The plant mitochondrial proteome and the challenge of defining the posttranslational modifications responsible for signalling and stress effects on respiratory functions

Physiologia Plantarum

Volumn 129, Issue 1, 2007, Pages 207-224

  Ito, Jun ^a   Heazlewood, Joshua L ^a   Millar, A Harvey ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CARBON DIOXIDE; CELLS; OXIDATION; RESPIRATORY MECHANICS; STRESS ANALYSIS;

PLANT MITOCHONDRIAL; RESPIRATORY ELECTRON TRANSPORT; RESPIRATORY FUNCTIONS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 33845679901     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2006.00795.x     Document Type: Conference Paper

References (99)

1. Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schurmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101: 2642-2647
2. Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylidès C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13: 519-527
3. Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10: 1723-1732
4. Bykova NV, Egsgaard H, Møller IM (2003a) Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 540: 141-146
5. Bykova NV, Stensballe A, Egsgaard H, Jensen ON, Møller IM (2003b) Phosphorylation of formate dehydrogenase in potato tuber mitochondria. J Biol Chem 278: 26021-26030
6. Chen J, Henderson GI, Freeman GL (2001) Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/reperfused rat heart. J Mol Cell Cardiol 33: 1919-1927
7. 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. J Biol Chem 278: 46869-46877
8. Choksi KB, Boylston WH, Rabek JP, Widger WR, Papaconstantinou J (2004) Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 1688: 95-101
9. Corso M, Thomson M (2001) Protein phosphorylation in mitochondria from human placenta. Placenta 22: 432-439
10. da-Silva WS, Gomez-Puyou A, de Gomez-Puyou MT, Moreno-Sanchez R, De Felice FG, de Meis L, Oliveira MF, Galina A (2004) Mitochondrial bound hexokinase activity as a preventive antioxidant defense: steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J Biol Chem 279: 39846-39855
11. Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15: 1212-1226
12. Eubel H, Jansch L, 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
13. Eubel H, Heinemeyer J, Braun HP (2004) Identification and characterization of respirasomes in potato mitochondria. Plant Physiol 134: 1450-1459
14. Foster MW, Stamler JS (2004) New insights into protein S-nitrosylation. Mitochondria as a model system. J Biol Chem 279: 25891-25897
15. Gaberc-Porekar V, Menart V (2001) Perspectives of immobilized-metal affinity chromatography. J Biochem Biophys Methods 49: 335-360
16. Gelhaye E, Rouhier N, Gerard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot JP (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101: 14545-14550
17. Grad LI, Lemire BD (2004) Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. Hum Mol Genet 13: 303-314
18. Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17: 3436-3450
19. Hakansson G, Allen JF (1995) Histidine and tyrosine phosphorylation in pea mitochondria: evidence for protein phosphorylation in respiratory redox signalling. FEBS Lett 372: 238-242
20. Hansson M, Vener AV (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2: 550-559
21. Heazlewood JL, Howell KA, Millar AH (2003a) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim Biophys Acta 1604: 159-169
22. Heazlewood JL, Whelan J, Millar AH (2003b) The products of the mitochondrial orf25 and orfB genes are FO components in the plant F1FO ATP synthase. FEBS Lett 540: 201-205
23. Heazlewood JL, Howell KA, Whelan J, Millar AH (2003c) Towards an analysis of the rice mitochondrial proteome. Plant Physiol 132: 230-242
24. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, 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
25. Herald VL, Heazlewood JL, Day DA, Millar AH (2003) Proteomic identification of divalent metal cation binding proteins in plant mitochondria. FEBS Lett 537: 96-100
26. Holtzapffel RC, Castelli J, Finnegan PM, Millar AH, Whelan J, Day DA (2003) A tomato alternative oxidase protein with altered regulatory properties. Biochim Biophys Acta 1606: 153-162
27. Hopper RK, Carroll S, Aponte AM, Johnson DT, French S, Shen RF, Witzmann FA, Harris RA, Balaban RS (2006) Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 45: 2524-2536
28. Huang J, Struck F, Matzinger DF, Levings CSR (1994) Flower-enhanced expression of a nuclear-encoded mitochondrial respiratory protein is associated with changes in mitochondrion number. Plant Cell 6: 439-448
29. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197
30. Jansch L, Kruft V, Schmitz UK, Braun HP (1996) New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J 9: 357-368
31. Jensen ON (2004) Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol 8: 33-41
32. Kalume DE, Molina H, Pandey A (2003) Tackling the phosphoproteome: tools and strategies. Curr Opin Chem Biol 7: 64-69
33. Kim MV, Seit-Nebi AS, Marston SB, Gusev NB (2004) Some properties of human small heat shock protein Hsp22 (H11 or HspB8). Biochem Biophys Res Commun 315: 796-801
34. Koroleva OA, Tomlinson ML, Leader D, Shaw P, Doonan JH (2005) High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J 41: 162-174
35. Kristensen BK, Askerlund P, Bykova NV, Egsgaard H, Møller IM (2004) Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65: 1839-1851
36. Kruft V, Eubel H, Jansch L, Werhahn W, Braun HP (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol 127: 1694-1710
37. Kuzmin EV, Karpova OV, Elthon TE, Newton KJ (2004) Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins. J Biol Chem 279: 20672-20677
38. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jorgensen TJ (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4: 873-886
39. Laugesen S, Bergoin A, Rossignol M (2004) Deciphering the plant phosphoproteome: tools and strategies for a challenging task. Plant Physiol Biochem 42: 929-936
40. Lenne C, Douce R (1994) A low molecular mass heat-shock protein is localized to higher plant mitochondria. Plant Physiol 105: 1255-1261
41. Lund AA, Rhoads DM, Lund AL, Cerny RL, Elthon TE (2001) In vivo modifications of the maize mitochondrial small heat stress protein, HSP22. J Biol Chem 276: 29924-29929
42. Mann M, Ong SE, Gronborg M, Steen H, Jensen ON, Pandey A (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20: 261-268
43. Marcillat O, Zhang Y, Lin SW, Davies KJA (1988) Mitochondria contain a proteolytic system which can recognise and degrade oxidatively-denatured proteins. Biochem J 254: 677-683
44. Michaud S, Marin R, Tanguay RM (1997) Regulation of heat shock gene induction and expression during Drosophila development. Cell Mol Life Sci 53: 104-113
45. Millar AH, Leaver CH, Hill SA (1999) Characterization of the dihydrolipoamide acetyltransferase of the mitochondrial pyruvate dehydrogenase complex from potato and comparisons with similar enzymes in diverse plant species. Eur J Biochem 264: 973
46. Millar AH, Leaver CJ (2000) The cytotoxic lipid peroxidation product, 4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydrogenases in the matrix of plant mitochondria. FEBS Lett 481: 117-121
47. Millar AH, Heazlewood JL (2003) Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis. Plant Physiol 131: 443-453
48. Millar AH, Sweetlove LJ, Giege P, Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127: 1711-1727
49. Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Møller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10: 36-43
50. Mitsumoto A, Takeuchi A, Okawa K, Nakagawa Y (2002) A subset of newly synthesized polypeptides in mitochondria from human endothelial cells exposed to hydroperoxide stress. Free Radic Biol Med 32: 22-37
51. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591
52. Møller IM, Kristensen BK (2006) Protein oxidation in plant mitochondria detected as oxidized tryptophan. Free Radic Biol Med 40: 430-435
53. Morrow G, Samson M, Michaud S, Tanguay RM (2004a) Overexpression of the small mitochondrial Hsp22 extends Drosophila life span and increases resistance to oxidative stress. FASEB J 18: 598-599
54. Morrow G, Battistini S, Zhang P, Tanguay RM (2004b) Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J Biol Chem 279: 43382-43385
55. Noordermeer MA, Feussner I, Kolbe A, Veldink GA, Vliegenthart JF (2000) Oxygenation of (3Z)-alkenals to 4-hydroxy-(2E)-alkenals in plant extracts: a nonenzymatic process. Biochem Biophys Res Commun 277: 112-116
56. Nuhse TS, Stensballe A, Jensen ON, Peck SC (2003) Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Mol Cell Proteomics 2: 1234-1243
57. Nuhse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16: 2394-2405
58. O'Brien KM, Dirmeier R, Engle M, Poyton RO (2004) Mitochondrial protein oxidation in yeast mutants lacking Mn or CuZn superoxide dismutase: Evidence that MnSOD and CuZnSOD have both unique and overlapping functions in protecting mitochondrial proteins from oxidative damage. J Biol Chem 279: 51817-51827
59. Pagliarini DJ, Dixon JE (2006) Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem Sci 31: 26-34
60. Pedrajas JR, Miranda-Vizuete A, Javanmardy N, Gustafsson JA, Spyrou G (2000) Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J Biol Chem 275: 16296-16301
61. Pical C, Fredlund KM, Petit PX, Sommarin M, Moller IM (1993) The outer membrane of plant mitochondria contains a calcium-dependent protein kinase and multiple phosphoproteins. FEBS Lett 336: 347-351
62. Rabilloud T, Heller M, Rigobello MP, Bindoli A, Aebersold R, Lunardi J (2001) The mitochondrial antioxidant defence system and its response to oxidative stress. Proteomics 1: 1105-1110
63. Raggiaschi R, Gotta S, Terstappen GC (2005) Phosphoproteome analysis. Biosci Rep 25: 33-44
64. Randall DD, Rubin PM, Fenko M (1977) Plant pyruvate dehydrogenase complex purification, characterization and regulation by metabolites and phosphorylation. Biochim Biophys Acta 485: 336-349
65. Reinheckel T, Korn S, Mohring S, Augustin W, Halangk W, Schild L (2000) Adaptation of protein carbonyl detection to the requirements of proteome analysis demonstrated for hypoxia/reoxygenation in isolated rat liver mitochondria. Arch Biochem Biophys 376: 59-65
66. Richly E, Chinnery PF, Leister D (2003) Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends Genet 19: 356-362
67. Samokhvalov V, Ignatov V, Kondrashova M (2004) Inhibition of Krebs cycle and activation of glyoxylate cycle in the course of chronological aging of Saccharomyces cerevisiae. Compensatory role of succinate oxidation. Biochimie 86: 39-46
68. Sardanelli MA, Technikova-Dobrova Z, Scacco SC, Speranza F, Papa S (1995) Characterization of proteins phosphorylated by the cAMP-dependent protein kinase of bovine heart mitochondria. FEBS Lett 377: 470-474
69. Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223-231
70. Schneider C, Tallman KA, Porter NA, Brash AR (2001) Two distinct pathways of formation of 4-hydroxynonenal. Mechanisms of nonenzymatic transformation of the 9- and 13-hydroperoxides of linoleic acid to 4-hydroxyalkenals. J Biol Chem 276: 20831-20838
71. Schulenberg B, Aggeler R, Beechem JM, Capaldi RA, Patton WF (2003) Analysis of steady-state protein phosphorylation in mitochondria using a novel fluorescent phosphosensor dye. J Biol Chem 278: 27251-27255
72. Sommarin M, Petit PX, Moller IM (1990) Endogenous protein phosphorylation in purified plant mitochondria. Biochim Biophys Acta 1052: 195-203
73. Struglics A, Fredlund KM, Moller IM, Allen JF (1998) Two subunits of the F0F1-ATPase are phosphorylated in the inner mitochondrial membrane. Biochem Biophys Res Commun 243: 664-668
74. Struglics A, Fredlund KM, Moller IM, Allen JF (1999) Purification of a serine and histidine phosphorylated mitochondrial nucleoside diphosphate kinase from Pisum sativum. Eur J Biochem 262: 765-773
75. Struglics A, Fredlund KM, Konstantinov YM, Allen JF, Moller IM (2000) Protein phosphorylation/dephosphorylation in the inner membrane of potato tuber mitochondria. FEBS Lett 475: 213-217
76. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32: 891-904
77. Takahashi A, Kawasaki T, Wong HL, Suharsono U, Hirano H, Shimamoto K (2003) Hyperphosphorylation of a mitochondrial protein, prohibitin, is induced by calyculin A in a rice lesion-mimic mutant cdr1. Plant Physiol 132: 1861-1869
78. Talent JM, Kong Y, Gracy RW (1998) A double stain for total and oxidized proteins from two-dimensional fingerprints. Anal Biochem 263: 31-38
79. Taylor NL, Day DA, Millar AH (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J Biol Chem 277: 42663-42668
80. Taylor NL, Day DA, Millar AH (2004) Targets of stress-induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. J Exp Bot 55: 1-10
81. Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics 4: 1122-1133
82. Taylor SW, Fahy E, Murray J, Capaldi RA, Ghosh SS (2003) Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J Biol Chem 278: 19587-19590
83. Technikova-Dobrova Z, Sardanelli AM, Speranza F, Scacco S, Signorile A, Lorusso V, Papa S (2001) Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40: 13941-13947
84. Thelen JJ, Miernyk JA, Randall DD (2000) Pyruvate dehydrogenase kinase from Arabidopsis thaliana: a protein histidine kinase that phosphorylates serine residues. Biochem J 349: 195-201
85. Tian GW, Mohanty A, Chary SN, Li S, Paap B, Drakakaki G, Kopec CD, Li J, Ehrhardt D, Jackson D, Rhee SY, Raikhel NV, Citovsky V (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol 135: 25-38
86. Tovar-Mendez A, Miernyk JA, Randall DD (2003) Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 270: 1043-1049
87. Tretter L, Sipos I, Adam-Vizi V (2004) Initiation of neuronal damage by complex I deficiency and oxidative stress in Parkinson's disease. Neurochem Res 29: 569-577
88. Turko IV, Li L, Aulak KS, Stuehr DJ, Chang JY, Murad F (2003) Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J Biol Chem 278: 33972-33977
89. Vallejo CG, Seguido AM, Fernández-Renart M (1997) Protein kinases in mitochondria of the invertebrate Artemia franciscana. Arch Biochem Biophys 339: 9-16
90. Vanlerberghe GC, McIntosh L (1997) ALTERNATIVE OXIDASE: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48: 703-734
91. Vener AV, Harms A, Sussman MR, Vierstra RD (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276: 6959-6966
92. Venkatraman A, Landar A, Davis AJ, Chamlee L, Sanderson T, Kim H, Page G, Pompilius M, Ballinger S, Darley-Usmar V, Bailey SM (2004) Modification of the mitochondrial proteome in response to the stress of ethanol-dependent hepatotoxicity. J Biol Chem 279: 22092-22101
93. Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 276(Pt 3): 643-648
94. Vidal V, Ranty B, Dillenschneide M, Charpenteau M, Ranjeva R (1993) Molecular characterization of a 70 kDa heat-shock protein of bean mitochondria. Plant J 3: 143-150
95. Werhahn W, Jänsch L, Braun H-P (2003) Identification of novel subunits of the TOM complex from Arabidopsis thaliana. Plant Physiol Biochem 41: 407-416
96. Winger AM, Millar AH, Day DA (2005) Sensitivity of plant mitochondrial terminal oxidases to the lipid peroxidation product 4-hydroxy-2-nonenal (HNE). Biochem J 387: 865-870
97. Wolschin F, Weckwerth W (2005) Combining metal oxide affinity chromatography (MOAC) and selective mass spectrometry for robust identification of in vivo protein phosphorylation sites. Plant Methods 1: 9
98. Wolschin F, Wienkoop S, Weckwerth W (2005) Enrichment of phosphorylated proteins and peptides from complex mixtures using metal oxide/hydroxide affinity chromatography (MOAC). Proteomics 5: 4389-4397
99. Zhang Y, Marcillat O, Giulivi C, Ernster L, Davies KJ (1990) The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265: 16330-16336