane-bound NAD(P)H dehydrogenases in higher plant cells. Ann Rev Plant Physiol 37: 309–334 (1986).
Mooney B, Harmey MA: The occurrence of hsp70 in the outer membrane of plant mitochondria. Biochem Biophys Res Comm 218: 309–313 (1996).
Moore AL, Siedow JN: The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059: 121–140 (1991).
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).
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).
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).
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).
Nast G, Muller-Rober B: Molecular characterisation of potato fumarate hydratase and functional expression in Escherichia coli. Plant Physiol 112: 1219–1227 (1996).
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).
Neupert W: Protein import into mitochondria. Ann Rev Biochem 66: 863–917(1997).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Rawlings N, Barrett AJ: Homologous of insulinase, a new superfamily of metallopeptidase. Biochem J 275: 389–391.
Rawlings ND, Barrett AJ: Evolutionary families of metallopeptidase. Methods Enzymol 248: 183–228 (1995).
Rawlings ND, Barrett AJ: Classification of peptidases by comparisons of primary and tertiary structures, in 11th ICOP conference. Turku, Finland, IOS Press (1997).
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).
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).
Roise D: Recognition and binding of mitochondrial prese-quences during the import of proteins into mitochondria. J Bioener Biomem 29: 19–27 (1977).
Roise D, Schatz G: Mitochondrial presequences. J Biol Chem 263:4509–4511 (1998).
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).
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).
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).
Schatz G, Butow RA: How are protein imported into mitochondria. Cell 32: 316–318 (1983).
Schatz G, Dobberstein B: Common principles of protein translocation across membranes. Science 271: 1519–1526 (1996).
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).
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).
Schoppink P: Yeast ubiquinol: Cytochrome c Oxidoreductase. Ph. D. Thesis, Universiteit Van Amsterdam (1989).
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).
Schuster W, Kloska S, Brennicke A: An adenine nucleotide translocator gene from Arabidopsis thaliana. Biochim Biophys. Acta 1172: 205–208 (1993).
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).
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).
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).
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).
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).
Sjoling S, Glaser E: Characteristics of mitochondrial targeting peptides in plants. Trends Plant Sci 7: 1–4 (1998).
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).
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).
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).
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).
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).
Sulli C, Oliver DJ: Cloning of the delta-prime subunit of the mitochondrial Fl-ATPase from peas. Plant Sci 91: 149–156 (1993).
Surpin M., Chory J: The co-ordinatio of nuclear and organellar genome in eukaryotic cells. Essays Biochem 32: 113–125 (1997).
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).
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).
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).
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).
Tohru K, Masao S, Katsuyoshi M: Cytosolic chaperones determine the targeting pathway of precursor proteins to mitochondria. EMBO J 15: 399–407 (1996).
Trumpower BL: Cytochrome bc1 complexes of microorganisms. Microbiol Rev 54: 101–129 (1990).
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).
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).
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).
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).
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).
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).
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).
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).
Von Heijne G.: Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5: 1335–1342 (1986).
Von Heijne G, Steppuhn J, Herrmann RG: Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535–546 (1989).
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).
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).
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).
Waegemann K, Soll J: Phosphorylation of the transit sequence of chloroplast proteins. J Biol Chem 271: 6545–6554 (1996).
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).
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).
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).
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).
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).
Whelan J, Glaser E: Protein import into plant mitochondria. Plant Mol Biol 33: 771–789 (1997).
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).
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).
Whelan J, O’Mahony P, Harmey MA: Processing of precursor proteins by plant mitochondria. Arc Biochem Biophys 279:281–285 (1990).
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).
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).
Whelan JM, Mcintosh L, Day DA: Sequencing of a cDNA alternative oxidase cDNA clone. Plant Physiol 103: 1481 (1993).
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).
White JA, Scandalios JG: Deletion analysis of the maize mitochondrial superoxide dismutase transit peptide. Proc Natl Acad Sci USA 86: 3534–3538 (1989).
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).
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).
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).
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).
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).
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).
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).
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.
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).
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).
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).
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).
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).
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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
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