Mitochondrial Respiratory Complex Biogenesis: Communication, Geneexpression and Assembly

Plant Mitochondria

Volumn , Issue , 2007, Pages 141-170

  Giegé, Philippe ^a  

^a INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

Assembly; Biogenesis; Heme synthesis; Mitochondrial genome; Respiratory complexes

Indexed keywords

EID: 37249061995     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470986592.ch5     Document Type: Chapter

References (165)

1. Abdel-Ghany SE, Ye H, Garifullina GF, Zhang L, Pilon-Smits EA and Pilon M (2005) Iron-sulfur cluster biogenesis in chloroplasts. Involvement of the scaffold protein CpIscA. Plant Physiol 138, 161-172.
2. Ackerman SH (2002) Atp11p and Atp12p are chaperones for F(1)-ATPase biogenesis in mitochondria. Biochim Biophys Acta 1555, 101-105.
3. Ackerman SH and Tzagoloff A (1990) Identification of two nuclear genes (ATP11, ATP12) required for assembly of the yeast F1-ATPase. Proc Natl Acad Sci USA 87, 4986-4990.
4. Adams KL and Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29, 380-395.
5. Agrawal GK, Agrawal SK, Shibato J, Iwahashi H and Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300, 775-783.
6. Ahuja U, Thony-Meyer L (2005) CcmD is involved in complex formation between CcmC and the heme chaperone CcmE during cytochrome c maturation. J Biol Chem 280, 236-243.
7. Altamura N, Capitanio N, Bonnefoy N, Papa S and Dujardin G (1996) The Saccharomyces cerevisiae OXA1gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase. FEBS Lett 382, 111-115.
8. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
9. Balandin T and Castresana C (2002) AtCOX17, an Arabidopsis homolog of the yeast copper chaperone COX17. Plant Physiol 129, 1852-1857.
10. Balk J and Lobreaux S (2005) Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci 10, 324-331.
11. Barros MH, Nobrega FG and Tzagoloff A (2002) Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J Biol Chem 277, 9997-10002.
12. Beinert H (2000) Iron-sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5, 2-15.
13. Bernard DG, Quevillon-Cheruel S, Merchant S, Guiard B and Hamel PP (2005) Cyc2p, a membranebound flavoprotein involved in the maturation of mitochondrial c-type cytochromes. J Biol Chem 280, 39852-39859.
14. Bonnard G and Grienenberger JM (1995) A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria. Mol Gen Genet 246, 81-99.
15. Bourges I, Ramus C, Mousson de Camaret B, et al. (2004) Structural organization of mitochondrial human complex I: role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem J 383, 491-499.
16. Braun HP, Kruft V and Schmitz UK (1994) Molecular identification of the ten subunits of cytochrome-c reductase from potato mitochondria. Planta 193, 99-106.
17. Busi MV, Zabaleta EJ, Araya A and Gomez-Casati DF (2004) Functional and molecular characterization of the frataxin homolog from Arabidopsis thaliana. FEBS Lett 576, 141-144.
18. Butow RA and Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14, 1-15.
19. Cardazzo B, Hamel P, Sakamoto W, Wintz H and Dujardin G (1998) Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity. Gene 221, 117-125.
20. Carr HS, George GN and Winge DR (2002) Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J Biol Chem 277, 31237-31242.
21. Carr HS and Winge DR (2003) Assembly of cytochrome c oxidase within the mitochondrion. Acc Chem Res 36, 309-316.
22. Chow KS, Singh DP, Roper JM and Smith AG (1997) A single precursor protein for ferrochelatase-I from Arabidopsis is imported in vitro into both chloroplasts and mitochondria. J Biol Chem 272, 27565-27571.
23. Chuman L and Brody S (1989) Acyl carrier protein is present in the mitochondria of plants and eucaryotic micro-organisms. Eur J Biochem 184, 643-649.
24. Clifton R, Lister R, Parker KL, et al. (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol Biol 58, 193-212.
25. Cornah JE, Roper JM, Pal Singh D and Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem J 362, 423-432.
26. Crivellone MD (1994) Characterization of CBP4, a new gene essential for the expression of ubiquinolcytochrome c reductase in Saccharomyces cerevisiae. J Biol Chem 269, 21284-21292.
27. Cruciat CM, Hell K, Folsch H, Neupert W and Stuart RA (1999) Bcs1p, an AAA-family member, is a chaperone for the assembly of the cytochrome bc(1) complex. EMBO J 18, 5226-5233.
28. Curi GC, Chan RL and Gonzalez DH (2005) The leader intron of Arabidopsis thaliana genes encoding cytochrome c oxidase subunit 5c promotes high-level expression by increasing transcript abundance and translation efficiency. J Exp Bot 56, 2563-2571.
29. Dojcinovic D, Krosting J, Harris AJ, Wagner DJ and Rhoads DM (2005) Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Mol Biol 58, 159-175.
30. Dumont ME, Ernst JF, Hampsey DM and Sherman F (1987) Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. EMBO J 6, 235-241.
31. Elorza A, Leon G, Gomez I, et al. (2004) Nuclear SDH2-1 and SDH2-2 genes, encoding the iron-sulfur subunit of mitochondrial complex II in Arabidopsis, have distinct cell-specific expression patterns and promoter activities. Plant Physiol 136, 4072-4087.
32. Eubel H, Jansch L and Braun HP (2003) New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol 133, 274-286.
33. Eyal Y, Curie C and McCormick S (1995) Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell 7, 373-384.
34. Faivre-Nitschke E, Nazoa P, Gualberto JM, Grienenberger JM and Bonnard G (2001) Wheat mitochondria ccmB encodes the membrane domain of a putative ABC transporter involved in cytochromes c biogenesis. Biochim Biophys Acta 1519, 199-208.
35. Funes S, Nargang FE, Neupert W and Herrmann JM (2004) The Oxa2 protein of Neurospora crassa plays a critical role in the biogenesis of cytochrome oxidase and defines a ubiquitous subbranch of the Oxa1/YidC/Alb3 protein family. Mol Biol Cell 15, 1853-1861.
36. Garland SA, Hoff K, Vickery LE and Culotta VC (1999) Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for iron-sulfur cluster assembly. J Mol Biol 294, 897-907.
37. Giegé P, Knoop V and Brennicke A (1998) Complex II subunit 4 (sdh4) homologous sequences in plant mitochondrial genomes. Curr Genet 34, 313-317.
38. Giegé P, Rayapuram N, Meyer EH, Grienenberger JM and Bonnard G (2004) CcmF(C) involved in cytochrome c maturation is present in a large sized complex in wheat mitochondria. FEBS Lett 563, 165-169.
39. Giegé P, Sweetlove L and Leaver C (2003) Identification of mitochondrial protein complexes in Arabidopsis using two-dimensional Blue-Native polyacrylamide gel electrophoresis. Plant Mol Biol Reporter 21, 133-144.
40. Giegé P, Sweetlove LJ, Cognat V and Leaver CJ (2005) Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17, 1497-1512.
41. Glerum DM, Muroff I, Jin C and Tzagoloff A (1997) COX15 codes for a mitochondrial protein essential for the assembly of yeast cytochrome oxidase. J Biol Chem 272, 19088-19094.
42. Gomez-Casati DF, Busi MV, Gonzalez-Schain N, Mouras A, Zabaleta EJ and Araya A (2002) A mitochondrial dysfunction induces the expression of nuclear-encoded complex I genes in engineered male sterile Arabidopsis thaliana. FEBS Lett 532, 70-74.
43. Gonzalez DH, Bonnard G and Grienenberger JM (1993) A gene involved in the biogenesis of c-type cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 21, 248-255.
44. Gray GR, Maxwell DP, Villarimo AR and McIntosh L (2004a) Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Rep 23, 497-503.
45. Gray GR, Villarimo AR, Whitehead CL and McIntosh L (2004b) Transgenic tobacco (Nicotiana tabacum L.) plants with increased expression levels of mitochondrial NADP+-dependent isocitrate dehydrogenase: evidence implicating this enzyme in the redox activation of the alternative oxidase. Plant Cell Physiol 45, 1413-1425.
46. Green-Willms NS, Butler CA, Dunstan HM and Fox TD (2001) Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J Biol Chem 276, 6392-6397.
47. Grefen C and Harter K (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta 219, 733-742.
48. Grohmann L, Rasmusson AG, Heiser V, Thieck O and Brennicke A (1996) TheNADH-binding subunit of respiratory chain complex I is nuclear-encoded in plants and identified only in mitochondria. Plant J 10, 793-803.
49. Guenebaut V, Schlitt A, Weiss H, Leonard K and Friedrich T (1998) Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276, 105-112.
50. Hamel P, Sakamoto W, Wintz H and Dujardin G (1997) Functional complementation of an oxa1-yeast mutation identifies an Arabidopsis thaliana cDNA involved in the assembly of respiratory complexes. Plant J 12, 1319-1327.
51. Harrison MD, Jones CE and Dameron CT (1999) Copper chaperones: function, structure and copperbinding properties. J Biol Inorg Chem 4, 145-153.
52. Hass C, Lohrmann J, Albrecht V, et al. (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23, 3290-3302.
53. Heazlewood JL, Howell KA and Millar AH (2003) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim Biophys Acta 1604, 159-169.
54. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J and Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241-256.
55. Heazlewood JL, Whelan J and Millar AH (2003) The products of the mitochondrial orf25 and orfB genes are FO components in the plant F1FO ATP synthase. FEBS Lett 540, 201-205.
56. Heiser V, Brennicke A and Grohmann L (1996) 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.
57. Helfenbein KG, Ellis TP, Dieckmann CL and Tzagoloff A (2003) ATP22, a nuclear gene required for expression of the F0 sector of mitochondrial ATPase in Saccharomyces cerevisiae. J Biol Chem 278, 19751-19756.
58. Hernould M, Suharsono S, Zabaleta E, et al. (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol Biol 36, 499-508.
59. Herrmann JM and Funes S (2005) Biogenesis of cytochrome oxidase-sophisticated assembly lines in the mitochondrial inner membrane. Gene 354, 43-52.
60. Horng YC, Cobine PA, Maxfield AB, Carr HS and Winge DR (2004) Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J Biol Chem 279, 35334-35340.
61. Howell KA, Millar AH and Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with promitochondrial structures rich in components of the protein import apparatus. Plant Mol Biol 60, 201-223.
62. Huang J, Struck F, Matzinger DF and Levings CS (1994) Flower-enhanced expression of a nuclearencoded mitochondrial respiratory protein is associated with changes in mitochondrion number. Plant Cell 6, 439-448.
63. Jacinto E and Hall MN (2003) Tor signalling in bugs, brain and brawn. Nat Rev Mol Cell Biol 4, 117-126.
64. Johnson DC, Dean DR, Smith AD and Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74: 247-281.
65. Juszczuk IM and Rychter AM (2003) Alternative oxidase in higher plants. Acta Biochim Pol 50, 1257-1271.
66. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G and Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657.
67. Karpova OV, Kuzmin EV, Elthon TE and Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14, 3271-3284.
68. Kermorgant M, Bonnefoy N and Dujardin G (1997) Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr Genet 31, 302-307.
69. Koo AJ, Fulda M, Browse J and Ohlrogge JB (2005) Identification of a plastid acyl-acyl carrier protein synthetase in Arabidopsis and its role in the activation and elongation of exogenous fatty acids. Plant J 44, 620-632.
70. Kosugi S and Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9, 1607-1619.
71. Kranz R, Lill R, Goldman B, Bonnard G and Merchant S (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol Microbiol 29, 383-396.
72. Kronekova Z and Rodel G (2005) Organisation of assembly factors Cbp3p and Cbp4p and their effect on bc(1) complex assembly in Saccharomyces cerevisiae. Curr Genet 47, 203-212.
73. Kuhn A, Stuart R, Henry R and Dalbey RE (2003) The Alb3/Oxa1/YidC protein family: membranelocalized chaperones facilitating membrane protein insertion? Trends Cell Biol 13, 510-516.
74. Kushnir S, Babiychuk E, Storozhenko S, et al. (2001) Amutation of the mitochondrialABCtransporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13, 89-100.
75. Lefebvre-Legendre L, Salin B, Schaeffer J, et al. (2005) Failure to assemble the alpha 3 beta 3 subcomplex of the ATP synthase leads to accumulation of the alpha and beta subunits within inclusion bodies and the loss of mitochondrial cristae in Saccharomyces cerevisiae. J Biol Chem 280, 18386-18392.
76. Lefebvre-Legendre L, Vaillier J, Benabdelhak H, Velours J, Slonimski PP and di Rago JP (2001) Identification of a nuclear gene (FMC1) required for the assembly/stability of yeast mitochondrial F (1)-ATPase in heat stress conditions. J Biol Chem 276, 6789-6796.
77. Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354, 110-116.
78. Leon S, Touraine B, Briat JF and Lobreaux S (2005) Mitochondrial localization of Arabidopsis thaliana Isu Fe-S scaffold proteins. FEBS Lett 579, 1930-1934.
79. Leon S, Touraine B, Ribot C, Briat JF and Lobreaux S (2003) Iron-sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371, 823-830.
80. Levitan A, Danon A and Lisowsky T (2004) Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279, 20002-20008.
81. Lill R and Muhlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30, 133-141.
82. Lister R, Chew O, Rudhe C, Lee MN and Whelan J (2001) Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett 506, 291-295.
83. Little HN and Jones OT (1976) The subcellular loclization and properties of the ferrochelatase of etiolated barley. Biochem J 156, 309-314.
84. Lohrmann J, Sweere U, Zabaleta E, et al. (2001) The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol Genet Genomics 265, 2-13.
85. Loiseau L, Ollagnier-de-Choudens S, Nachin L, Fontecave M and Barras F (2003) Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J Biol Chem 278, 38352-38359.
86. Mackenzie SA and McIntosh L (1999) Higher plant mitochondria. Plant Cell 11, 571-585.
87. Marienfeld JR and Newton KJ (1994) The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics 138, 855-863.
88. Masuda T, Suzuki T, Shimada H, Ohta H and Takamiya K (2003) Subcellular localization of two types of ferrochelatase in cucumber. Planta 217, 602-609.
89. Maxwell DP, Wang Y and McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96, 8271-8276.
90. Meyer EH, Giegé P, Gelhaye E, et al. (2005) AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c. Proc Natl Acad Sci USA 102, 16113-16118.
91. Millar AH, Eubel H, Jansch L, Kruft V, Heazlewood JL and Braun HP (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol Biol 56, 77-90.
92. Millar AH, Sweetlove LJ, Giegé P and Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127, 1711-1727.
93. Moller IM and Kristensen BK (2004) Protein oxidation in plant mitochondria as a stress indicator. Photochem Photobiol Sci 3, 730-735.
94. Moulin M and Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33, 737-742.
95. Moye-Rowley WS (2005) Retrograde regulation of multidrug resistance in Saccharomyces cerevisiae. Gene 354, 15-21.
96. Muhlenhoff U and Lill R (2000) Biogenesis of iron-sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochim Biophys Acta 1459, 370-382.
97. Neill S, Desikan R and Hancock J (2002a) Hydrogen peroxide signalling. Curr Opin Plant Biol 5, 388-395.
98. Neill SJ, Desikan R, Clarke A, Hurst RD and Hancock JT (2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53, 1237-1247.
99. Newton KJ, Knudsen C, Gabay-Laughnan S and Laughnan JR (1990) An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell 2, 107-113.
100. Newton KJ, Mariano JM, Gibson CM, Kuzmin E and Gabay-Laughnan S (1996) Involvement of S2 episomal sequences in the generation of NCS4 deletion mutation in maize mitochondria. Dev Genet 19, 277-286.
101. Nicholson DW, Stuart RA and Neupert W (1989) Biogenesis of cytochrome c1. Role of cytochrome c1 heme lyase and of the two proteolytic processing steps during import into mitochondria. J Biol Chem 264, 10156-10168.
102. Nijtmans LG, Artal SM, Grivell LA and Coates PJ (2002) The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 59, 143-155.
103. Nobrega MP, Bandeira SC, Beers J and Tzagoloff A (2002) Characterization of COX19, a widely distributed gene required for expression of mitochondrial cytochrome oxidase. J Biol Chem 277, 40206-40211.
104. Nobrega MP, Nobrega FG and Tzagoloff A (1990) COX10 codes for a protein homologous to the ORF1 product of Paracoccus denitrificans and is required for the synthesis of yeast cytochrome oxidase. J Biol Chem 265, 14220-14226.
105. Noctor G, Dutilleul C, De Paepe R and Foyer CH (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J Exp Bot 55, 49-57.
106. Nott A, Jung HS, Koussevitzky S and Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57, 739-759.
107. op denCamp RG, Przybyla D, Ochsenbein C, et al. (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320-2332.
108. Palumaa P, Kangur L, Voronova A and Sillard R (2004) Metal-binding mechanism of Cox17, a copper chaperone for cytochrome c oxidase. Biochem J 382, 307-314.
109. Parisi G, Perales M, Fornasari MS, et al. (2004) Gamma carbonic anhydrases in plant mitochondria. Plant Mol Biol 55, 193-207.
110. Perales M, Eubel H, Heinemeyer J, Colaneri A, Zabaleta E and Braun HP (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I +III2 levels and alters mitochondrial physiology in Arabidopsis. J Mol Biol 350, 263-277.
111. Perales M, Parisi G, Fornasari MS, et al. (2004) Gamma carbonic anhydrase like complex interact with plant mitochondrial complex I. Plant Mol Biol 56, 947-957.
112. Picciocchi A, Douce R and Alban C (2003) The plant biotin synthase reaction. Identification and characterization of essential mitochondrial accessory protein components. J Biol Chem 278, 24966-24975.
113. Pickova A, Potocky M and Houstek J (2005) Assembly factors of F1FO-ATP synthase across genomes. Proteins 59, 393-402.
114. Plesofsky N, Gardner N, Videira A and Brambl R (2000) NADH dehydrogenase in Neurospora crassa contains myristic acid covalently linked to the ND5 subunit peptide. Biochim Biophys Acta 1495, 223-230.
115. Porra RJ and Lascelles J (1968) Studies on ferrochelatase. The enzymic formation of haem in proplastids, chloroplasts and plant mitochondria. Biochem J 108, 343-348.
116. Ribas-Carbo M, Taylor NL, Giles L, et al. (2005) Effects of water stress on respiration in soybean leaves. Plant Physiol 139, 466-473.
117. Ribichich KF, Tioni MF, Chan RL and Gonzalez DH (2001) Cell-type-specific expression of plant cytochrome c mRNA in developing flowers and roots. Plant Physiol 125, 1603-1610.
118. Rouhier N, Gelhaye E and Jacquot JP (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61, 1266-1277.
119. Sacconi S, Trevisson E, Pistollato F, et al. (2005) hCOX18 and hCOX19: two human genes involved in cytochrome c oxidase assembly. Biochem Biophys Res Commun 337, 832-839.
120. Sakamoto W, Spielewoy N, Bonnard G, Murata M and Wintz H (2000) Mitochondrial localization of AtOXA1, an arabidopsis homologue of yeast Oxa1p involved in the insertion and assembly of protein complexes in mitochondrial inner membrane. Plant Cell Physiol 41, 1157-1163.
121. Saracco SA and Fox TD (2002) Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane. Mol Biol Cell 13, 1122-1131.
122. Schmidt-Bleek K, Heiser V, Thieck O, Brennicke A and Grohmann L (1997) The 28.5-kDa iron-sulfur protein of mitochondrial complex I is encoded in the nucleus in plants. Mol Gen Genet 253, 448-454.
123. Schneider R, Brors B, Massow M and Weiss H (1997) Mitochondrial fatty acid synthesis: a relic of endosymbiontic origin and a specialized means for respiration. FEBS Lett 407, 249-252.
124. Schulte U (2001) Biogenesis of respiratory complex I. J Bioenerg Biomembr 33, 205-212.
125. Schulze M and Rodel G (1988) SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol Gen Genet 211, 492-498.
126. Shintani DK and Ohlrogge JB (1994) The characterization of a mitochondrial acyl carrier protein isoform isolated from Arabidopsis thaliana. Plant Physiol 104, 1221-1229.
127. Smart CJ, Moneger F and Leaver CJ (1994) Cell-specific regulation of gene expression in mitochondria during another development in sunflower. Plant Cell 6, 811-825.
128. Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9, 214-219.
129. Smith AG, Marsh O and Elder GH (1993) Investigation of the subcellular location of the tetrapyrrolebiosynthesis enzyme coproporphyrinogen oxidase in higher plants. Biochem J 292, 503-508.
130. Spielewoy N, Schulz H, Grienenberger JM, Thony-Meyer L and Bonnard G (2001) CCME, a nuclearencoded heme-binding protein involved in cytochrome c maturation in plant mitochondria. J Biol Chem 276, 5491-5497.
131. Stahl A, Nilsson S, Lundberg P, et al. (2005) Two novel targeting peptide degrading proteases, PrePs, in mitochondria and chloroplasts, so similar and still different. J Mol Biol 349, 847-860.
132. Strand A, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421, 79-83.
133. Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74, 787-799.
134. Svensson AS and Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28, 73-82.
135. Sweere U, Eichenberg K, Lohrmann J, et al. (2001) Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294, 1108-1111.
136. Takubo K, Morikawa T, Nonaka Y, et al. (2003) Identification and molecular characterization of mitochondrial ferredoxins and ferredoxin reductase from Arabidopsis. Plant Mol Biol 52, 817-830.
137. Tatsuta T, Model K and Langer T (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16, 248-259.
138. Thony-Meyer L (2002) Cytochrome c maturation: a complex pathway for a simple task? Biochem Soc Trans 30, 633-638.
139. Thöny-Meyer L (1997) Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61, 337-376.
140. Thöny-Meyer L, Fischer F, Kunzler P, Ritz D and Hennecke H (1995) Escherichia coli genes required for cytochrome c maturation. J Bacteriol 177, 4321-4326.
141. Tone Y, Kawai-Yamada M and Uchimiya H (2004) Isolation and characterization of Arabidopsis thaliana ISU1 gene. Biochim Biophys Acta 1680, 171-175.
142. Tremousaygue D, Garnier L, Bardet C, Dabos P, Herve C and Lescure B (2003) Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J 33, 957-966.
143. Twell D, Yamaguchi J, Wing RA, Ushiba J and McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev 5, 496-507.
144. Tzagoloff A, Barrientos A, Neupert W and Herrmann JM (2004) Atp10p assists assembly of Atp6p into the F0 unit of the yeast mitochondrial ATPase. J Biol Chem 279, 19775-19780.
145. Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J and Nijtmans L (2004) Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum Mol Genet 13, 2461-2472.
146. Unseld M, Marienfeld JR, Brandt P and Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nature Genet 15, 57-61.
147. Urantowka A, Knorpp C, Olczak T, Kolodziejczak M and Janska H (2005) Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol Biol 59, 239-252.
148. van Lis R, Atteia A, Nogaj LA and Beale SI (2005) Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii. Plant Physiol 139, 1946-1958.
149. van Steensel B (2005) Mapping of genetic and epigenetic regulatory networks using microarrays. Nat Genet 37 (Suppl.), S18-S24.
150. Vogel RO, Janssen RJ, Ugalde C, et al. (2005) Human mitochondrial complex I assembly is mediated by NDUFAF1. Febs J 272, 5317-5326.
151. Vranova E, Inze D and Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53, 1227-1236.
152. Wagner AM (1995) Arole for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett 368, 339-342.
153. Wagner D, Przybyla D, Op den Camp R, et al. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185.
154. Watanabe N, Che FS, Iwano M, Takayama S, Yoshida S and Isogai A (2001) Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem 276, 20474-20481.
155. Welchen E, Chan RL and Gonzalez DH (2004) The promoter of the Arabidopsis nuclear gene COX5b-1, encoding subunit 5b of the mitochondrial cytochrome c oxidase, directs tissue-specific expression by a combination of positive and negative regulatory elements. J Exp Bot 55, 1997-2004.
156. Welchen E and Gonzalez DH (2005) Differential expression of the Arabidopsis cytochrome c genes Cytc-1 and Cytc-2. Evidence for the involvement of TCP-domain protein-binding elements in anther- and meristem-specific expression of the Cytc-1 gene. Plant Physiol 139, 88-100.
157. Welchen E and Gonzalez DH (2006) Overexpression of elements recognised by TCP-domain transcription factors in the upstream regions of nuclear genes encoding components of the mitochondrial oxidative phosphorylation machinery. Plant Physiol 141, 540-545.
158. Wood CK, Dudley P, Albury MS, et al. (1996) Developmental regulation of respiratory activity and protein import in plant mitochondria. Biochem Soc Trans 24, 746-749.
159. Wu M and Tzagoloff A (1989) Identification and characterization of a new gene (CBP3) required for the expression of yeast coenzyme QH2-cytochrome c reductase. J Biol Chem 264, 11122-11130.
160. Xu XM and Moller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25, 900-909.
161. Yabe T, Morimoto K, Kikuchi S, Nishio K, Terashima I and Nakai M (2004) The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron-sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I. Plant Cell 16, 993-1007.
162. Zabaleta E, Heiser V, Grohmann L and Brennicke A (1998) Promoters of nuclear-encoded respiratory chain complex I genes from Arabidopsis thaliana contain a region essential for anther/pollenspecific expression. Plant J 15, 49-59.
163. Zara V, Palmisano I, Conte L and Trumpower BL (2004) Further insights into the assembly of the yeast cytochrome bc1 complex based on analysis of single and double deletion mutants lacking supernumerary subunits and cytochrome b. Eur J Biochem 271, 1209-1218.
164. Zarkovic J, Anderson SL and Rhoads DM (2005) A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis. Plant Mol Biol 57, 871-888.
165. Zollner A, Rodel G and Haid A (1992) Molecular cloning and characterisation of S. cerevisiae CYT2 gene encoding cytochrome-c1-heme lyase. Eur J Biochem 207, 1093-1100.