Protein import into plant mitochondria: Signals, machinery, processing, and regulation

Journal of Experimental Botany

Volumn 65, Issue 22, 2014, Pages 6301-6335

  Murcha, Monika W ^a   Kmiec, Beata ^b   Kubiszewski Jakubiak, Szymon ^a,c   Teixeira, Pedro F ^a,b   Glaser, Elzbieta ^a   Whelan, James ^c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Dual targeting; mitochondria; peptidase; protein import; signalling; targeting signals.

Indexed keywords

SACCHAROMYCES CEREVISIAE;

VEGETABLE PROTEIN;

METABOLISM; MITOCHONDRION; PLANT; PROTEIN PROCESSING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

MITOCHONDRIA; PLANT PROTEINS; PLANTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84921352947     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru399     Document Type: Review

References (348)

1. Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D. 2000. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100, 551-560
2. Adams KL, Palmer JD. 2003. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Molecular Phylogenetics and Evolution 29, 380-395
3. Agne B, Infanger S, Wang F, Hofstetter V, Rahim G, Martin M, Lee DW, Hwang I, Schnell D, Kessler F. 2009. A toc159 import receptor mutant, Defective in hydrolysis of GTP, supports preprotein import into chloroplasts. Journal of Biological Chemistry 284, 8670-8679
4. Alkhaja AK, Jans DC, Nikolov M, et al. 2012. MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Molecular Biology of the Cell 23, 247-257
5. Apel W, Schulze WX, Bock R. 2010. IDentification of protein stability Determinants in chloroplasts. The Plant Journal 63, 636-650
6. Armstrong LC, Komiya T, Bergman BE, Mihara K, Bornstein P. 1997. Metaxin is a component of a preprotein import complex in the outer membrane of the mammalian mitochondrion. Journal of Biological Chemistry 272, 6510-6518
7. Aronsson H, Jarvis P. 2011. Dimerization of TOC receptor GTPases and its implementation for the control of protein import into chloroplasts. Biochemical Journal 436, e1-e2
8. Bachmair A, Finley D, Varshavsky A. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186
9. Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I. 2008. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nature Cell Biology 10, 220-227
10. Baglieri J, Beck D, Vasisht N, Smith CJ, Robinson C. 2012. Structure of TatA paralog TatE, suggests a structurally homogeneous form of Tat protein translocase that transports folDed proteins of differing diameter. Journal of Biological Chemistry 287, 7335-7344
11. Bahaji A, Munoz FJ, Ovecka M, et al. 2011. Specific Delivery of AtBT1 to mitochondria complements the aberrant growth and sterility phenotype of homozygous Atbt1 Arabidopsis mutants. The Plant Journal 68, 1115-1121
12. Bassham DC, Bartling D, Mould RM, Dunbar B, Weisbeek P, Herrmann RG, Robinson C. 1991. Transport of proteins into chloroplasts. Delineation of envelope transit and thylakoid transfer signals within the pre-sequences of three imported thylakoid lumen proteins. Journal of Biological Chemistry 266, 23606-23610
13. Basu S, Leonard JC, Desai N, Mavridou DA, Tang KH, Goddard AD, Ginger ML, Lukes J, Allen JW 2013. Divergence of Erv1-Associated mitochondrial import and export pathways in trypanosomes and anaerobic protists. Eukaryotic Cell 12, 343-355
14. Battersby BJ, Richter U. 2013. Why translation counts for mitochondria-retrograDe signalling links mitochondrial protein synthesis to mitochondrial biogenesis and cell proliferation. Journal of Cell Science 126, 4331-4338
15. Baudisch B, Klosgen RB 2012. Dual targeting of a processing peptidase into both endosymbiotic organelles mediated by a transport signal of unusual architecture. Molecular Plant 5, 494-503
16. Baudisch B, Langner U, Garz I, Klosgen RB 2014. The exception proves the rule? Dual targeting of nuclear-encoDed proteins into endosymbiotic organelles. New Phytologist 201, 80-90
17. Becker T, Wenz LS, Thornton N, Stroud D, Meisinger C, WieDemann N, Pfanner N. 2011. Biogenesis of mitochondria: dual role of Tom7 in modulating assembly of the preprotein translocase of the outer membrane. Journal of Molecular Biology 405, 113-124
18. Bdard J, Jarvis P. 2008. Green light for chloroplast outer-membrane proteins. Nature Cell Biology 10, 120-122
19. Benz M, Soll J, Ankele E. 2013. Arabidopsis thaliana Oxa proteins locate to mitochondria and fulfill essential roles during embryo Development. Planta 237, 573-588
20. Berger KH, Sogo LF, Yaffe MP 1997. Mdm12p, a component required for mitochondrial inheritance that is conserved between budding and fission yeast. Journal of Cell Biology 136, 545-553
21. Berglund AK, Pujol C, Duchene AM, Glaser E (2009a). Defining the Determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts. Journal of Molecular Biology 393, 803-814
22. Berglund AK, Spanning E, Biverstahl H, Maddalo G, Tellgren-Roth C, Maler L, Glaser E (2009b). Dual targeting to mitochondria and chloroplasts: characterization of Thr-tRNA synthetase targeting peptiDe. Molecular Plant 2, 1298-1309
23. Bhushan S, Kuhn C, Berglund AK, Roth C, Glaser E. 2006. The role of the N-terminal domain of chloroplast targeting peptiDes in organellar protein import and miss-sorting. FEBS Letters 580, 3966-3972
24. Bhushan S, Lefebvre B, Stahl A, Wright SJ, Bruce BD, Boutry M, Glaser E. 2003. Dual targeting and function of a protease in mitochondria and chloroplasts. EMBO Reports 4, 1073-1078
25. Bhushan S, Stahl A, Nilsson S, et al. 2005. Catalysis, subcellular localization, expression and evolution of the targeting peptiDes Degrading protease AtPreP2. Cell 46, 985-996
26. Bohnert M, Rehling P, Guiard B, Herrmann JM, Pfanner N, Van Der Laan M. 2010. Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport. Current Biology 20, 1227-1232
27. Bohnert M, Wenz LS, Zerbes RM, et al. 2012. Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane. Molecular Biology of the Cell 23, 3948-3956
28. BolenDer N, Sickmann A, Wagner R, Meisinger C, Pfanner N. 2008. Multiple pathways for sorting mitochondrial precursor proteins. EMBO Reports 9, 42-49
29. Bomer U, Meijer M, Guiard B, Dietmeier K, Pfanner N, Rassow J. 1997. The sorting route of cytochrome b2 branches from the general mitochondrial import pathway at the preprotein translocase of the inner membrane. Journal of Biological Chemistry 272, 30439-46
30. Boutry M, Nagy F, Poulsen C, Aoyagi K, Chua NH 1987. Targeting of bacterial chloramphenicol acetyltransferase to mitochondria in transgenic plants. Nature 328, 340-342
31. Branda SS, Yang ZY, Chew A, Isaya G. 1999. Mitochondrial intermediate peptidase and the yeast frataxin homolog together maintain mitochondrial iron homeostasis in Saccharomyces cerevisiae. Human Molecular Genetics 8, 1099-1110
32. Brandt U, Yu L, Yu CA, Trumpower BL 1993. The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc1 complex in mammals and retained as a subunit in the complex. Journal of Biological Chemistry 268, 8387-8390
33. Braun HP, BinDer S, Brennicke A, et al. 2014. The life of plant mitochondrial complex I. Mitochondrion doi: S1567-7249(14)00020-8 [Epub ahead of print].
34. Braun HP, Emmermann M, Kruft V, Schmitz UK 1992. The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO Journal 11, 3219-3227
35. Braun HP, Schmitz UK. 1995. Are the core proteinsof the mitochondrial bc1 complex evolutionary relics of a processing protease? Trends in Biochemical Science 20, 171-175
36. Brink S, Flugge UI, Chaumont F, Boutry M, Emmermann M, Schmitz U, Becker K, Pfanner N. 1994. Preproteins of chloroplast envelope inner membrane contain targeting information for receptor-DepenDent import into fungal mitochondria. Journal of Biological Chemistry 269, 16478-16485
37. Brix J, Dietmeier K, Pfanner N. 1997. Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20 Tom22, and Tom70. Journal of Biological Chemistry 272, 20730-20735
38. Bruce BD. 2000. Chloroplast transit peptiDes: structure, function and evolution. Trends in Cell Biology 10, 440-447
39. Bruce BD. 2001. The paradox of plastid transit peptiDes: conservation of function Despite divergence in primary structure. Biochimica et Biophysica Acta 1541, 2-21
40. Brumme S, Kruft V, Schmitz UK, Braun HP. 1998. New insights into the co-evolution of cytochrome c reductase and the mitochondrial processing peptidase. Journal of Biological Chemistry 273, 13143-9
41. Burger G, Gray MW, Forget L, Lang BF 2013. Strikingly bacterialike and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biology and Evolution 5, 418-438
42. Burgess SM, Delannoy M, Jensen RE 1994. MMM1 encoDes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. Journal of Cell Biology 126, 1375-1391
43. Busi MV, Gomez-Lobato ME, Rius SP, Turowski VR, Casati P, Zabaleta EJ, Gomez-Casati DF, Araya A. 2011. Effect of mitochondrial dysfunction on carbon metabolism and gene expression in flower tissues of Arabidopsis thaliana. Molecular Plant 4, 127-143
44. Carrie C, Small I. 2013. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochimica et Biophysica Acta 1833, 253-259
45. Carrie C, Whelan J. 2013. WiDespread dual targeting of proteins in land plants: when, where, how and why. Plant Signal Behav 8.
46. Carrie C, Giraud E, Whelan J. 2009. Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS Journal 276, 1187-1195
47. Carrie C, Giraud E, Duncan O, et al. 2010a. Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. Journal of Biological Chemistry 285, 36138-48
48. Carrie C, Giraud E, Duncan O, et al. 2010b. Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. Journal of Biological Chemistry 285, 36138-48
49. Carrie C, Murcha MW, Whelan J. 2010c. An in silico analysis of the mitochondrial protein import apparatus of plants. BMC Plant Biology 10, 249.
50. Carroll J, Shannon RJ, Fearnley IM, Walker JE, Hirst J. 2002. Definition of the nuclear encoDed protein composition of bovine heart mitochondrial complex I. IDentification of two new subunits. Journal of Biological Chemistry 277, 50311-7
51. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644
52. Chacinska A, Lind M, Frazier AE, et al. 2005. Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17. Cell 120, 817-829
53. Chacinska A, Pfannschmidt S, WieDemann N, Kozjak V, Sanjuan Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, Pfanner N. 2004. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO Journal 23, 3735-3746
54. Chacinska A, Van Der Laan M, Mehnert CS, et al. 2010. Distinct forms of mitochondrial TOM-TIM supercomplexes Define signal-DepenDent states of preprotein sorting. Molecular and Cellular Biology 30, 307-318
55. Chan NC, Lithgow T. 2008. The peripheral membrane subunits of the SAM complex function coDepenDently in mitochondrial outer membrane biogenesis. Molecular Biology of the Cell 19, 126-136
56. Chew O, Lister R, Qbadou S, Heazlewood JL, Soll J, Schleiff E, Millar AH, Whelan J. 2004. A plant outer mitochondrial membrane protein with high amino acid sequence iDentity to a chloroplast protein import receptor. FEBS Letters 557, 109-114
57. Chew O, Whelan J, Millar AH. 2003. Molecular Definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant Defenses in plants. Journal of Biological Chemistry 278, 46869-46877
58. Chotewutmontri P, Reddick LE, McWilliams DR, Campbell IM, Bruce BD. 2012. Differential transit peptiDe recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 24, 3040-3059
59. Christensen AC, Lyznik A, Mohammed S, Elowsky CG, Elo A, Yule R, Mackenzie AS 2005. Dual-domian, dual-targeting organelle protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 17, 2805-2816
60. Cleary SP, Tan FC, Nakrieko KA, Thompson SJ, Mullineaux PM, Creissen GP, von Stedingk E, Glaser E, Smith AG, Robinson C. 2002. Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. Journal of Biological Chemistry 277, 5562-5569
61. Court DA, Nargang FE, Steiner H, Hodges RS, Neupert W, Lill R. 1996. Role of the intermembrane-space domain of the preprotein receptor Tom22 in protein import into mitochondria. Molecular Cell Biology 16, 4035-4042
62. Creissen G, Reynolds H, Xue Y, Mullineaux P. 1995. Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. The Plant Journal 8, 167-175
63. Dabney-Smith C, Van Den Wijngaard PW, Treece Y, VreDenberg WJ, Bruce BD. 1999. The C terminus of a chloroplast precursor modulates its interaction with the translocation apparatus and PIRAC. Journal of Biological Chemistry 274, 32351-9
64. Daley DO, Adams KL, Clifton R, Qualmann S, Millar AH, Palmer JD, Pratje E, Whelan J. 2002. Gene transfer from mitochondrion to nucleus: novel mechanisms for gene activation from Cox2. The Plant Journal 30, 11-21
65. Danpure CJ. 1995. How can the products of a single gene be localized to more than one intracellular compartment? Trends in Cell Biology 5, 230-238
66. Daras G, Rigas S, Tsitsekian D, Zur H, Tuller T, Hatzopoulos P. 2014. Alternative transcription initiation and the AUG context configuration control dual-organellar targeting and functional competence of Arabidopsis Lon1 protease. Molecular Plant 7, 989-1005
67. Darshi M, Trinh KN, Murphy AN, Taylor SS. 2012. Targeting and import mechanisms of coiled-coil helix coiled-coil helix domain-containing protein 3 (ChChd3) into the mitochondrial intermembrane space. Journal of Biological Chemistry 287, 39480-39491
68. Davis AJ, AlDer NN, Jensen RE, Johnson AE. 2007. The Tim9p/10p and Tim8p/13p complexes bind to specific sites on Tim23p during mitochondrial protein import. Molecular Biology of the Cell 18, 475-486
69. Davis AJ, Sepuri NB, HolDer J, Johnson AE, Jensen RE. 2000. Two intermembrane space TIM complexes interact with different domains of Tim23p during its import into mitochondria. Journal of Cell Biology 150, 1271-1282
70. De Clercq I, Vermeirssen V, Van Aken O, et al. 2013. The membranebound NAC transcription factor ANAC013 functions in mitochondrial retrograDe regulation of the oxidative stress response in Arabidopsis. Plant Cell 25, 3472-3490
71. Dekker PJ, Keil P, Rassow J, Maarse AC, Pfanner N, Meijer M. 1993. IDentification of MIM23, a putative component of the protein import machinery of the mitochondrial inner membrane. FEBS Letters 330, 66-70
72. Delage L, Leblanc C, Nyvall Collen P, Gschloessl B, Oudot MP, Sterck L, Poulain J, Aury JM, Cock JM. 2011. In silico survey of the mitochondrial protein uptake and maturation systems in the brown alga Ectocarpus siliculosus. PLoS One 6, e19540.
73. Deng Y, Zou W, Li G, Zhao J. 2014. AtTIM9 and AtTIM10 are essential for maintaining mitochondrial function during early embryo cell and endosperm free-nucleus divisions in Arabidopsis. Plant Physiology doi:10.1104/pp.114.242560 [Epub ahead of print].
74. Dessi P, Whelan J. 1997. Temporal regulation of in vitro import of precursor proteins into tobacco mitochondria. FEBS Letters 415, 173-178
75. Dessi P, Pavlov PF, Wallberg F, Rudhe C, Brack S, Whelan J, Glaser E. 2003. Investigations on the in vitro import ability of mitochondrial precursor proteins synthesized in wheat germ transcription-translation extract. Plant Molecular Biology 52, 259-271
76. Dietmeier K, Honlinger A, Bomer U, Dekker PJ, Eckerskorn C, Lottspeich F, Kubrich M, Pfanner N. 1997. Tom5 functionally links mitochondrial preprotein receptors to the general import pore. Nature 388, 195-200
77. Dimmer KS, Rapaport D. 2012. Unresolved mysteries in the biogenesis of mitochondrial membrane proteins. Biochimica et Biophysica Acta 1818, 1085-1090
78. Dimmer KS, Papic D, Schumann B, Sperl D, Krumpe K, Walther DM, Rapaport D. 2012. A crucial role for Mim2 in the biogenesis of mitochondrial outer membrane proteins. Journal of Cell Science 125, 3464-3473
79. Donzeau M, Kaldi K, Adam A, Paschen S, Wanner G, Guiard B, Bauer MF, Neupert W, Brunner M. 2000. Tim23 links the inner and outer mitochondrial membranes. Cell 101, 401-412
80. Duchene AM, Giege P. 2012. Dual localized mitochondrial and nuclear proteins as gene expression regulators in plants? Frontiers in Plant Science 3, 221.
81. Dudley P, Wood CK, Pratt JR, Moore AL. 1997. Developmental regulation of the plant mitochondrial matrix located HSP70 chaperone and its role in protein import. FEBS Letters 417, 321-324
82. Duncan O, Murcha MW, Whelan J. 2013. Unique components of the plant mitochondrial protein import apparatus. Biochimica et Biophysica Acta 1833, 304-313
83. Dvorakova-Hola K, Matuskova A, Kubala M, Otyepka M, Kucera T, Vecer J, Herman P, Parkhomenko N, Kutejova E, Janata J. 2010. Glycine-rich loop of mitochondrial processing peptidase -subunit is responsible for substrate recognition by a mechanism analogous to mitochondrial receptor Tom20. Journal of Molecular Biology 396, 1197-1210
84. Eliyahu E, Pnueli L, Melamed D, Scherrer T, Gerber AP, Pines O, Rapaport D, Arava Y. 2010. Tom20 mediates localization of mRNAs to mitochondria in a translation-DepenDent manner. Molecular Cell Biology 30, 284-294
85. Endo T, Yamano K, Kawano S. 2011. Structural insight into the mitochondrial protein import system. Biochimica et Biophysica Acta 1808, 955-970
86. Endres M, Neupert W, Brunner M. 1999. Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO Journal 18, 3214-3221
87. Esser K, Tursun B, Ingenhoven M, Michaelis G, Pratje E. 2002. A novel two-step mechanism for removal of a mitochondrial signal sequence involves the mAAA complex and the putative rhomboid protease Pcp1. Journal of Molecular Biology 323, 835-843
88. Falkevall A, Alikhani N, Bhushan S, Pavlov PF, Busch K, Johnson KA, Eneqvist T, Tjernberg L, Ankarcrona M, Glaser E. 2006. Degradation of the amyloid beta-protein by the novel mitochondrial peptidasome PreP. Journal of Biological Chemistry 281, 29096-29104
89. Ferramosca A, Zara V. 2013. Biogenesis of mitochondrial carrier proteins: molecular mechanisms of import into mitochondria. Biochimica et Biophysica Acta 1833, 494-502
90. Fischer M, Riemer J. 2013. The mitochondrial disulfiDe relay system: roles in oxidative protein folding and beyond. International Journal of Cell Biology 2013, 742923.
91. Flores-Perez U, Jarvis P. 2013. Molecular chaperone involvement in chloroplast protein import. Biochimica et Biophysica Acta 1833, 332-340
92. Formighieri C, Cazzaniga S, Kuras R, Bassi R. 2013. Biogenesis of photosynthetic complexes in the chloroplast of Chlamydomonas reinhardtii requires ARSA1, a homolog of prokaryotic arsenite transporter and eukaryotic TRC40 for guiDed entry of tail-Anchored proteins. The Plant Journal 73, 850-886
93. Fraga H, Bech-Serra JJ, Canals F, Ortega G, Millet O, Ventura S. 2014. The mitochondrial intermembrane space oxireductase Mia40 funnels the oxidative folding pathway of the cytochrome c oxidase assembly protein cox19. Journal of Biological Chemistry 289, 9852-9864
94. Frazier AE, DuDek J, Guiard B, et al. 2004. Pam16 has an essential role in the mitochondrial protein import motor. Nature Structural &Molecular Biology 11, 226-233
95. Gabriel K, Milenkovic D, Chacinske A, Muller J, Pfanner N, Meisinger C. 2007. Novel mitochondrial intermembrane space proteins as substrates of the MIA import pathway. Journal of Molecular Biology 365, 612-620
96. Gavel Y, von Heijne G. 1990. Cleavage-site motifs in mitochondrial targeting peptiDes. Protein Engineering 4, 33-37
97. Ge C, Spanning E, Glaser E, WieslanDer A. 2014. Import Determinants of organelle-specific and dual targeting peptiDes of mitochondria and chloroplasts in Arabidopsis thaliana. Molecular Plant 7, 121-136
98. Gebert M, Schrempp SG, Mehnert CS, et al. 2012. Mgr2 promotes coupling of the mitochondrial presequence translocase to partner complexes. Journal of Cell Biology 197, 595-604
99. Gebert N, Gebert M, Oeljeklaus S, et al. 2011. Dual function of Sdh3 in the respiratory chain and TIM22 protein translocase of the mitochondrial inner membrane. Molecular Cell 44, 811-818
100. Gentle IE, Perry AJ, Alcock FH, et al. 2007. Conserved motifs reveal Details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Molecular Biology and Evolution 24, 1149-1160
101. Gerbeth C, Schmidt O, Rao S, Harbauer AB, Mikropoulou D, Opalinska M, Guiard B, Pfanner N, Meisinger C. 2013. Glucoseinduced regulation of protein import receptor Tom22 by cytosolic and mitochondria-bound kinases. Cell Metabolism 18, 578-587
102. Giraud E, Ng S, Carrie C, Duncan O, Low J, Lee CP, Van Aken O, Millar AH, Murcha M, Whelan J. 2010. TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. The Plant Cell 22, 3921-3934
103. Glaser E, Dessi P. 1999. Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J, Bioenerg Biomembr 31, 259-274
104. Glaser E, Eriksson A, Sjoling S. 1994. Bifunctional role of the bc1 complex in plants. Mitochondrial bc1 complex catalyses both electron transport and protein processing. FEBS Letters 346, 83-87
105. Glaser E, Sjoling S, Tanudji M, Whelan J. 1998. Mitochondrial protein import in plants. Signals, sorting, targeting, processing and regulation. Plant Moleclar Biology 38, 311-338
106. Graham JW, Williams TC, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ. 2007. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory Demand and support substrate channeling. Plant Cell 19, 3723-3738
107. Gray MW. 2012. Mitochondrial evolution. Cold Spring Harbor Perspectives in Biology 4, a011403.
108. Hachiya N, Komiya T, Alam R, Iwahashi J, Sakaguchi M, Omura T, Mihara K. 1994. MSF, a novel cytoplasmic chaperone which functions in precursor targeting to mitochondria. EMBO Journal 13, 5146-5154
109. Hamasaki H, Yoshizumi T, Takahashi N, Higuchi M, Kuromori T, Imura Y, Shimada H, Matsui M. 2012. SD3, an Arabidopsis thaliana homolog of TIM21, affects intracellular ATP levels and seedling Development. Molecular Plant 5, 461-471
110. Harmey MA, Hallermayer G, Korb H, Neupert W. 1977. Transport of cytoplasmically synthesized proteins into the mitochondria in a cell free system from Neurospora crassa. European Journal of Biochemistry 81, 533-544
111. Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W. 2011. The mitochondrial contact site complex, a Determinant of mitochondrial architecture. EMBO Journal 30, 4356-4370
112. Hawlitschek G, SchneiDer H, Schmidt B, Tropschug M, Hartl FU, Neupert W. 1988. Mitochondrial protein import: iDentification of processing peptidase and of PEP, a processing enhancing protein. Cell 53, 795-806
113. Hedtke B, Borner T, Weihe A. 2000. One RNA polymerase serving two genomes. EMBO Reports 1, 435-440
114. Heins L, Schmitz UK. 1996. A receptor for protein import into potato mitochondria. The Plant Journal 9, 829-839
115. Hell K. 2008. The Erv1-Mia40 disulfiDe relay system in the intermembrane space of mitochondria. Biochimica et Biophysica Acta 1783, 601-609
116. Herrmann JM, Riemer J. 2012. Mitochondrial disulfiDe relay: redoxregulated protein import into the intermembrane space. Journal of Biological Chemistry 287, 4426-4433
117. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, Nunnari J. 2011. A mitochondrial-focused genetic interaction map reveals a scaffoldlike complex required for inner membrane organization in mitochondria. Journal of Cell Biology 195, 323-340
118. Howell KA, Cheng K, Murcha MW, Jenkin LE, Millar AH, Whelan J. 2007. Oxygen initiation of respiration and mitochondrial biogenesis in rice. Journal of Biological Chemistry 282, 15619-15631
119. Howell KA, Millar AH, Whelan J. 2006. OrDered assembly of mitochondria during rice germination begins with pro-mitochondrial structures rich in components of the protein import apparatus. Plant Molecular Biology 60, 201-223
120. Howell SH. 2013. Endoplasmic reticulum stress responses in plants. Annual Review of Plant Biology 64, 477-499
121. Huang J, Hack E, Thornburg RW, Myers AM. 1990. A yeast mitochondrial leaDer peptiDe functions in vivo as a dual targeting signal for both chloroplasts and mitochondria. Plant Cell 2, 1249-1260
122. Huang S, Taylor NL, Narsai R, Eubel H, Whelan J, Millar AH. 2009a. Experimental analysis of the rice mitochondrial proteome, its biogenesis, and heterogeneity. Plant Physiology 149, 719-734
123. Huang S, Taylor NL, Whelan J, Millar AH. 2009b. Refining the Definition of plant mitochondrial presequences through analysis of sorting signals N-terminal modifications, and cleavage motifs. Plant Physiology 150, 1272-1285
124. Hugosson M, Andreu D, Boman HG, Glaser E. 1994. Antibacterial peptiDes and mitochondrial presequences affect mitochondrial coupling, respiration and protein import. European Journal of Biochemistry 223, 1027-1033
125. Hurt EC, Goldschmidt-Clermont M, Pesold-Hurt B, Rochaix JD, Schatz G. 1986. A mitochondrial presequence can transport a chloroplast-encoDed protein into yeast mitochondria. Journal of Biological Chemistry 261, 11440-11443
126. Hwang YT, Pelitire SM, HenDerson MP, Andrews DW, Dyer JM, Mullen RT. 2004. Novel targeting signals mediate the sorting of different isoforms of the tail-Anchored membrane protein cytochrome b5 to either endoplasmic reticulum or mitochondria. Plant Cell 16, 3002-3019
127. Structure of the chloroplast NADH Dehydrogenase-like complex: nomenclature for nuclear-encoDed subunits. Plant Cell Physiology 52, 1560-1568
128. Isaya G, Kalousek F, Rosenberg LE. 1992. Sequence analysis of rat mitochondrial intermediate peptidase: similarity to zinc metallopeptidases and to a putative yeast homologue. Proceedings of the National AcaDemy of Sciences, USA 89, 8317-8321
129. Isaya G, Miklos D, Rollins RA. 1994. MIP1, a new yeast gene homologous to the rat mitochondrial intermediate peptidase gene, is required for oxidative metabolism in Saccharomyces cerevisiae. Molecular Cell Biology 14, 5603-5616
130. Ishikawa D, Yamamoto H, Tamura Y, Moritoh K, Endo T. 2004. Two novel proteins in the mitochondrial outer membrane mediate -barrel protein assembly. Journal of Cell Biology 166, 621-627
131. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S, Jap BK. 1998. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281, 64-71
132. Jansch L, Kruft V, Schmitz UK, Braun HP. 1998a. Unique composition of the preprotein translocase of the outer mitochondrial membrane from plants. Journal of Biological Chemistry 273, 17251-7
133. Jarosch E, Tuller G, Daum G, Waldherr M, Voskova A, Schweyen RJ 1996. Mrs5p, an essential protein of the mitochondrial intermembrane space, affects protein import into yeast mitochondria. Journal of Biological Chemistry 271, 17219-25
134. Jarvis P, Lopez-Juez E. 2014. Biogenesis and homeostasis of chloroplasts and otehr plastids. Nature Reviews Molecular Cell Biology 14, 787-802
135. Johnson KA, Bhushan S, Stahl A, Hallberg BM, Frohn A, Glaser E, Eneqvist T. 2006. The closed structure of presequence protease PreP forms a unique 10 000 A3 chamber for proteolysis. EMBO Journal 25, 1977-1986
136. Kalousek F, Hendrick JP, Rosenberg LE. 1988. Two mitochondrial matrix proteases act sequentially in the processing of mammalian matrix enzymes. Proceedings of the National AcaDemy of Sciences, USA 85, 7536-7540
137. Kambacheld M, Augustin S, Tatsuta T, Muller S, Langer T. 2005. Role of the novel metallopeptidase Mop112 and saccharolysin for the complete Degradation of proteins residing in different subcompartments of mitochondria. Journal of Biological Chemistry 280, 20132-20139
138. Kerscher O, HolDer J, Srinivasan M, Leung RS, Jensen RE. 1997. The Tim54p-Tim22p complex mediates insertion of proteins into the mitochondrial inner membrane. Journal of Cell Bioogy 139, 1663-1675
139. Kerscher O, Sepuri NB, Jensen RE. 2000. Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Molecular Biology of the Cell 11, 103-116
140. Kim DH, Xu Z-H, Na YJ, Yoo YJ, Lee J, Sohn EJ, Hwang I. 2011. Small heat shock protein Hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in Arabidopsis. Plant Physiology 157, 132-146
141. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, SjlanDer K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 15, 354-362
142. Klodmann J, Braun HP. 2011. Proteomic approach to characterize mitochondrial complex I from plants. Phytochemistry 72, 1071-1080
143. Klodmann J, Senkler M, RoDe C, Braun HP. 2011. Defining the protein complex proteome of plant mitochondria. Plant Physiology 157, 587-598
144. Klodmann J, SunDerhaus S, Nimtz M, Jansch L, Braun HP. 2010. Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell 22, 797-810
145. Kmiec B, Teixeira PF, Glaser E. 2014. Phenotypical consequences of expressing the dually targeted Presequence Protease AtPreP, exclusively in mitochondria. Biochimie 100, 167-170
146. Kmiec B, Teixeira PF, Berntsson RP, et al. 2013. Organellar oligopeptidase (OOP) proviDes a complementary pathway for targeting peptiDe Degradation in mitochondria and chloroplasts. Proceedings of the National AcaDemy of Sciences, USA 110 E3761-9
147. Kmiec B, Urantowka A, Lech M, Janska H. 2012. Two-step processing of AtFtsH4 precursor by mitochondrial processing peptidase in Arabidopsis thaliana. Molecular Plant 5, 1417-1419
148. Kmiec-Wisniewska B, Krumpe K, Urantowka A, Sakamoto W, Pratje E, Janska H. 2008. Plant mitochondrial rhomboid AtRBL12, has different substrate specificity from its yeast counterpart. Plant Molecular Biology 68, 159-171
149. Koch JR, Schmid FX. 2014. Mia40 targets cysteines in a hydrophobic environment to direct oxidative protein folding in the mitochondria. Nature Communications 5, 3041.
150. Koehler CM, Jarosch E, Tokatlidis K, Schmid K, Schweyen RJ, Schatz G. 1998. Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279, 369-373
151. Komiya T, Rospert S, Koehler C, Looser R, Schatz G, Mihara K. 1998. Interaction of mitochondrial targeting signals with acidic receptor domains along the protein import pathway: eviDence for the acid chain hypothesis. EMBO Journal 17, 3886-3898
152. Kopec KO, Alva V, Lupas AN. 2010. Homology of SMP domains to the TULIP superfamily of lipid-binding proteins proviDes a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26, 1927-1931
153. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481
154. Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. 2010. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22, 3574-3588
155. Kozjak V, WieDemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. Journal of Biological Chemistry 278, 48520-48523
156. Kozjak-Pavlovic V, Ross K, Benlasfer N, Kimmig S, Karlas A, RuDel T. 2007. Conserved roles of Sam50 and metaxins in VDAC biogenesis. EMBO Reports 8, 576-582
157. Krumpe K, Frumkin I, Herzig Y, Rimon N, Ozbalci C, Brugger B, Rapaport D, Schuldiner M. 2012. Ergosterol content specifies targeting of tail-Anchored proteins to mitochondrial outer membranes. Molecular Biology of the Cell 23, 3927-3935
158. Kuhn K, Richter U, Meyer EH, Delannoy E, De Longevialle AF, OToole N, Borner T, Millar AH, Small ID, Whelan J. 2009a. Phagetype RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 21, 2762-2779
159. Kuhn S, Bussemer J, Chigri F, Vothknecht UC. 2009a. Calcium Depletion and calmodulin inhibition affect the import of nuclear-encoDed proteins into plant mitochondria. The Plant Journal 58, 694-705
160. Kulawiak B, Hopker J, Gebert M, Guiard B, WieDemann N, Gebert N. 2013. The mitochondrial protein import machinery has multiple connections to the respiratory chain. Biochimica et Biophysica Acta 1827, 612-626
161. Kwasniak M, Majewski P, Skibior R, Adamowicz A, Czarna M, Sliwinska E, Janska H. 2013. Silencing of the nuclear RPS10 gene encoding mitochondrial ribosomal protein alters translation in Arabidopsis mitochondria. Plant Cell 25, 1855-1867
162. Kwasniak M, Pogorzelec L, Migdal I, Smakowska E, Janska H. 2012. Proteolytic system of plant mitochondria. Physiologia Plantarum 145, 187-195
163. Lamberti G, Drurey C, Soll J, Schwenkert S. 2011. The phosphorylation state of chloroplast transit peptiDes regulates preprotein import. Plant Signaling &Behaviour 6, 1918-1920
164. Lane N, Martin W. 2010. The energetics of genome complexity. Nature 467, 929-934
165. Langner U, Baudisch B, Klosgen RB. 2014. Organelle import of proteins with dual targeting properties into mitochondria and chloroplasts takes place by the general import pathways. Plant Signaling &Behaviour doi: 10.4161/psb.29301 [Epub ahead of print].
166. Law SR, Narsai R, Whelan J. 2014. Mitochondrial biogenesis in plants during seed germination. Mitochondrion doi: 10.1016/j.mito.2014.04.002 [Epub ahead of print].
167. Law SR, Narsai R, Taylor NL, Delannoy E, Carrie C, Giraud E, Millar AH, Small I, Whelan J. 2012. NucleotiDe and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiology 158, 1610-1627
168. Lee J, Lee H, Kim J, Lee S, Kim DH, Kim S, Hwang I. 2011. Both the hydrophobicity and a positively charged region flanking the C-terminal region of the transmembrane domain of signal-Anchored proteins play critical roles in Determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in Arabidopsis cells. Plant Cell 23, 1588-1607
169. IDentification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell 13, 2175-2190
170. Recent adVances in the composition and heterogeneity of the Arabidopsis mitochondrial proteome. Frontiers in Plant Science 4, 4.
171. Lee DW, Lee S, Lee GJ, Lee KH, Kim S, Cheong GW, Hwang I. 2006. Functional characterization of sequence motifs in the transit peptiDe of Arabidopsis small subunit of rubisco. Plant Physiology 140, 466-483
172. Lee J, Kim DH, Hwang I. 2014. Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Frontiers in Plant Science 5, 173.
173. Lee MN, Whelan J. 2004. IDentification of signals required for import of the soybean F(A)d subunit of ATP synthase into mitochondria. Plant Molecular Biology 54, 193-203
174. Lee S, Lee DW, Yoo YJ, Duncan O, Oh YJ, Lee YJ, Lee G, Whelan J, Hwang I. 2012. Mitochondrial targeting of the Arabidopsis F1-ATPase γ-subunit via multiple compensatory and synergistic presequence motifs. Plant Cell 24, 5037-5057
175. Li L, Nelson CJ, Carrie C, Gawryluk RM, Solheim C, Gray MW, Whelan J, Millar AH. 2013. Subcomplexes of ancestral respiratory complex I subunits rapidly turn over in vivo as productive assembly intermediates in Arabidopsis. Journal of Biological Chemistry 288, 5707-5717
176. Ling Q, Jarvis P. 2013. Dynamic regulation of endosymbiotic organelles by ubiquitination. Trends in Cell Biology 23, 399-408
177. Ling Q, Huang W, Baldwin A, Jarvis P. 2012. Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338, 655-659
178. Lisowsky T. 1992. Dual function of a new nuclear gene for oxidative phosphorylation and vegetative growth in yeast. Molecular and General Genetics 232, 58-64
179. Lister R, Carrie C, Duncan O, Ho LH, Howell KA, Murcha MW, Whelan J. 2007. Functional Definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19, 3739-3759
180. Lister R, Chew O, Lee MN, Heazlewood JL, Clifton R, Parker KL, Millar AH, Whelan J. 2004. A transcriptomic and proteomic characterization of the Arabidopsis mitochondrial protein import apparatus and its response to mitochondrial dysfunction. Plant Physiology 134, 777-789
181. Lister R, Chew O, Rudhe C, Lee MN, Whelan J. 2001. Arabidopsis thaliana ferrochelatase-I and-II are not imported into Arabidopsis mitochondria. FEBS Letters 506, 291-295
182. Lister R, Mowday B, Whelan J, Millar AH 2002. Zinc-DepenDent intermembrane space proteins stimulate import of carrier proteins into plant mitochondria. The Plant Journal 30, 555-566
183. Lister R, Murcha MW, Whelan J. 2003. The Mitochondrial Protein Import Machinery of Plants (MPIMP) database. Nucleic Acids Research 31, 325-327
184. Lithgow T, Junne T, Suda K, Gratzer S, Schatz G. 1994. The mitochondrial outer membrane protein Mas22p is essential for protein import and viability of yeast. Proceedings of the National AcaDemy of Sciences, USA 91, 11973-7
185. Longen S, Woellhaf MW, Petrungaro C, Riemer J, Herrmann JM. 2014. The disulfiDe relay of the intermembrane space oxidizes the ribosomal subunit mrp10 on its transit into the mitochondrial matrix. Development Cell 28, 30-42
186. Luciano P, Geoffroy S, Brandt A, HernanDez JF, Geli V. 1997. Functional cooperation of the mitochondrial processing peptidase subunits. Journal of Molecular Biology 272, 213-225
187. Maarse AC, Blom J, Keil P, Pfanner N, Meijer M. 1994. IDentification of the essential yeast protein MIM17, an integral mitochondrial inner membrane protein involved in protein import. FEBS Letters 349, 215-221
188. Macasev D, Newbigin E, Whelan J, Lithgow T. 2000. How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiology 123, 811-816
189. Macasev D, Whelan J, Newbigin E, Silva-Filho MC, Mulhern TD, Lithgow T. 2004. Tom22, an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes. Molecular Biology and Evolution 21, 1557-1564
190. Mackenzie SA. 2005. Plant organellar protein targeting: a traffic plan still unDer construction. Trends in Cell Biology 15, 548-554
191. Malhotra K, Sathappa M, Landin JS, Johnson AE, AlDer NN. 2013. Structural changes in the mitochondrial Tim23 channel are coupled to the proton-motive force. Nature Structural and Molecular Biology 20, 965-972
192. Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinski M, Jacq C. 2002. Genome-wiDe analysis of mRNAs targeted to yeast mitochondria. EMBO Reports 3, 159-164
193. Martin T, Sharma R, Sippel C, Waegemann K, Soll J, Vothknecht UC 2006. A protein kinase family in Arabidopsis phosphorylates chloroplast precursor proteins. Journal of Biological Chemistry 281, 40216-40223
194. Martin-Trillo M, Cubas P. 2010. TCP genes: a family snapshot ten years later. Trends in Plant Science 15, 31-39
195. May T, Soll J. 2000. 14-13-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12, 53-64
196. McQuibban GA, Saurya S, Freeman M. 2003. Mitochondrial membrane remoDelling regulated by a conserved rhomboid protease. Nature 423, 537-541
197. Meisinger C, Pfannschmidt S, Rissler M, et al. 2007. The morphology proteins Mdm12/Mmm1 function in the major -barrel assembly pathway of mitochondria. EMBO Journal 26, 2229-2239
198. Meisinger C, Rissler M, Chacinska A, et al. 2004. The mitochondrial morphology protein Mdm10 functions in assembly of the preprotein translocase of the outer membrane. Developmental Cell 7, 61-71
199. Meisinger C, Sickmann A, Pfanner N. 2008. The mitochondrial proteome: from inventory to function. Cell 134, 22-24
200. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM. 2005. A disulfiDe relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121, 1059-1069
201. Meyer EH. 2012. Proteomic investigations of complex I composition: how to Define a subunit? Frontiers in Plant Science 3, 106.
202. Meyer EH, Solheim C, Tanz SK, Bonnard G, Millar AH. 2011. Insights into the composition and assembly of the membrane arm of plant complex I through analysis of subcomplexes in Arabidopsis mutant lines. Journal of Biological Chemistry 286, 26081-26092
203. Meyer EH, Taylor NL, Millar AH. 2008. Resolving and iDentifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis. Journal of Proteome Research 7, 786-794
204. Michaud M, Marechal-Drouard L, Duchene AM. 2010. RNA trafficking in plant cells: targeting of cytosolic mRNAs to the mitochondrial surface. Plant Molecular Biology 73, 697-704
205. Mick DU, Dennerlein S, Wiese H, et al. 2012. MITRAC links mitochondrial protein translocation to respiratory-chain assembly and translational regulation. Cell 151, 1528-1541
206. Milenkovic D, Ramming T, Muller JM, Wenz L-S. Gebert N, Schulze-Specking A, Stojanovski D, Rospert S, Chacinska A. 2009. IDentification of the signal directing Tim9 and Tim10 into the intermembrane space of mitochondria. Molecular Biology of the Cell 20, 2530-2539
207. Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM. 2005. The plant mitochondrial proteome. Trends in Plant Science 10, 36-43
208. Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH. 2003. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiology 133, 443-447
209. Mitschke J, Fuss J, Blum T, Hoglund A, Reski R, Kohlbacher O, Rensing SA. 2009. Prediction of dual protein targeting to plant organelles. New Phytologist 183, 224-235
210. Moberg P, Nilsson S, Stahl A, Eriksson AC, Glaser E, Maler L. 2004. NMR solution structure of the mitochondrial F1? presequence from Nicotiana plumbaginifolia. Journal of Molecular Biology 336, 1129-1140
211. Moberg P, Stahl A, Bhushan S, Wright SJ, Eriksson A, Bruce BD, Glaser E. 2003. Characterization of a novel zinc metalloprotease involved in Degrading targeting peptiDes in mitochondria and chloroplasts. The Plant Journal 36, 616-628
212. Moczko M, Dietmeier K, Sollner T, Segui B, Steger HF, Neupert W, Pfanner N. 1992. IDentification of the mitochondrial receptor complex in Saccharomyces cerevisiae. FEBS Letters 310, 265-268
213. Mokranjac D, Neupert W. 2010. The many faces of the mitochondrial TIM23 complex. Biochimica et Biophysica Acta 1797, 1045-1054
214. Mokranjac D, Popov-Celeketic D, Hell K, Neupert W. 2005. Role of Tim21 in mitochondrial translocation contact sites. Journal of Biological Chemistry 280, 23437-40
215. Mossmann D, Meisinger C, Vogtle FN. 2012. Processing of mitochondrial presequences. Biochimica et Biophysica Acta 1819, 1098-1106
216. Mueller SJ, Lang D, Hoernstein SN, et al. 2014. Quantitative analysis of the mitochondrial and plastid proteomes of the moss Physcomitrella patens reveals protein macrocompartmentation and microcompartmentation. Plant Physiology 164, 2081-2095
217. Mukhopadhyay A, Hammen P, Waltner-Law M, Weiner H. 2002. Timing and structural consiDeration for the processing of mitochondrial matrix space proteins by the mitochondrial processing peptidase (MPP). Protein Science 11, 1026-1035
218. Muller M, Mentel M, Van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, Van Der Giezen M, Tielens AG, Martin WF. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiology Molecular Biology Reviews 76, 444-495
219. Murakami K, Mori M. 1990. Purified presequence binding factor (PBF) forms an import-competent complex with a purified mitochondrial precursor protein. EMBO Journal 9, 3201-3208
220. Murcha MW, Elhafez D, Lister R, Tonti-Filippini J, Baumgartner M, Philippar K, Carrie C, Mokranjac D, Soll J, Whelan J. 2007. Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiology 143, 199-212
221. Murcha MW, Elhafez D, Millar AH, Whelan J (2004b). The N-terminal extension of plant mitochondrial carrier proteins is removed by twostep processing: the first cleavage is by the mitochondrial processing peptidase. Journal of Molecular Biology 344, 443-454
222. Murcha MW, Elhafez D, Millar AH, Whelan J (2005a). The C-terminal region of TIM17 links the outer and inner mitochondrial membranes in Arabidopsis and is essential for protein import. Journal of Biological Chemistry 280, 16476-83
223. Murcha MW, Huang T, Whelan J. 1999. Import of precursor proteins into mitochondria from soybean tissues during Development. FEBS Letters 464, 53-59
224. Murcha MW, Kubiszewski-Jakubiak S, Wang Y, Whelan J. 2014a. EviDence for interactions between the mitochondrial import apparatus and respiratory chain complexes via Tim21-like proteins in Arabidopsis. Frontiers in Plant Science 5, 82.
225. Murcha MW, Lister R, Ho AY, Whelan J. 2003. IDentification, expression, and import of components 17 and 23 of the inner mitochondrial membrane translocase from Arabidopsis. Plant Physiology 131, 1737-1747
226. Murcha MW, Millar AH, Whelan J. 2005b. The N-terminal cleavable extension of plant carrier proteins is responsible for efficient insertion into the inner mitochondrial membrane. Journal of Molecular Biology 351, 16-25
227. Murcha MW, Wang Y, Whelan J. 2012. A molecular link between mitochondrial preprotein transporters and respiratory chain complexes. Plant Signaling &Behavior 7, 1594-1597
228. Murcha MW, Wang Y, Narsai R, Whelan. 2014b. The plant mitochondrial protein import apparatus-The differences make it interesting. Biochimica et Biophysica Acta 1840, 1233-1245
229. Muto T. Obita T. Abe Y. Shodai T. Endo T. Kohda D. NMR iDentification of the Tom20 binding segment in mitochondrial presequences. Journal of Molecular Biology 306, 137-143
230. Nagashima Y, Mishiba K, Suzuki E, Shimata Y, Iwata Y, Koizumi N. 2011. Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Scientific Reports 1, doi: 10.1038/srep00029.
231. Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K. 2010. Large-scale comparative phosphoproteomics iDentifies conserved phosphorylation sites in plants. Plant Physiology 153, 1161-1174
232. Neupert W. 1997. Protein import into mitochondria. Annual Review of Biochemistry 66, 863-917
233. Neupert W, Herrmann JM. 2007. Translocation of proteins into mitochondria. Annual Review of Biochemistry 76, 723-749
234. Ng S, De Clercq I, Van Aken O, Law SR, IVanova A, Willems P, Giraud E, Van Breusegem F, Whelan J. 2014. AnterograDe and retrograDe regulation of nuclear genes encoding mitochondrial proteins during growth, Development, and stress. Molecular Plant 7, 1075-1093
235. Ng S, IVanova A, Duncan O, et al. 2013. A membrane-bound NAC transcription factor ANAC017, mediates mitochondrial retrograDe signaling in Arabidopsis. Plant Cell 29, 3450-3471
236. Ni RJ, Shen Z, Yang CP, Wu YD, Bi YD, Wang BC. 2010. IDentification of low abundance polyA-binding proteins in Arabidopsis chloroplast using polyA-Affinity column. Molecular Biology Reporter 37, 637-641
237. Nicolay K, Laterveer FD, Van HeerDe WL 1994. Effects of amphipathic peptiDes, including presequences, on the functional integrity of rat liver mitochondrial membranes. Journal of Bioenergetics and Biomembranes 26, 327-334
238. Nilsson CeDerholm S, Backman HG, Pesaresi P, Leister D, Glaser E. 2009. Deletion of an organellar peptidasome PreP affects early Development in Arabidopsis thaliana. Plant Molecular Biology 71, 497-508
239. Nunnari J, Fox TD, Walter P. 1993. A mitochondrial protease with two catalytic subunits of nonoverlapping specificities. Science 262, 1997-2004
240. Obita T, Muto T, Endo T, Kohda D. 2003. PeptiDe library approach with a disulfiDe tether to refine the Tom20 recognition motif in mitochondrial presequences. Journal of Molecular Biology 328, 495-504
241. Ono H, Tuboi S. 1990. Purification and iDentification of a cytosolic factor required for import of precursors of mitochondrial proteins into mitochondria. Archives of Biochemistry and Biophysics 280, 299-304
242. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR. 2011. Evolution, structure and function of mitochondrial carriers: a review with new insights. The Plant Journal 66, 161-181
243. Pan R, Kaur N, Hu J. 2014. The Arabidopsis mitochondrial membranebound ubiquitin protease UBP27 contributes to mitochondrial morphogenesis. The Plant Journal 78, 1047-1059
244. Panigrahi R, Adina-Zada A, Whelan J, Vrielink A. 2013. Ligand recognition by the TPR domain of the import factor Toc64 from Arabidopsis thaliana. PLoS One 8, e83461.
245. Panigrahi R, Whelan J, Vrielink A. 2014. Exploring ligand recognition, selectivity and dynamics of TPR domains of chloroplast Toc64 and mitochondria Om64 from Arabidopsis thaliana. Journal of Molecular Recognition 27, 402-414
246. Papic D, Elbaz-Alon Y, Koerdt SN, Leopold K, Worm D, Jung M, Schuldiner M, Rapaport D. 2013. The role of Djp1 in import of the mitochondrial protein Mim1 Demonstrates specificity between a cochaperone and its substrate protein. Molecular Cell Biology 33, 4083-4094
247. Peeters N, Small I. 2001. Dual targeting to mitochondria and chloroplasts. Biochimica et Biophysica Acta 1541, 54-63
248. Perry AJ, Hulett JM, Likic VA, Lithgow T, Gooley PR. 2006. Convergent evolution of receptors for protein import into mitochondria. Current Biology 16, 221-229
249. Pesaresi P, Masiero S, Eubel H, Braun HP, Bhushan S, Glaser E, Salamini F, Leister D. 2006. Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18, 970-991
250. Peters K, Belt K, Braun HP. 2013. 3D gel map of Arabidopsis complex I. Frontiers in Plant Science 4, 153.
251. Peters K, Niessen M, Peterhansel C, Spath B, Holzle A, BinDer S, MarchfelDer A, Braun HP. 2012. Complex I-complex II ratio strongly differs in various organs of Arabidopsis thaliana. Plant Molecular Biology 79, 273-284
252. Pett W, Lavrov DV 2013. The twin-Arginine subunit C in oscarella: origin, evolution, and potential functional significance. Integrative and Comparative Biology 53, 495-502
253. Piechota J, Kolodziejczak M, Juszczak I, Sakamoto W, Janska H. 2010. IDentification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. Journal of Biological Chemistry 285, 12512-12521
254. Preuss M, Ott M, Funes S, Luirink J, Herrmann JM. 2005. Evolution of mitochondrial oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. Journal of Biological Chemistry 280, 13004-13011
255. Pruneda-Paz JL, Breton G, Para A, Kay SA. 2009. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323, 1481-1485
256. PuDelski B, Schock A, Hoth S, Radchuk R, Weber H, Hofmann J, Sonnewald U, Soll J, Philippar K. 2012. The plastid outer envelope protein OEP16 affects metabolic fluxes during ABA-controlled seed Development and germination. Journal of Experimental Botany 63, 1919-1936
257. Pujol C, Marechal-Drouard L, Duchene AM. 2007. How can organellar protein N-terminal sequences be dual targeting signals? In silico analysis and mutagenesis approach. Journal of Molecular Biology 369, 356-367
258. Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E. 2006. The molecular chaperone Hsp90 Delivers precursor proteins to the chloroplast import receptor Toc64. EMBO Journal 25, 1836-1847
259. Qiu J, Wenz LS, Zerbes RM, et al. 2013. Coupling of mitochondrial import and export translocases by receptor-mediated supercomplex formation. Cell 154, 596-608
260. Rassow J, Dekker PJ, Van Wilpe S, Meijer M, Soll J. 1999. The preprotein translocase of the mitochondrial inner membrane: function and evolution. Journal of Molecular Biology 286, 105-120
261. Rensink WA, Schnell DJ, Weisbeek PJ. 2000. The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. Journal of Biological Chemistry 275, 10265-10271
262. Richter U, Lahtinen T, Marttinen P, Myohanen M, Greco D, Cannino G, Jacobs HT, Lietzen N, Nyman TA, Battersby BJ. 2013. A mitochondrial ribosomal and RNA Decay pathway blocks cell proliferation. Current Biology 23, 535-541
263. Rimmer KA, Foo JH, Ng A, Petrie EJ, Shilling PJ, Perry AJ, Mertens HD, Lithgow T, Mulhern TD, Gooley PR. 2011. Recognition of mitochondrial targeting sequences by the import receptors Tom20 and Tom22. Journal of Molecular Biology 405, 804-818
264. Rissler M, WieDemann N, Pfannschmidt S, Gabriel K, Guiard B, Pfanner N, Chacinska A. 2005. The essential mitochondrial protein Erv1 cooperates with Mia40 in biogenesis of intermembrane space proteins. Journal of Molecular Biology 353, 485-492
265. RoDe C, Senkler M, Klodmann J, Winkelmann T, Braun HP. 2011. GelMap-A novel software tool for building and presenting proteome reference maps. Journal of Proteomics 74, 2214-2219
266. Roesch K, Hynds PJ, Varga R, Tranebjaerg L, Koehler CM. 2004. The calcium-binding aspartate/glutamate carriers, citrin and aralar1, are new substrates for the DDP1/TIMM8a-TIMM13 complex. Human Molecular Genetics 13, 2101-2111
267. Roise D, Horvath SJ, Tomich JM, Richards JH, Schatz G. 1986. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO Journal 5, 1327-1334
268. Rosenbaum Hofmann N, Theg SM. 2005. Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens. The Plant Journal 43, 675-687
269. Rossig C, Reinbothe C, Gray J, ValDes O, von Wettstein D, Reinbothe S. 2013. Three proteins mediate import of transit sequenceless precursors into the inner envelope of chloroplasts in Arabidopsis thaliana. Proceedings of the National AcaDemy of Sciences, USA 110, 19962-19967
270. Rudhe C, Chew O, Whelan J, Glaser E. 2002. A novel in vitro system forsimultaneous import of precursor proteins into mitochondria and chloroplasts. The Plant Journal 30, 213-220
271. Rudhe C, Clifton R, Chew O, Zemam K, Richter S, Lamppa G, Whelan J, Glaser E. 2004. Processing of the dual-targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. Journal of Molecular Biology 343, 639-647
272. Saitoh T, Igura M, Obita T, Ose T, Kojima R, Maenaka K, Endo T, Kohda D. 2007. Tom20 recognizes mitochondrial presequences through dynamic equilibrium among multiple bound states. EMBO Journal 26, 4777-4787
273. Schertl P, SunDerhaus S, Klodmann J, Grozeff GE, Bartoli CG, Braun HP. 2012. l-Galactono-1,4-lactone Dehydrogenase (GLDH) forms part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana. Journal of Biological Chemistry 287, 14412-9
274. Schleiff E, Becker T. 2011. Common ground for protein translocation: access control for mitochondria and chloroplasts. Nature Reviews Molecular Cell Biology 12, 48-59
275. Schleiff E, Soll J. 2000. Travelling of proteins through membranes: translocation into chloroplasts. Planta 211, 449-456
276. Schmidt B, Wachter E, Sebald W, Neupert W. 1984. Processing peptidase of Neurospora mitochondria. Two-step cleavage of imported ATPase subunit 9. European Journal of Biochemistry 144, 581-588
277. Schmidt O, Harbauer AB, Rao S, et al. 2011. Regulation of mitochondrial protein import by cytosolic kinases. Cell 144, 227-239
278. Schmitt S, Ahting U, Eichacker L, Granvogl B, Go NE, Nargang FE, Neupert W, Nussberger S. 2005. Role of Tom5 in maintaining the structural stability of the TOM complex of mitochondria. Journal of Biological Chemistry 280, 14499-506
279. SchneiDer G, Sjoling S, Wallin E, WreDe P, Glaser E, von Heijne G. 1998. Feature-extraction from endopeptidase cleavage sites in mitochondrial targeting peptiDes. Proteins 30, 49-60
280. Schulte U, Arretz M, SchneiDer H, Tropschug M, Wachter E, Neupert W, Weiss H. 1989. A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature 339, 147-149
281. SchwarzlanDer M, Logan DC, Johnston IG, Jones NS, Meyer AJ, Fricker MD, Sweetlove LJ. 2012. Pulsing of membrane potential in individual mitochondria: a stress-induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 24, 1188-1201
282. Schweiger R, Soll J, Jung K, Heermann R, Schwenkart S. 2013. Qunatification of interaction strengths between chaperone and tetratricopeptiDe repeat domain containing membrane proteins. Journal of Biological Chemistry 288, 30614-30625
283. Schwenkert S, Soll J, Bolter B. 2011. Protein import into chloroplasts-how chaperones feature into the game. Biochimica et Biophysica Acta 1808, 901-911
284. Senapin S, Chen XJ, Clark-Walker GD. 2003. Transcription of TIM9, a new factor required for the petite-positive phenotype of Saccharomyces cerevisiae, is Defective in spt7 mutants. Current Genetics 44, 202-210
285. SiDeris DP, Petrakis N, Katrakili N, Mikropoulou D, Gallo A, Ciofi-Baffoni S, Banci L, Bertini I, Tokatlidis K. 2009. A novel intermembrane space-targeting signal docks cysteines onto Mia40 during mitochondrial oxidative folding. Journal of Cell Biology 187, 1007-1022
286. Sieber F, Duchene AM, Marechal-Drouard L. 2011. Mitochondrial RNA import: from diversity of natural mechanisms to potential applications. International Reviews of Cell and Molecular Biology 287, 145-190
287. Silva-Filho MC. 2003. One ticket for multiple Destinations: dual targeting of proteins to distinct subcellular locations. Current Opinions in Plant Biology 6, 589-595
288. Silva-Filho MD, Wieers MC, Flugge UI, Chaumont F, Boutry M. 1997. Different in vitro and in vivo targeting properties of the transit peptiDe of a chloroplast envelope inner membrane protein. Journal of Biological Chemistry 272, 15264-15269
289. Sirrenberg C, Bauer MF, Guiard B, Neupert W, Brunner M. 1996. Import of carrier proteins into the mitochondrial inner membrane mediated by Tim22. Nature 384, 582-585
290. Sirrenberg C, Endres M, Folsch H, Stuart RA, Neupert W, Brunner M. 1998. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391, 912-915
291. Sjoling S, Eriksson AC, Glaser E. 1994. A helical element in the C-terminal domain of the N plumbaginifolia F1? presequence is important for recognition by the mitochondrial processing peptidase. Journal of Biological Chemistry 269, 32059-62
292. Sogo LF, Yaffe MP 1994. Regulation of mitochondrial morphology and inheritance by Mdm10p, a protein of the mitochondrial outer membrane. Journal of Cell Biology 126, 1361-1373
293. Sohrt K, Soll J. 2000. Toc64, a new component of the protein translocon of chloroplasts. Journal of Cell Biology 148, 1213-1221
294. Sommer M, Rudolf M, Tillmann B, Tripp J, Sommer MS, Schleiff E. 2013. Toc33 and Toc64-III cooperate in precursor protein import into the chloroplasts of Arabidopsis thaliana. Plant Cell &Environment 36, 970-983
295. Song J, Tamura Y, Yoshihisa T, Endo T. 2014. A novel import route for an N-Anchor mitochondrial outer membrane protein aiDed by the TIM23 complex. EMBO Reports 5, 670-677
296. Stahl A, Moberg P, Ytterberg J, Panfilov O, Brockenhuus Von Lowenhielm H, Nilsson F, Glaser E. 2002. Isolation and iDentification of a novel mitochondrial metalloprotease (PreP) that DegraDes targeting presequences in plants. Journal of Biological Chemistry 277, 41931-9
297. 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. Journal of Molecular Biology 349, 847-860
298. Stuart RA, Neupert W. 1990. Apocytochrome c: an exceptional mitochondrial precursor protein using an exceptional import pathway. Biochimie 72, 115-121
299. Stuart RA, Nicholson DW, Neupert W. 1990. Early steps in mitochondrial protein import: receptor functions can be substituted by the membrane insertion activity of apocytochrome c. Cell 60, 31-43
300. Sweetlove LJ, Fernie AR. 2013. The spatial organization of metabolism within the plant cell. Annual Review of Plant Biology 64, 723-746
301. Sweetlove LJ, Obata T, Fernie AR. 2014. Systems analysis of metabolic phenotypes: what have we learnt? Trends in Plant Science 19, 222-230
302. Szigyarto C, Dessi P, Smith MK, Knorpp C, Harmey MA, Day DA, Glaser E, Whelan J. 1998. A matrix-located processing peptidase of plant mitochondria. Plant Molecular Biology 36, 171-181
303. Tanudji M, Sjoling S, Glaser E, Whelan J. 1999. Signals required for the import and processing of the alternative oxidase into mitochondria. Journal of Biological Chemistry 274, 1286-1293
304. Tanz SK, CastleDen I, Hooper CM, Vacher M, Small I, Millar HA. 2013. SUBA3: a database for integrating experimentation and prediction to Define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Research 41 D1185-D1191
305. Taylor AB, Smith BS, Kitada S, Kojima K, Miyaura H, Otwinowski Z, Ito A, Deisenhofer J. 2001. Crystal structures of mitochondrial processing peptidase reveal the moDe for specific cleavage of import signal sequences. Structure 9, 615-625
306. Teixeira PF, Glaser E. 2013. Processing peptidases in mitochondria and chloroplasts. Biochimica et Biophysica Acta 1833, 360-370
307. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, Hell K. 2005. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Letters 579, 179-184
308. Truscott KN, Kovermann P, Geissler A, Merlin A, Meijer M, Driessen AJ, Rassow J, Pfanner N, Wagner R. 2001. A presequence-And voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nature Structural Biology 8, 1074-1082
309. Truscott KN, Voos W, Frazier AE, et al. 2003. A J-protein is an essential subunit of the presequence translocase-Associated protein import motor of mitochondria. Journal of Cell Biology 163, 707-713
310. Van Der Laan M, Bohnert M, WieDemann N, Pfanner N. 2012. Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends in Cell Biology 22, 185-192
311. Van Der Laan M, Hutu DP, Rehling P. 2010. On the mechanism of preprotein import by the mitochondrial presequence translocase. Biochimica et Biophysica Acta 1803, 732-739
312. Van Der Laan M, WieDemann N, Mick DU, Guiard B, Rehling P, Pfanner N. 2006. A role for Tim21 in membrane-potential-DepenDent preprotein sorting in mitochondria. Current Biology 16, 2271-2276
313. Van Wilpe S, Ryan MT, Hill K, et al. 1999. Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature 401, 485-489
314. Vasiljev A, Ahting U, Nargang FE, et al. 2004. Reconstituted TOM core complex and Tim9/Tim10 complex of mitochondria are sufficient for translocation of the ADP/ATP carrier across membranes. Molecular Biology of the Cell 15, 1445-1458
315. Viola IL, Guttlein LN, Gonzalez DH. 2013. Redox modulation of plant Developmental regulators from the class I TCP transcription factor family. Plant Physiology 162, 1434-1447
316. Vitu E, Bentzur M, Lisowsky T, Kaiser CA, Fass D. 2006. Gain of function in an ERV/ALR sulfhydryl oxidase by molecular engineering of the shuttle disulfiDe. Journal of Molecular Biology 362, 89-101
317. Vogtle FN, Prinz C, Kellermann J, Lottspeich F, Pfanner N, Meisinger C. 2011. Mitochondrial protein turnover: role of the precursor intermediate peptidase Oct1 in protein stabilization. Molecular Biology of the Cell 22, 2135-2143
318. Vogtle FN, Wortelkamp S, Zahedi RP, et al. 2009. Global analysis of the mitochondrial N-proteome iDentifies a processing peptidase critical for protein stability. Cell 139, 428-439
319. von Der Malsburg K, Muller JM, Bohnert M, et al. 2011. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Development Cell 21, 694-707
320. von Heijne G. 1986. Mitochondrial targeting sequences may form amphiphilic helices. EMBO Journal 5, 1335-1342
321. Voos W, Rottgers K. 2002. Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochimica et Biophysica Acta 1592, 51-62
322. Waegemann K, Soll J. 1996. Phosphorylation of the transit sequence of chloroplast precursor proteins. Journal of Biological Chemistry 271, 6545-6554
323. Wagener N, Ackermann M, Funes S, Neupert W. 2011. A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Molecular Cell 44, 191-202
324. Wagner K, Mick DU, Rehling P. 2009. Protein transport machineries for precursor translocation across the inner mitochondrial membrane. Biochimica et Biophysica Acta. 1793, 52-59
325. Waizenegger T, Stan T, Neupert W, Rapaport D. 2003. Signal-Anchor domains of proteins of the outer membrane of mitochondria: structural and functional characteristics. Journal of Biological Chemistry 278, 42064-42071
326. Wang Y, Carrie C, Giraud E, Elhafez D, Narsai R, Duncan O, Whelan J, Murcha MW. 2012. Dual location of the mitochondrial preprotein transporters B14.7 and Tim23-2 in complex I and the TIM17:23 complex in Arabidopsis links mitochondrial activity and biogenesis. Plant Cell 24, 2675-2695
327. Webb CT, Gorman MA, Lazarou M, Ryan MT, Gulbis JM. 2006. Crystal structure of the mitochondrial chaperone TIM9.10 reveals a sixblaDed -propeller. Molecular Cell 21, 123-133
328. Wenz LS, Qiu J, Becker T, WieDemann N. 2014. Biogenesis and folding of -barrel membrane proteins. Cell Cycle 13, 169-170
329. Werhahn W, Jansch L, Braun HP. 2003. IDentification of novel subunits of the TOM complex from Arabidopsis thaliana. Plant Physiology and Biochemistry 41, 407-416
330. Werhahn W, Niemeyer A, Jansch L, Kruft V, Schmitz UK, Braun H. 2001. Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. IDentification of multiple forms of TOM20. Plant Physiology 125, 943-954
331. Whelan J Knorpp C, Glaser E. 1990. Sorting of precursor proteins between isolated spinach leaf mitochondria and chloroplasts. Plant Molecular Biology 14, 977-982
332. Whelan J, Dolan L, Harmey MA. 1988. Import of precursor proteins into Vicia faba mitochondria. FEBS Letters 236, 217-220
333. Whelan J, Knorpp C, Harmey MA, Glaser E. 1991. Specificity of leaf mitochondrial and chloroplast processing systems for nuclear-encoDed precursor proteins. Plant Molecular Biology 16, 283-292
334. WiDeman JG, Lackey SW, Srayko MA, Norton KA, Nargang FE. 2013. Analysis of mutations in Neurospora crassa ERMES components reveals specific functions related to -barrel protein assembly and maintenance of mitochondrial morphology. PLoS One 8, e71837.
335. WieDemann N, Frazier AE, Pfanner N. 2004. The protein import machinery of mitochondria. Journal of Biological Chemistry 279, 14473-14476
336. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J. 2013. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496, 181-186
337. Xu L, Carrie C, Law SR, Murcha MW, Whelan J. 2013. Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiology 161, 644-662
338. Xu YZ, Arrieta-Montiel MP, Virdi KS, et al. 2011. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 23, 3428-3441
339. Yamano K, Tanaka-Yamano S, Endo T. 2010. Mdm10 as a dynamic constituent of the TOB/SAM complex directs coordinated assembly of Tom40. EMBO Reports 11, 187-193
340. Yang MJ, Geli V, Oppliger W, Suda K, James P, Schatz G. 1991. The MAS-encoDed processing protease of yeast mitochondria. Interaction of the purified enzyme with signal peptiDes and a purified precursor protein. Journal of Biological Chemistry 266, 6416-6423
341. Yano M, Terada K, Mori M. 2003. AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins. Journal of Cell Biology 163, 45-56
342. Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T. 2001. Role of the ABC transporter Mdl1 in peptiDe export from mitochondria. Science 291, 2135-2138
343. Youngman MJ, Hobbs AE, Burgess SM, Srinivasan M, Jensen RE. 2004. Mmm2p, a mitochondrial outer membrane protein required for yeast mitochondrial shape and maintenance of mtDNA nucleoids. Journal of Cell Biology 164, 677-688
344. Zerbes RM, Bohnert M, Stroud DA, et al. 2012. Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially Depend on mitofilin domains. Journal of Molecular Biology 422, 183-191
345. Zhang B, Carrie C, IVanova A, et al. 2012. LETM proteins play a role in the accumulation of mitochondrially encoDed proteins in Arabidopsis thaliana and AtLETM2 displays parent of origin effects. Journal of Biological Chemistry 287, 41757-41773
346. Zhang B, Van Aken O, Thatcher L, et al. 2014. The mitochondrial outer membrane AAA ATPase AtOM66 affects cell Death and pathogen resistance in Arabidopsis thaliana. The Plant Journal 80, 709-727
347. Zhang XP, Glaser E. 2002. Interaction of plant mitochondrial and chloroplast signal peptiDes with the Hsp70 molecular chaperone. Trends in Plant Science 7, 14-21
348. Zybailov B, Rutschow H, Friso G, RuDella A, Emanuelsson O, Sun Q, Van Wijk KJ. 2008. Sorting signals N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994