Mitochondrial Composition, Function and Stress Response in Plants

Journal of Integrative Plant Biology

Volumn 54, Issue 11, 2012, Pages 887-906

  Jacoby, Richard P ^a,b   Li, Lei ^a,b   Huang, Shaobai ^a,b   Pong Lee, Chun ^c   Millar, A Harvey ^a,b   Taylor, Nicolas L ^a,b  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Carbon; Complex assembly; Electron transport chain; Oxidative stress; Plant mitochondria; Respiration; ROS signaling

Indexed keywords

BIOCHEMICAL COMPOSITION; CARBON; CATABOLISM; MITOCHONDRION; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; PLANT; POLLUTION EXPOSURE; RESPIRATION; TRANSITION ELEMENT; TRANSPORT PROCESS;

ANTIBODY SPECIFICITY; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PLANT; REVIEW; SIGNAL TRANSDUCTION;

MITOCHONDRIA; ORGAN SPECIFICITY; OXIDATIVE STRESS; PLANTS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84869221236     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01177.x     Document Type: Review

References (180)

1. Abe F, Saito K, Miura K, Toriyama K (2002) A single nucleotide polymorphism in the alternative oxidase gene among rice varieties differing in low temperature tolerance. FEBS Lett. 527, 181-185.
2. Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radic. Biol. Med. 23, 473-479.
3. Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann. Bot. 86, 1-20.
4. Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys. J. 47, 411-414.
5. Araujo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R, Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, Martinoia E, Jordana X, DaMatta FM, Fernie AR (2011) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23, 600-627.
6. Armstrong AF, Logan DC, Tobin AK, O'Toole P, Atkin OK (2006) Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. Plant Cell Environ. 29, 940-949.
7. Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: Unravelling the variable response of plant respiration to temperature. Funct. Plant Biol. 32, 87-105.
8. Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 103, 581-597.
9. Attallah CV, Welchen E, Pujol C, Bonnard G, Gonzalez DH (2007) Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol. Biol. 65, 343-355.
10. Barrientos A, Gouget K, Horn D, Soto IC, Fontanesi F (2009) Suppression mechanisms of COX assembly defects in yeast and human: Insights into the COX assembly process. Biochim. Biophys. Acta 1793, 97-107.
11. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol. 143, 312-325.
12. Bhuiyan NH, Hamada A, Yamada N, Rai V, Hibino T, Takabe T (2007) Regulation of betaine synthesis by precursor supply and choline monooxygenase expression in Amaranthus tricolor. J. Exp. Bot 58, 4203-4212.
13. Cardol P (2011) Mitochondrial NADH:ubiquinone oxidoreductase (complex I) in eukaryotes: A highly conserved subunit composition highlighted by mining of protein databases. Biochim. Biophys. Acta 1807, 1390-1397.
14. Carrie C, Murcha MW, Kuehn K, Duncan O, Barthet M, Smith PM, Eubel H, Meyer E, Day DA, Millar AH, Whelan J (2008) Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079.
15. Catoni E, Desimone M, Hilpert M, Wipf D, Kunze R, Schneider A, Flugge UI, Schumacher K, Frommer WB (2003a) Expression pattern of a nuclear encoded mitochondrial arginine- ornithine translocator gene from Arabidopsis. BMC Plant Biol. 3, 1.
16. Catoni E, Schwab R, Hilpert M, Desimone M, Schwacke R, Flugge UI, Schumacher K, Frommer WB (2003b) Identification of an Arabidopsis mitochondrial succinate-fumarate translocator. FEBS Lett. 534, 87-92.
17. Chen CB, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc. Natl. Acad. Sci. USA 102, 3459-3464.
18. Chen X, Wang Y, Li J, Jiang A, Cheng Y, Zhang W (2009) Mitochondrial proteome during salt stress-induced programmed cell death in rice. Plant Physiol. Biochem. 47, 407-415.
19. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529-533.
20. Considine MJ, Goodman M, Echtay KS, Laloi M, Whelan J, Brand MD, Sweetlove LJ (2003) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. J. Biol. Chem. 278, 22298-22302.
21. Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress response in rice seedlings. Proteomics 5, 3162-3172.
22. De Block M, Van Lijsebettens M (2011) Energy efficiency and energy homeostasis as genetic and epigenetic components of plant performance and crop productivity. Curr. Opin. Plant Biol. 14, 275-282.
23. de Longevialle AoF, Meyer EH, Andres C, Taylor NL, Lurin C, Millar AH, Small ID (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19, 3256-3265.
24. Deighton N, Muckenschnabel I, Goodman BA, Williamson B (1999) Lipid peroxidation and the oxidative burst associated with infection of Capsicum annuum by Botrytis cinerea. Plant J. 20, 485-492.
25. Diaz F, Kotarsky H, Fellman V, Moraes CT (2011) Mitochondrial disorders caused by mutations in respiratory chain assembly factors. Sem. Fetal Neonatal. Med. 16, 197-204.
26. Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6, 6498-6507.
27. Drew MC, Lauchli A (1985) Oxygen dependent exclusion of sodium ions from shoots by roots of Zea mays (cv Pioneer 3906) in relation to salinity damage. Plant Physiol. 79, 171-176.
28. Dungey NO, Davies DD (1982) Protein turnover in isolated barley leaf segments and the effects of stress. J. Exp. Bot. 33, 12-20.
29. 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.
30. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Rad. Biol. Med. 11, 81-128.
31. 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.
32. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280, 12168-12180.
33. Finnegan P, Soole KL, Umbach AL (2004) Alternative mitochondrial electron transport proteins in higher plants. In: Day DA, Millar AH, Whelan J, eds. Plant Mitochondria: From Genome to Function - Advances in Photosynthesis and Respiration Springer. pp. 163-230.
34. Flowers TJ (1972) Salt tolerance in Suaeda maritima- Effect of sodium chloride on growth, respiration, and soluble enzymes in a comparative study with Pisum sativum. J. Exp. Bot. 23, 310.
35. Foyer CH, Noctor G (2011) Ascorbate and glutathione: The heart of the redox hub. Plant Physiol. 155, 2-18.
36. Fuentes D, Meneses M, Nunes-Nesi A, Araujo W, Tapia R, Gomez I, Holuigue L, Gutierrez RA, Fernie AR, Jordana X (2011) A deficiency in the flavoprotein of Arabidopsis mitochondrial complex II results in elevated photosynthesis and better growth in nitrogen-limiting conditions. Plant Physiol 10.1104/pp.1111.183939.
37. Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF (2012) Acquisition of aluminium tolerance by modification of a single gene in barley. Nat. Commun. 3, 713.
38. Garmier M, Carroll AJ, Delannoy E, Vallet C, Day DA, Small ID, Millar AH (2008) Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 148, 1324-1341.
39. Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ. 29, 1956-1969.
40. Ghezzi D, Goffrini P, Uziel G, Horvath R, Klopstock T, Lochmuller H, D'Adamo P, Gasparini P, Strom TM, Prokisch H, Invernizzi F, Ferrero I, Zeviani M (2009) SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nature Genet. 41, 654-656.
41. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of alternative oxidase1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 147, 595-610.
42. Gleason C, Huang S, Thatcher LF, Foley RC, Anderson CR, Carroll AJ, Millar AH, Singh KB (2011) Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. USA 108, 10768-10773.
43. Gonzalez DH, Welchen E, Attallah CV, Comelli RN, Mufarrege EF (2007) Transcriptional coordination of the biogenesis of the oxidative phosphorylation machinery in plants. Plant J. 51, 105-116.
44. Guan Y, Rawsthorne S, Scofield G, Shaw P, Doonan J (1995) Cloning and characterization of a dihydrolipoamide acetyltransferase (E2) subunit of the pyruvate dehydrogenase complex from Arabidopsis thaliana. J. Biol. Chem. 270, 5412-5417.
45. Hamasur B, Glaser E (1992) Plant mitochondrial F0F1 ATP synthase. Identification of the individual subunits and properties of the purified spinach leaf mitochondrial ATP synthase. Eur. J. Biochem 205, 409-416.
46. Hamel P, Saint-Georges Y, de Pinto B, Lachacinski N, Altamura N, Dujardin G (2004) Redundancy in the function of mitochondrial phosphate transport in Saccharomyces cerevisiae and Arabidopsis thaliana. Mol. Microbiol. 51, 307-317.
47. Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol. 126, 1266-1274.
48. Hanning I, Heldt HW (1993) On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves (Partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products). Plant Physiol. 103, 1147-1154.
49. Hao HX, Khalimonchuk O, Schraders M, Dephoure N, Bayley JP, Kunst H, Devilee P, Cremers CW, Schiffman JD, Bentz BG, Gygi SP, Winge DR, Kremer H, Rutter J (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325, 1139-1142.
50. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21, 535-553.
51. Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B, De Block M (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc. Natl. Acad. Sci. USA 106, 20109-20114.
52. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D (2010) The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol. Cell 37, 529-540.
53. 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.
54. Heazlewood JL, Howell KA, Whelan J, Millar AH (2003b) Towards an analysis of the rice mitochondrial proteome. Plant Physiol. 132, 230-242.
55. O ATP synthase. FEBS Lett. 540, 201-205.
56. Hossain Z, Nouri MZ, Komatsu S (2012) Plant cell organelle proteomics in response to abiotic stress. J. Proteome Res. 11, 37-48.
57. Hoyos ME, Palmieri L, Wertin T, Arrigoni R, Polacco JC, Palmieri F (2003) Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast. Plant J. 33, 1027-1035.
58. Huang BR, Rachmilevitch S, Xu JC (2012) Root carbon and protein metabolism associated with heat tolerance. J. Exp. Bot. 63, 3455-3465.
59. Huang S, Millar AH, Taylor NL (2011) The plant mitochondrial proteome composition and stress response: Conservation and divergence between monocots and dicots. In: Kempken F, ed. Advances in Plant Biology Springer, New York pp. 533.
60. Huang S, Taylor NL, Ströher E, Fenske R, Millar AH (2012) Succinate dehydrogenase assembly factor 2 is needed for assembly and activity of mitochondrial complex II and for normal root elongation in Arabidopsis. Plant J. (in press).
61. Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J. Prot. Res. 9, 6595-6604.
62. Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci. 16, 614-623.
63. 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.
64. Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J. Exp. Bot. 58, 3591-3607.
65. Johnson DT, Harris RA, French S, Blair PV, You J, Bemis KG, Wang M, Balaban RS (2007) Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. 292, C689-C697.
66. Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14, 3271-3284.
67. 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.
68. Komatsu S, Yamamoto A, Nakamura T, Nouri MZ, Nanjo Y, Nishizawa K, Furukawa K (2011) Comprehensive analysis of mitochondria in roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. J. Prot. Res. 10, 3993-4004.
69. Koyama H, Kawamura A, Kihara T, Hara T, Takita E, Shibata D (2000) Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol. 41, 1030-1037.
70. Kuffner R, Rohr A, Schmiede A, Krull C, Schulte U (1998) Involvement of two novel chaperones in the assembly of mitochondrial NADH:Ubiquinone oxidoreductase (complex I). J. Mol. Biol. 283, 409-417.
71. Kurimoto K, Day DA, Lambers H, Noguchi K (2004) Effect of respiratory homeostasis on plant growth in cultivars of wheat and rice. Plant Cell Environ. 27, 853-862.
72. Kuzmin EV, Karpova OV, Elthon TE, Newton KJ (2004) Mitochondrial respiratory deficiencies signal pu-regulation of genes for heat shock proteins. J. Biol. Chem. 279, 20672-20677.
73. La Cognata U, Landschutze V, Willmitzer L, Muller-Rober B (1996) Structure and expression of mitochondrial citrate synthases from higher plants. Plant Cell Physiol. 37, 1022-1029.
74. Laloi M (1999) Plant mitochondrial carriers: An overview. Cell Mol. Life Sci. 56, 918-944.
75. Lazarou M, McKenzie M, Ohtake A, Thorburn DR, Ryan MT (2007) Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Mol. Cell Biol. 27, 4228-4237.
76. Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14, 1235-1251.
77. Lee CP, Eubel H, O'Toole N, Millar A (2011) Combining proteomics of root and shoot mitochondria and transcript analysis to define constitutive and variable components in plant mitochondria. Phytochemistry 72, 1092-1108.
78. Lee CP, Eubel H, O'Toole N, Millar AH (2008) Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol. Cell Proteomics 7, 1297-1316.
79. Lee CP, Eubel H, Solheim C, Millar AH (2012) Mitochondrial proteome heterogeneity between tissues from the vegetative and reproductive stages of Arabidopsis thaliana development. J. Prot. Res. 11, 3326-3343.
80. Leon G, Holuigue L, Jordana X (2007) Mitochondrial complex II Is essential for gametophyte development in Arabidopsis. Plant Physiol. 143, 1534-1546.
81. Li L, Carrie C, Nelson C, Whelan J, Millar AH (2012) Accumulation of newly synthesised F1 in vivo in Arabidopsis mitochondria provides evidence for modular assembly of the plant F1Fo ATP synthase. J. Biol. Chem. 287, 25749-25757.
82. Luethy MH, Miernyk JA, Randall DD (1995) The mitochondrial pyruvate dehydrogenase complex: Nucleotide and deduced amino-acid sequences of a cDNA encoding the Arabidopsis thaliana E1 alpha-subunit. Gene 164, 251-254.
83. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273-278.
84. + cycling at the root plasma membrane in rice (Oryza sativa L.): Kinetics, energetics, and relationship to salinity tolerance. J. Exp. Bot. 59, 4109-4117.
85. Mannella CA (1992) The 'ins' and 'outs' of mitochondrial membrane channels. Trends Biochem. Sci. 17, 315-320.
86. Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru II, Slepchenko B, Loew LM, Hsieh CE, Buttle K, Marko M (2001) Topology of the mitochondrial inner membrane: Dynamics and bioenergetic implications. IUBMB Life 52, 93-100.
87. Mannella CA, Tedeschi H (1987) Importance of the mitochondrial outer membrane channel as a model biological channel. J. Bioenerg. Biomembr. 19, 305-308.
88. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96, 8271-8276.
89. McCree KJ (1986) Whole-plant carbon balance during osmotic adjustment to drought and salinity stress. Aust. J. Plant Physiol. 13, 33-43.
90. McDonald AE (2008) Alternative oxidase: An inter-kingdom perspective on the function and regulation of this broadly distributed 'cyanide-resistant' terminal oxidase. Funct. Plant Biol. 35, 535-552.
91. 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. J. Biol. Chem. 286, 26081-26092.
92. Meyer EH, Taylor NL, Millar AH (2008) Resolving and identifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis. J. Prot. Res. 7, 786-794.
93. Meyer EH, Tomaz T, Carroll AJ, Estavillo G, Delannoy E, Tanz SK, Small ID, Pogson BJ, Millar AH (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 151, 603-619.
94. Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol. 133, 642-652.
95. Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398, 155-158.
96. Millar AH, Eubel H, Jansch L, Kruft V, Heazlewood JL, Braun HP (2004a) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 56, 77-90.
97. 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.
98. Millar AH, Trend AE, Heazlewood JL (2004b) Changes in the mitochondrial proteome during the anoxia to air transition in rice focus around cytochrome-containing respiratory complexes. J. Biol. Chem. 279, 39471-39478.
99. Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Ann. Rev. Plant Biol. 62, 79-104.
100. Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009) Unraveling delta(1)-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J. Biol. Chem. 284, 26482-26492.
101. Miller RJ, Bittell JE, Koeppe DE (1973) Effect of cadmium on electron transport and energy transfer reactions in corn mitochondria. Physiol. Plant. 28, 166-171.
102. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT (2012) Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 1817, 851-862.
103. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
104. Moller IM (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann. Rev. Plant Physiol. Plant Mol. Biol. 52, 561-591.
105. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Ann. Rev. Plant Biol. 58, 459-481.
106. Møller IM, Sweetlove LJ (2011) ROS signalling - specificity is required. Trends Plant Sci. 15, 370-374.
107. Montillet J-L, Agnel J-P, Ponchet M, Vailleau F, Roby D, Triantaphylides C (2002) Lipoxygenase-mediated production of fatty acid hydroperoxides is a specific signature of the hypersensitive reaction in plants. Plant Physiol. Biochem. 40, 633-639.
108. Moore CS, Cook-Johnson R, Rudhe C, Whelan J, Day DA, Wiskich JT, Soole KL (2003) Identification of AtNDI1, an internal non-phosphorylating NAD(P)H dehydrogenase in Arabidopsis thaliana mitochondria. Plant Physiol. 133, 1968-1978.
109. Morgan MJ, Lehmann M, Schwarzländer M, Baxter CJ, Sienkiewicz-Porzucek A, Williams TCR, Schauer N, Fernie AR, Fricker MD, Ratcliffe RG, Sweetlove LJ, Finkemeier I (2008) Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 147, 101-114.
110. Ndimba BK, Chivasa S, Simon WJ, Slabas AR (2005) Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 5, 4185-4196.
111. Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12, 125-134.
112. Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8, 87-99.
113. Noordermeer MA, Feussner I, Kolbe A, Veldink GA, Vliegenthart JFG (2000) Oxygenation of (3Z)-alkenals to 4-hydroxy-(2E)-alkenals in plant extracts: A nonenzymatic process. Biochem. Biophys. Res. Comm. 277, 112-116.
114. Nouws J, Nijtmans LG, Smeitink JA, Vogel RO (2012) Assembly factors as a new class of disease genes for mitochondrial complex I deficiency: Cause, pathology and treatment options. Brain 135, 12-22.
115. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 50, 1093-1106.
116. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol. 137, 611-622.
117. Osman C, Wilmes C, Tatsuta T, Langer T (2007) Prohibitins interact genetically with Atp23, a novel processing peptidase and chaperone for the F1Fo-ATP synthase. Mol. Biol. Cell 18, 627-635.
118. Palmieri F, Rieder B, Ventrella A, Blanco E, Do PT, Nunes-Nesi A, Trauth AU, Fiermonte G, Tjaden J, Agrimi G, Kirchberger S, Paradies E, Fernie AR, Neuhaus HE (2009) Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD+ carrier proteins. J. Biol. Chem. 284, 31249-31259.
119. Palmieri L, Santoro A, Carrari F, Blanco E, Nunes-Nesi A, Arrigoni R, Genchi F, Fernie AR, Palmieri F (2008) Identification and characterization of ADNT1, a novel mitochondrial adenine nucleotide transporter from Arabidopsis. Plant Physiol. 148, 1797-1808.
120. Peiffer WE, Ingle RT, Ferguson-Miller S (1990) Structurally unique plant cytochrome c oxidase isolated from wheat germ, a rich source of plant mitochondrial enzymes. Biochemistry 29, 8696-8701.
121. Picault N, Palmieri L, Pisano I, Hodges M, Palmieri F (2002) Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J. Biol. Chem. 277, 24204-24211.
122. Pickova A, Potocky M, Houstek J (2005) Assembly factors of F1FO-ATP synthase across genomes. Proteins 59, 393-402.
123. Pineau B, Layoune O, Danon A, De Paepe R (2008) L-galactono-1, 4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J. Biol. Chem. 283, 32500-32505.
124. Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol. 94, 621-627.
125. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, Brand MD (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J. Biol. Chem. 10.1074/jbc.M1112.374629.
126. Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8, 546-553.
127. Rak M, Gokova S, Tzagoloff A (2011) Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30, 920-930.
128. Rak M, Tzagoloff A (2009) F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc. Natl. Acad. Sci. USA 106, 18509-18514.
129. Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Ann. Rev. Plant Biol. 55, 23-39.
130. Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10, 20.
131. Rigas S, Daras G, Laxa M, Marathias N, Fasseas C, Sweetlove LJ, Hatzopoulos P (2009) Role of Lon1 protease in post-germinative growth and maintenance of mitochondrial function in Arabidopsis thaliana. New Phytol. 181, 588-600.
132. Robert N, d'Erfurth I, Marmagne A, Erhardt M, Allot M, Boivin K, Gissot L, Monachello D, Michaud M, Duchene AM, Barbier-Brygoo H, Marechal-Drouard L, Ephritikhine G, Filleur S (2012) Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Mol. Biol. 78, 431-446.
133. Robison MM, Ling X, Smid MP, Zarei A, Wolyn DJ (2009) Antisense expression of mitochondrial ATP synthase subunits OSCP (ATP5) and gamma (ATP3) alters leaf morphology, metabolism and gene expression in Arabidopsis. Plant Cell Physiol. 50, 1840-1850.
134. Rutter J, Winge DR, Schiffman JD (2010) Succinate dehydrogenase - Assembly, regulation and role in human disease. Mitochondrion 10, 393-401.
135. Sabar M, Balk J, Leaver CJ (2005) Histochemical staining and quantification of plant mitochondrial respiratory chain complexes using blue-native polyacrylamide gel electrophoresis. Plant J. 44, 893-901.
136. Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F(1)F(O)-ATP synthase: Insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep. 4, 1-6.
137. Saisho D, Nakazono M, Lee K, Tsutsumi N, Akita S, Hirai A (2001) The gene for alternative oxidase-2 (AOX2) from Arabidopsis thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination. Genes Genet. Syst. 76, 89-97.
138. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J. 58, 53-68.
139. Saradadevi K, Raghavendra AS (1992) Dark respiration protects photosynthesis against photoinhibtion in mesophyll protoplasts of pea (Pisum sativum). Plant Physiol. 99, 1232-1237.
140. Sarria R, Lyznik A, Vallejos CE, Mackenzie SA (1998) A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell 10, 1217-1228.
141. Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6, 2180-2198.
142. Schulte U (2001) Biogenesis of respiratory complex I. J. Bioenerg. Biomembr. 33, 205-212.
143. Senior AE (1990) The proton-translocating ATPase of Escherichia coli. Ann. Rev. Biophys. Biophys. Chem. 19, 7-41.
144. Shingaki-Wells RN, Huang SB, Taylor NL, Carroll AJ, Zhou WX, Millar AH (2011) Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant Physiol. 156, 1706-1724.
145. Siddique M, Gernhard S, von Koskull-Doring P, Vierling E, Scharf KD (2008) The plant sHSP superfamily: Five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13, 183-197.
146. Smith PM, Fox JL, Winge DR (2012) Biogenesis of the cytochrome bc(1) complex and role of assembly factors. Biochim. Biophys. Acta 1817, 276-286.
147. Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier P, Dauzat M, Heurtevin L, Guyon V, Takenaka M, Rogowsky PM (2012) PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24, 676-691.
148. Stadtman ER (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62, 797-821.
149. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: Flux modes in the plant TCA cycle. Trends Plant Sci. 15, 462-470.
150. 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.
151. Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc. Natl. Acad. Sci. USA 103, 19587-19592.
152. Tan YF, Millar AH, Taylor NL (2012) Components of mitochondrial oxidative phosphorylation vary in abundance following exposure to cold and chemical stresses. J. Prot. Res. 11, 3860-3879.
153. Tan YF, O'Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol. 152, 747-761.
154. Tateda C, Watanabe K, Kusano T, Takahashi Y (2011) Molecular and genetic characterization of the gene family encoding the voltage-dependent anion channel in Arabidopsis. J. Exp. Bot. 62, 4773-4785.
155. 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.
156. 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.
157. Taylor NL, Howell KA, Heazlewood JL, Tan TYW, Narsai R, Huang SB, Whelan J, Millar AH (2010) Analysis of the rice mitochondrial carrier family reveals anaerobic accumulation of a basic amino acid carrier involved in arginine metabolism during seed germination. Plant Physiol. 154, 691-704.
158. Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteomics 72, 367-378.
159. 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.
160. Thirkettle-Watts D, McCabe TC, Clifton R, Moore C, Finnegan PM, Day DA, Whelan J (2003) Analysis of the alternative oxidase promoters from soybean. Plant Physiol. 133, 1158-1169.
161. Tomaz T, Bagard M, Pracharoenwattana I, Linden P, Lee CP, Carroll AJ, Stroher E, Smith SM, Gardestrom P, Millar AH (2010) Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol. 154, 1143-1157.
162. Tuschen G, Sackmann U, Nehls U, Haiker H, Buse G, Weiss H (1990) Assembly of NADH: Ubiquinone reductase (complex I) in Neurospora mitochondria. Independent pathways of nuclear-encoded and mitochondrially encoded subunits. J. Mol. Biol. 213, 845-857.
163. Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J, 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.
164. Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366, 924 nucleotides. Nature Genet. 15, 57-61.
165. Van Aken O, Giraud E, Clifton R, Whelan J (2009) Alternative oxidase: A target and regulator of stress responses. Physiol. Plant. 137, 354-361.
166. van der Merwe MJ, Osorio S, Moritz T, Nunes-Nesi A, Fernie AR (2009) Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol. 149, 653-669.
167. Velours J, Arselin G (2000) The saccharomyces cerevisiae ATP synthase. J. Bioenerg. Biomembr. 32, 383-390.
168. Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem. J. 276, 643-648.
169. Verslues PE, Sharp RE (1999) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiol. 119, 1349-1360.
170. Videira A, Duarte M (2002) From NADH to ubiquinone in Neurospora mitochondria. Biochim. Biophys. Acta 1555, 187-191.
171. Vigani G (2012) Discovering the role of mitochondria in the iron deficiency-induced metabolic responses of plants. J. Plant Physiol. 169, 1-11.
172. Vogel RO, van den Brand MA, Rodenburg RJ, van den Heuvel LP, Tsuneoka M, Smeitink JA, Nijtmans LG (2007) Investigation of the complex I assembly chaperones B17.2L and NDUFAF1 in a cohort of CI deficient patients. Mol. Gen. Met. 91, 176-182.
173. Welchen E, 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.
174. Werhahn W, Braun HP (2002) Biochemical dissection of the mitochondrial proteome from Arabidopsis thaliana by three-dimensional gel electrophoresis. Electrophoresis 23, 640-646.
175. 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.
176. Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH (2007) The cytotoxic lipid peroxidation product 4-hydroxy-2-nonenal covalently modifies a selective range of proteins linked to respiratory function in plant mitochondria. J. Biol. Chem. 282, 37436-37447.
177. Xu P, Yang Y, Zhang Z, Chen W, Zhang C, Zhang L, Zou S, Ma Z (2008) Expression of the nuclear gene TaF(A)d is under mitochondrial retrograde regulation in anthers of male sterile wheat plants with timopheevii cytoplasm. J. Exp. Bot. 59, 1375-1381.
178. Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide 5, 261-270.
179. Zagdanska B (1995) Respiratory energy demand for protein turnover and ion transport in wheat leaves upon water deficit. Physiol. Plant. 95, 428-436.
180. Zottini M, Formentin E, Scattolin M, Carimi F, Lo Schiavo F, Terzi M (2002) Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett. 515, 75-78.