Alternative oxidase: A mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 6805-6847

  Vanlerberghe, Greg C ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Abiotic and biotic stress; Alternative oxidase; Carbon and energy metabolism; Metabolic homeostasis; Photosynthesis; Plant mitochondria; Reactive nitrogen species; Reactive oxygen species; Respiration; Signaling homeostasis

Indexed keywords

ALTERNATIVE OXIDASE; ALUMINUM; CARBON; OXIDOREDUCTASE; OXYGEN; OZONE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN; VEGETABLE PROTEIN;

ABIOTIC STRESS; APOPTOSIS; ARABIDOPSIS; BACTERIUM; BIOTIC STRESS; DROUGHT STRESS; ELECTRON TRANSPORT; ENERGY METABOLISM; ENZYME ACTIVITY; FUNGUS; GENETIC REGULATION; HOMEOSTASIS; METABOLIC HOMEOSTASIS; METABOLITE; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUTRIENT LIMITATION; OXIDATION REDUCTION STATE; PHOTOSYNTHESIS; PLANT GROWTH; PLANT STRESS; REVIEW; SALT STRESS; SIGNAL TRANSDUCTION; SIGNALING HOMEOSTASIS; STRESS; TEMPERATURE STRESS; TOXICITY; VIRUS; CELL RESPIRATION; ENZYMOLOGY; METABOLISM; MITOCHONDRION; PHYSIOLOGICAL STRESS; PLANT;

BACTERIA (MICROORGANISMS);

CELL RESPIRATION; HOMEOSTASIS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDOREDUCTASES; PLANT PROTEINS; PLANTS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84875446745     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14046805     Document Type: Review

References (264)

1. Millar, A.H.; Whelan, J.; Soole, K.L.; Day, D.A. Organization and regulation of mitochondrial respiration in plants. Annu. Rev. Plant Biol. 2011, 62, 79-104.
2. Finnegan, P.M.; Soole, K.L.; Umbach, A.L. Alternative Mitochondrial Electron Transport Proteins in Plants. In Plant Mitochondria: From Genome to Function; Day, D.A., Millar, A.H., Whelan, J., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2004; pp. 163-230.
3. Gifford, R.M. Plant respiration in productivity models: Conceptualization, representation and issues of global terrestrial carbon-cycle research. Funct. Plant Biol. 2003, 30, 171-186.
4. Ciais, Ph.; Reichstein, M.; Viovy, N.; Granier, A.; Ogée, J.; Allard, V.; Aubinet, M.; Buchmann, N.; Bernhofer, Chr.; Carrara, A.; et al. Europe-Wide reduction in primary productivity caused by the heat and drought in 2003. Nature 2005, 437, 529-533.
5. Amthor, J.S. From sunlight to biomass: On the potential efficiency of converting solar radiation to phyto-energy. New Phytol. 2010, 188, 939-959.
6. Zhu, X.-G.; Long, S.P.; Ort, D.R. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 2010, 61, 235-261.
7. Wilson, K.E.; Ivanov, A.G.; Öquist, G.; Grodzinski, B.; Sarhan, F.; Hüner, N.P.A. Energy balance, organellar redox status, and acclimation to environmental stress. Can. J. Bot. 2006, 84, 1355-1370.
8. Scharte, J.; Schön, H.; Weis, E.; von Schaewen, A. Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. Proc. Natl. Acad. Sci. USA 2009, 106, 8061-8066
9. Dal Santo, S.; Stampfl, H.; Krasensky, J.; Kempa, S.; Gibon, Y.; Petutschnig, E.; Rozhon, W.; Heuck, A.; Clausen, T.; Jonak, C. Stress-Induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. Plant Cell 2012, 24, 3380-3392.
10. Møller, I.M. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 561-591.
11. Poyton, R.O.; Ball, K.A.; Castello, P.R. Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 2009, 20, 332-340.
12. Morgan, M.J.; Lehmann, M.; Schwarzländer, M.; Baxter, C.J.; Sienkiewicz-Porzucek, A.; Williams, T.C.R.; Schauer, N.; Fernie, M.D.; Ratcliffe, R.G.; Sweetlove, L.J.; et al. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 2008, 147, 101-114.
13. Planchet, E.; Gupta, K.J.; Sonoda, M.; Kaiser, W.M. Nitric oxide emission from tobacco leaves and cell suspensions: Rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 2005, 41, 732-743.
14. Gupta, K.J.; Fernie, A.R.; Kaiser, W.M.; van Dongen, J.T. On the origins of nitric oxide. Trends Plant Sci. 2010, 16, 160-168.
15. Gleason, C.; Huang, S.; Thatcher, L.F.; Foley, R.C.; Anderson, C.R.; Carroll, A.J.; Millar, A.H.; Singh, K.B. Mitochondrial complex II has a key role in mitochondria-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. USA 2011, 108, 10768-10773.
16. He, J.; Duan, Y.; Hua, D.; Fan, G.; Wang, L.; Liu, Y.; Chen, Z.; Han, L.; Qu, L.-J.; Gong, Z. DEXH Box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 2012, 24, 1815-1833.
17. Rhoads, D.M. Plant Mitochondrial Retrograde Regulation. In Plant Mitochondria; Kempken, F., Ed.; Springer Science + Business Media, LLC 2011: New York, USA, 2011; Volume 1, pp. 411-437.
18. Garmier, M.; Carroll, A.J.; Delannoy, E.; Vallet, C.; Day, D.A.; Small, I.D.; Millar, A.H. Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 2008, 148, 1324-1341.
19. Yu, J.; Nickels, R.; McIntosh, L. A genome approach to mitochondrial-nuclear communication in Arabidopsis. Plant Physiol. Biochem. 2001, 39, 345-353.
20. Umbach, A.L.; Zarkovic, J.; Yu, J.; Ruckle, M.E.; McIntosh, L.; Hock, J.J.; Bingham, S.; White, S.J.; George, R.M.; Subbaiah, C.C.; et al. Comparision of intact Arabidopsis thaliana leaf transcript profiles during treatment with inhibitors of mitochondrial electron transport and TCA cycle. PLoS One 2012, 7, e44339.
21. Busi, M.V.; Gomez-Lobato, M.E.; Rius, S.P.; Turowski, V.R.; Casati, P.; Zabaleta, E.J.; Gomez-Casati, D.F.; Araya, A. Effect of mitochondrial dysfunction on carbon metabolism and gene expression in flower tissues of Arabidopsis thaliana. Mol. Plant 2011, 4, 127-143.
22. Geisler, D.A.; Päpke, C.; Obata, T.; Nunes-Nesi, A.; Matthes, A.; Schneitz, K.; Maximova, E.; Araújo, W.L.; Fernie, A.R.; Persson, S. Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. Plant Cell 2012, 24, 2792-2811.
23. Van Aken, O.; Zhang, B.; Carrie, C.; Uggalla, V.; Paynter, E.; Giraud, E.; Whelan, J. Defining the mitochondrial stress response in Arabidopsis thaliana. Mol. Plant 2010, 2, 1310-1324.
24. Schwarzländer, M.; König, A-C.; Sweetlove, L.J.; Finkemeier, I. The impact of impaired mitochondrial function on retrograde signalling: A meta-analysis of transcriptomic responses. J. Exp. Bot. 2012, 63, 1735-1750.
25. Van Aken, O.; Whelan, J. Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in Arabidopsis. Front. Plant Sci. 2012, doi:10.3389/fpls.2012.00281.
26. Kuzmin, E.V.; Karpova, O.V.; Elthon, T.E.; Newton, K.J. Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins. J. Biol. Chem. 2004, 279, 20672-20677.
27. Leόn, G.; Holuigue, L.; Jordana, X. Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol. 2007, 143, 1534-1546.
28. Falcon de Longevialle, A.; Meyer, E.H.; Andrés, C.; Taylor, N.L.; Lurin, C.; Millar, A.H.; Small, I.D. The pentatricopeptide repeat gene OTP43 is required or trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell 2007, 19, 3256-3265.
29. Van Aken, O.; Pečenková, T.; van de Cotte, B.; de Rycke, R.; Eeckhout, D.; Fromm, H.; de Jaeger, G.; Witters, E.; Beemster, G.T.S.; Inzé, D.; et al. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development. Plant J. 2007, 52, 850-864.
30. Vidal, G.; Ribas-Carbo, M.; Garmier, M.; Dubertret, G.; Rasmusson, A.G.; Mathieu, C.; Foyer, C.H.; de Paepe, R. Lack of respiratory chain Complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 2007, 19, 640-655.
31. Zsigmond, L.; Rigό, G.; Szarka, A.; Székely, G.; Ötvös, K.; Darula, Z.; Medzihradszky, K.F.; Koncz, C.; Koncz, Z.; Szabados, L. Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol. 2008, 146, 1721-1737.
32. Meyer, E.H.; Tomaz, T.; Carroll, A.J.; Estavillo, G.; Delannoy, E.; Tanz, S.K.; Small, I.D.; Pogson, B.J.; Millar, A.H. Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 2009, 151, 603-619.
33. Liu, Y.; He, J.; Chen, Z.; Ren, X.; Hong, X.; Gong, Z. ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. Plant J. 2010, 63, 749-765.
34. Araújo, W.L.; Nunes-Nesi, A.; Nikoloski, Z.; Sweetlove, L.J. Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ. 2012, 35, 1-21.
35. Gupta, K.J.; Shah, J.K.; Brotman, Y.; Jahnke, K.; Willmitzer, L.; Kaiser, W.M.; Bauwe, H.; Igamberdiev, A.U. Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J. Exp. Bot. 2012, 63, 1773-1784.
36. Solheim, C.; Li, L.; Hatzopoulus, P.; Millar, A.H. Loss of Lon1 in Arabidopsis changes the mitochondrial proteome leading to altered metabolic profiles and growth retardation without an accumulation of oxidative damage. Plant Physiol. 2012, 160, 1187-1203.
37. Sosso, D.; Mbelo, S.; Vernoud, V.; Gendrot, G.; Dedieu, A.; Chambrier, P.; Dauzat, M.; Heurtevin, L.; Guyon, V.; Takenaka, M.; et al. PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 2012, 24, 676-691.
38. Welchen, E.; Hildebrandt, T.M.; Lewejohann, D.; Gonzalez, D.H.; Braun, H.-P. Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes I and III. Biochim. Biophys. Acta 2012, 1817, 990-1001.
39. McDonald, A.E.; Vanlerberghe, G.C. Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp. Biochem. Physiol. D 2006, 1, 357-364.
40. Watling, J.R.; Robinson, S.A.; Seymour, R.S. Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus. Plant Physiol. 2006, 140, 1367-1373.
41. Wagner, A.M.; Krab, K.; Wagner, M.J.; Moore, A.L. Regulation of thermogenesis in flowering Araceae: The role of the alternative oxidase. Biochim. Biophys. Acta 2008, 1777, 993-1000.
42. Miller, R.E.; Grant, N.M.; Giles, L.; Ribas-Carbo, M.; Berry, J.A.; Watling, J.R.; Robinson, S.A. In the heat of the night-Alternative pathway respiration drives thermogenesis in Philodendron bipinnatifidum. New Phytol. 2011, 189, 1013-1026.
43. Stenmark, P.; Nordlund, P. A prokaryotic alternative oxidase present in the bacterium Novosphingobium. aromaticivorans. FEBS Lett. 2003, 552, 189-192.
44. Missall, T.A.; Lodge, J.K.; McEwen, J.E. Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukaryot. Cell 2004, 3, 835-846.
45. Chaudhuri, M.; Ott, R.D.; Hill, G.C. Trypanosome alternative oxidase: From molecule to function. Trends Parasitol. 2006, 22, 484-491.
46. Nargang, F.E.; Adames, K.; Rüb, C.; Cheung, S.; Easton, N.; Nargang, C.E. Identification of genes required for alternative oxidase production in the Neurospora crassa gene knockout library. Genes Genomes Genet. 2012, 2, 1345-1356.
47. Scheckhuber, C.Q.; Houthoofd, K.; Weil, A.C.; Werner, A.; de Vresse, A.; Vanfleteren, J.R.; Osiewacz, H.D. Alternative oxidase dependent respiration leads to an increased mitochondrial content in two long-lived mutants of the ageing model Podospora anserina. PLoS One 2011, 6, e16620.
48. McDonald, A.E.; Vanlerberghe, G.C. Branched mitochondrial electron transport in the Animalia: Presence of alternative oxidase in several animal phyla. IUBMB Life 2004, 56, 333-341.
49. Cannino, G.; El-Khoury, R.; Pirinen, M.; Hutz, B.; Rustin, P.; Jacobs, H.T.; Dufour, E. Glucose modulates respiratory Complex I activity in response to acute mitochondrial dysfunction. J. Biol. Chem. 2012, 287, 38729-38740.
50. Humphrey, D.M.; Parsons, R.B.; Ludlow, Z.N.; Riemensperger, T.; Esposito, G.; Verstreken, P.; Jacobs, H.T.; Birman, S.; Hirth, F. Alternative oxidase rescues mitochondria-mediated dopaminergic cell loss in Drosophila. Hum. Mol. Genet. 2012, 21, 2698-2712.
51. El-Khoury, R.; Dufour, E.; Rak, M.; Ramanantsoa, N.; Grandchamp, N.; Csaba, Z.; Duvillié, B.; Bénit, P.; Gallego, J.; Gressens, P.; et al. Alternative oxidase expression in the mouse enables bypassing cytochrome c oxidase blockade and limits mitochondrial ROS overproduction. PLoS Genet. 2013, 9, e1003182.
52. Moller, I.M.; Berczi, A.; van der Plas, L.H.W.; Lambers, H. Measurement of the activity and capacity of the alternative pathway in intact plant tissues: Identification of problems and possible solutions. Physiol. Plant. 1988, 72, 642-649.
53. McDonald, A.E.; Sieger, S.M.; Vanlerberghe, G.C. Methods and approaches to study plant mitochondrial alternative oxidase. Physiol. Plant. 2002, 116, 135-143.
54. Guy, R.D.; Berry, J.A.; Fogel, M.L.; Hoering, T.C. Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 1989, 177, 483-491.
55. Nagel, O.W.; Waldron, S.; Jones, H.G. An off-line implementation of the stable isotope technique for measurements of alternative respiratory pathway activities. Plant Physiol. 2001, 127, 1279-1286.
56. 2 isotopes. Plant Cell Environ. 2012, 35, 1518-1532.
57. Kornfeld, A.; Atkin, O.K.; Griffin, K.L.; Horton, T.W.; Yakir, D.; Turnbull, M.H. Modulation of respiratory metabolism in response to nutrient changes along a soil chronosequence. Plant Cell Environ. 2013, doi:10.1111/pce.12047.
58. Millar, A.H.; Atkin, O.K.; Menz, I.; Henry, B.; Farquhar, G.; Day, D.A. Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiol. 1998, 117, 1083-1093.
59. Florez-Sarasa, I.; Flexas, J.; Rasmusson, A.G.; Umback, A.L.; Siedow, J.N.; Ribas-Carbo, M. In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant Cell Environ. 2011, 34, 1373-1383.
60. Yoshida, K.; Watanabe, C.K.; Terashima, I.; Noguchi, K. Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Environ. 2011, 34, 1890-1899.
61. 2 in Arabidopsis thaliana. Plant Cell Physiol. 2012, 53, 1627-1637.
62. Robinson, S.A.; Ribas-Carbo, M.; Yakir, D.; Giles, L.; Reuveni, Y.; Berry, J.A. Beyond SHAM and cyanide: Opportunities for studying the alternative oxidase in plant respiration using oxygen isotope discrimination. Aust. J. Plant Physiol. 1995, 22, 487-496.
63. Henry, B.K.; Atkin, O.K.; Day, D.A.; Millar, A.H.; Menz, R.I.; Farquhar, G.D. Calculation of the oxygen isotope discrimination factor for studying plant respiration. Aust. J. Plant Physiol. 1999, 26, 773-780.
64. Considine, M.J.; Holtzapffel, R.C.; Day, D.A.; Whelan, J.; Millar, A.H. Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol. 2002, 129, 949-953.
65. Clifton, R.; Millar, A.H.; Whelan, J. Alternative oxidases in Arabidopsis: A comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim. Biophys. Acta 2006, 1757, 730-741.
66. Saisho, D.; Nakazono, M.; Lee, K.H.; Tsutsumi, N.; Akita, S.; Hirai, A. 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. 2001, 76, 89-97.
67. Chai, T.-T.; Simmonds, D.; Day, D.A.; Colmer, T.D.; Finnegan, P.M. Photosynthetic performance and fertility are repressed in GmAOX2b antisense soybean. Plant Physiol. 2010, 152, 1638-1649.
68. Macherel, D.; Benamar, A.; Avelange-Macherel, M.-H.; Tolleter, D. Function and stress tolerance of seed mitochondria. Physiol. Plant. 2007, 129, 233-241.
69. Vanlerberghe, G.C.; McIntosh, L. Mitochondrial electron transport regulation of nuclear gene expression: Studies with the alternative oxidase gene of tobacco. Plant Physiol. 1994, 105, 867-874.
70. Karpova, O.V.; Kuzmin, E.V.; Elthon, T.E.; Newton, K.J. Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 2002, 14, 3271-3284.
71. Vanlerberghe, G.C.; McIntosh, L. Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol. 1996, 111, 589-595.
72. Juszczuk, I.M.; Szal, B.; Rychter, A.M. Oxidation-Reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. Plant Cell Environ. 2012, 35, 296-307.
73. Zarkovic, J.; Anderson, S.L.; Rhoads, D.M. A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis. Plant Mol. Biol. 2005, 57, 871-888.
74. Ng, S.; Giraud, E.; Duncan, O.; Law, S.R.; Wang, Y.; Xu, L.; Narsai, R.; Carrie, C.; Walker, H.; Day, D.A.; et al. Cyclin-Dependent kinase E;1 (CDKE;1) provides a cellular switch in plants between growth and stress responses. J. Biol. Chem. 2013, 288, 3449-3459.
75. Giraud, E.; van Aken, O.; Ho, L.H.M.; Whelan, J. The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 2009, 150, 1286-1296.
76. Leόn, P.; Gregorio, J.; Cordoba, E. ABI4 and its role in chloroplast retrograde communication. Frontiers in Plant. Science 2013, 3, doi:10.3389/fpls.2012.00304.
77. Vanderauwera, S.; Vandenbroucke, K.; Inzé, A.; van de Cotte, B.; Mühlenbock, P.; de Rycke, R.; Naouar, N.; van Gaever, T.; van Montagu, M.C.E.; van Breusegem, F. AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 2012, 109, 20113-20118.
78. Dojcinovic, D.; Krosting, J.; Harris, A.J.; Wagner, D.J.; Rhoads, D.M. Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Mol. Biol. 2005, 58, 159-175.
79. Millenaar, F.F.; Gonzalez-Meler, M.A.; Siedow, J.N.; Wagner A.M.; Lambers, H. Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots. J. Exp. Bot. 2002, 53, 1081-1088.
80. Ho, L.H.M.; Giraud, E.; Uggalla, V.; Lister, R.; Clifton, R.; Glen, A.; Thirkettle-Watts, D.; Van Aken, O.; Whelan, J. Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 2008, 147, 1858-1873.
81. Maxwell, D.P.; Nickels, R.; McIntosh, L. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 2002, 29, 269-279.
82. Li, C.-R.; Liang, D.-D.; Li, J.; Duan, Y.-B.; Li, H.; Yang, Y.-C.; Qin, R.Y.; Li, L.; Wei, P.-C.; Yang, J.-B. Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice ALTERNATIVE OXIDASE 1 genes. Plant Cell Environ. 2013, 36, 775-788.
83. Takahashi, Y.; Berberich, T.; Miyazaki, A.; Seo, S.; Ohashi, Y.; Kusano, T. Spermine signaling in tobacco: Activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J. 2003, 36, 820-829.
84. Arpagaus, S.; Rawyler, A.; Braendle, R. Occurrence and characteristics of the mitochondrial permeability transition in plants. J. Biol. Chem. 2002, 277, 1780-1787.
85. Tiwari, B.S.; Belenghi, B.; Levine, A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 2002, 128, 1271-1281.
86. Rhoads, D.M.; McIntosh, L. Salicylic acid regulation of respiration in higher plants: Alternative oxidase expression. Plant Cell 1992, 4, 1131-1139.
87. Cvetkovska, M.; Vanlerberghe, G.C. Coordination of a mitochondrial superoxide burst during the hypersensitive response to bacterial pathogen in Nicotiana tabacum. Plant Cell Environ. 2012, 35, 1121-1136.
88. Clifton, R.; Lister, R.; Parker, K.L.; Sappl, P.G.; Elhafez, D.; Millar, A.H.; Day, D.A.; Whelan, J. Stress-Induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 2005, 58, 193-212.
89. Ho, L.H.M.; Giraud, E.; Lister, R.; Thirkettle-Watts, D.; Low, J.; Clifton, R.; Howell, K.A.; Carrie, C.; Donald, T.; Whelan, J. Characterization of the regulatory and expression context of an alternative oxidase gene provides insights into cyanide-insensitive respiration during growth and development. Plant Physiol. 2007, 143, 1519-1533.
90. Smith, C.A.; Melino, V.J.; Sweetman, C.; Soole, K.L. Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiol. Plant. 2009, 137, 459-472.
91. Smith, C.; Barthet, M.; Melino, V.; Smith, P.; Day, D.; Soole, K. Alterations in the mitochondrial alternative NAD(P)H dehydrogenase NDB4 lead to changes in mitochondrial electron transport chain composition, plant growth and response to oxidative stress. Plant Cell Physiol. 2011, 52, 1222-1237.
92. Berthold, D.A.; Stenmark, P. Membrane-bound diiron carboxylate proteins. Annu. Rev. Plant Biol. 2003, 54, 497-517.
93. Albury, M.S.; Affourtit, C.; Crichton, P.G.; Moore, A.L. Structure of the plant alternative oxidase: Site-Directed mutagenesis provides new information on the active site and membrane topology. J. Biol. Chem. 2002, 277, 1190-1194.
94. Moore, A.L.; Albury, M.S. Further insights into the structure of the alternative oxidase: From plants to parasites. Biochem. Soc. Trans. 2008, 36, 1022-1026.
95. Berthold, D.A.; Voevodskaya, N.; Stenmark, P.; Gräsland, A.; Nordlund, P. EPR studies of the mitochondrial alternative oxidase: Evidence for a diiron carboxylate center. J. Biol. Chem. 2002, 277, 43608-43614.
96. Moore, A.L.; Carré, J.E.; Affourtit, C.; Albury, M.S.; Crichton, P.G.; Kita, K.; Heathcote, P. Compelling EPR evidence that the alternative oxidase is a diiron carboxylate protein. Biochim. Biophys. Acta 2008, 1777, 327-33.
97. Albury, M.S.; Elliott, C.; Moore, A.L. Ubiquinol-binding site in the alternative oxidase: Mutagenesis reveals features important for substrate binding and inhibition. Biochim. Biophys. Acta 2010, 1797, 1933-1939.
98. Kido, Y.; Shiba, T.; Inaoka, D.K.; Sakamoto, K.; Nara, T.; Aoki, T.; Honma, T.; Tanaka, A.; Inoue, M.; Matsuoka, S.; et al. Crystallization and preliminary analysis of cyanide-insensitive alternative oxidase from Trypanosoma brucei brucei. Acta Crystallogr. 2010, F66, 275-278.
99. Umbach, A.L.; Siedow, J.N. Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol. 1993, 103, 845-854.
100. Rhoads, D.M.; Umbach, A.L.; Sweet, C.R.; Lennon, A.M.; Rauch, G.S.; Siedow, J.N. Regulation of the cyanide-resistant alternative oxidase of plant mitochondria: Identification of the cysteine residue involved in α-keto acid stimulation and intersubunit disulfide bond formation. J. Biol. Chem. 1998, 273, 30750-30756.
101. Vanlerberghe, G.C.; McIntosh, L.; Yip, J.Y.H. Molecular localization of a redox-modulated process regulating plant mitochondrial electron transport. Plant Cell 1998, 10, 1551-1560.
102. Vanlerberghe, G.C.; Day, D.A.; Wiskich, J.T.; Vanlerberghe, A.E.; McIntosh, L. Alternative oxidase activity in tobacco leaf mitochondria: Dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol. 1995, 109, 353-361.
103. Gelhaye, E.; Rouhier, N.; Gérard, J.; Jolivet, Y.; Gualberto, J.; Navrot, N.; Ohlsson, P.-I.; Wingsle, G.; Hirasawa, M.; Knaff, D.B.; et al. A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc. Natl. Acad. Sci. USA 2004, 101, 14545-14550.
104. Millar, A.H.; Wiskich, J.T.; Whelan, J.; Day, D.A. Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett. 1993, 329, 259-262.
105. Carré, J.E.; Affourtit, C.; Moore, A.L. Interaction of purified alternative oxidase from thermogenic Arum maculatum with pyruvate. FEBS Lett. 2011, 585, 397-401.
106. Umbach, A.L.; Gonzàlez-Meler, M.A.; Sweet, C.R.; Siedow, J.N. Activation of the plant mitochondrial alternative oxidase: Insights from site-directed mutagenesis. Biochim. Biophys. Acta 2002, 1554, 118-128.
107. Holtzapffel, R.C.; Castelli, J.; Finnegan, P.M.; Millar, A.H.; Whelan, J.; Day, D.A. A tomato alternative oxidase protein with altered regulatory properties. Biochim. Biophys. Acta 2003, 1606, 153-162.
108. Grant, N.; Onda, Y.; Kakizaki, Y.; Ito, K.; Watling, J.; Robinson, S. Two Cys or not two Cys? That is the question; alternative oxidase in the thermogenic plant sacred lotus. Plant Physiol. 2009, 150, 987-995.
109. Crichton, P.G.; Affourtit, C.; Albury, M.S.; Carré, J.E.; Moore, A.L. Constitutive activity of Sauromatum guttatum alternative oxidase in Schizosaccharomyces pombe implicates residues in addition to conserved cysteines in α-keto acid activation. FEBS Lett. 2005, 579, 331-336.
110. Umbach, A.L.; Ng, V.S.; Siedow, J.N. Regulation of plant alternative oxidase activity: A tale of two cysteines. Biochim. Biophys. Acta 2006, 1757, 135-142.
111. Guy, R.D.; Vanlerberghe, G.C. Partitioning of respiratory electrons in the dark in leaves of transgenic tobacco with modified levels of alternative oxidase. Physiol. Plant. 2005, 125, 171-180.
112. Purvis, A.C. Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 1997, 100, 165-170.
113. Cvetkovska, M.; Vanlerberghe, G.C. Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol. 2012, 195, 32-39.
114. Cvetkovska, M.; Vanlerberghe, G.C. Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 2013, 36, 721-732.
115. 2 effects on plant carbon, nitrogen, and water relations: Six important lessons from FACE. J. Exp. Bot. 2009, 60, 2859-2876.
116. 2 in thee invasive Opuntia ficus-indica. Plant Physiol. 2007, 145, 49-61.
117. Gandin, A.; Lapointe, L.; Dizengremel, P. The alternative respiratory pathway allows sink to cope with changes in carbon availability in the sink-limited plant Erythronium americanum. J. Exp. Bot. 2009, 60, 4235-4248.
118. Escobar, M.A.; Geisler, D.A.; Rasmusson, A.G. Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: Opposing effects of ammonium and nitrate. Plant J. 2006, 45, 775-788.
119. Hachiya, T.; Watanabe, C.K.; Boom, C.; Tholen, D.; Takahara, K.; Kawai-Yamada, M.; Uchimiya, H.; Uesono, Y.; Terashima, I.; Noguchi, K. Ammonium-dependent respiratory increase is dependent on the cytochrome pathway in Arabidopsis thaliana shoots. Plant Cell Environ. 2010, 33, 1888-1897.
120. Lambers, H.; Szaniawski, R.K.; de Visser, R. Respiration for growth, maintenance and ion uptake: An evaluation of concept, methods, values and their significance. Physiol. Plant. 1983, 58, 556-563.
121. Poorter, H.; van der Werf, A.; Atkin, O.K.; Lambers, H. Respiratory energy requirements of roots vary with the potential growth rate of a plant species. Physiol. Plant. 1991, 83, 469-475.
122. 4 + cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proc. Natl. Acad. Sci. USA 2001, 98, 4255-4258.
123. Kurimoto, K.; Millar, A.H.; Lambers, H.; Day, D.A.; Noguchi, K. Maintenance of growth rate at low temperature in rice nad wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiol. 2004, 45, 1015-1022.
124. + cycling at the root plasma membrane in rice (Oryza. sativa, L.): Kinetics, energetics, and relationship to salinity tolerance. J. Exp. Bot. 2008, 59, 4109-4117.
125. Noctor, G.; De Paepe, R.; Foyer, C.H. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 2007, 12, 125-134.
126. Diamond, M.; McCabe, P.F. Mitochondrial Regulation of Plant Programmed Cell Death. In Plant Mitochondria; Kempken, F., Ed.; Springer Science + Business Media, LLC 2011: New York, NY, USA, 2011; Volume 1, pp. 439-465.
127. Echtay, K.S. Mitochondrial uncoupling proteins-What is their physiological function? Free Radic. Biol. Med. 2007, 43, 1351-1371.
128. Amirsadeghi, S.; Robson, C.A.; McDonald, A.E.; Vanlerberghe G.C. Changes in plant mitochondrial electron transport alter cellular levels of reactive oxygen species and susceptibility to cell death signaling molecules. Plant Cell Physiol. 2006, 47, 1509-1519.
129. Giraud, E.; Ho, L.H.M.; Clifton, R.; Carroll, A.; Estavillo, G.; Tan, Y.-F.; Howell, K.A.; Ivanov, A.; Pogson, B.J.; Millar, A.H.; et al. The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 2008, 147, 595-610.
130. Sweetlove, L.J.; Lytovchenko, A.; Morgan, M.; Nunes-Nesi, A.; Taylor, N.L.; Baxter, C.J.; Eickmeier, I.; Fernie, A.R. Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc. Natl. Acad. Sci. USA 2006, 103, 19587-19592.
131. Timm, S.; Florian, A.; Arrivault, S.; Stitt, M.; Fernie, A.R. Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett. 2012, 586, 3692-3697.
132. Palmieri, M.C.; Lindermayr, C.; Bauwe, H.; Steinhauser, C.; Durner, J. Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol. 2010, 152, 1514-1528.
133. Taylor, N.L.; Day, D.A.; Millar, A.H. Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J. Biol. Chem. 2002, 277, 42663-42668.
134. Noctor, G. Metabolic signaling in defense and stress: The central roles of soluble redox couples. Plant Cell Environ. 2006, 29, 409-425.
135. Liu, Y.-J.; Nunes-Nesi, A.; Wallström, S.V.; Lager, I.; Michalecka, A.M.; Norberg, F.E.B.; Widell, S.; Fredlund, K.M.; Fernie, A.R.; Rasmusson, A.G. A redox-mediated modulation of stem bolting in transgenic Nicotiana sylvestris differentially expressing the external mitochondrial NADPH dehydrogenase. Plant Physiol. 2009, 150, 1248-1259.
136. Verdin, E.; Hirschey, M.D.; Finley, L.W.S.; Haigis, M.C. Sirtuin regulation of mitochondria: Energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35, 669-675.
137. Finkemeier, I.; Laxa, M.; Miguet, L.; Howden, A.J.M.; Sweetlove, L.J. Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiol. 2011, 155, 1779-1790.
138. Wu, X.; Oh, M.-H.; Schwarz, E.M.; Larue, C.T.; Sivaguru, M.; Imai, B.S.; Yau, P.M.; Ort, D.R.; Huber, S.C. Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol. 2011, 155, 1769-1778.
139. Millar, A.H.; Mittova, V.; Kiddle, G.; Heazlewood, J.L.; Bartoli, C.T.G.; Theodoulou, F.L.; Foyer, C.H. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 2003, 133, 443-447.
140. Bartoli, C.G.; Gόmez, F.; Fernández, L.; McIntosh, L.; Foyer, C.H. Inter-Relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J. Exp. Bot. 2006, 57, 1621-1631.
141. Wang, J.; Rajakulendran, N.; Amirsadeghi, S.; Vanlerberghe, G.C. Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol. Plant. 2011, 142, 339-351.
142. Vanlerberghe, G.C.; McIntosh, L. Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol. 1992, 100, 115-119.
143. Ito, Y.; Saisho, D.; Nakazono, M.; Tsutsumi, N.; Hirai, A. Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 1997, 203, 121-129.
144. Gonzàlez-Meler, M.A.; Ribas-Carbo, M.; Giles, L.; Siedow, J.N. The effect of growth and measurement temperature on the activity of the alternative respiratory pathway. Plant Physiol. 1999, 120, 765-772.
145. Fiorani, F.; Umbach, A.L.; Siedow, J.N. The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol. 2005, 139, 1795-1805.
146. Sugie, A.; Naydenov, N.; Mizuno, N.; Nakamura, C.; Takumi, S. Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet. Syst. 2006, 81, 349-354.
147. Campbell, C.; Atkinson, L.; Zaragoza-Castells, J.; Lundmark, M.; Atkin, O.; Hurry, V. Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytol. 2007, 176, 375-389.
148. Armstrong, A.F.; Badger, M.R.; Day, D.A.; Barthet, M.M.; Smith, P.M.C.; Millar, A.H.; Whelan, J.; Atkin, O.K. Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant Cell Environ. 2008, 31, 1156-1169.
149. Mizuno, N.; Sugie, A.; Kobayashi, F.; Takumi, S. Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. J. Plant Physiol. 2008, 165, 462-467.
150. Usadel, B.; Bläsing, O.E.; Gibon, Y.; Poree, F.; Höhne, M.; Günter, M.; Trethewey, R.; Kamlage, B.; Poorter, H.; Stitt, M. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 2008, 31, 518-547.
151. Watanabe, C.K.; Hachiya, T.; Terashima, I.; Noguchi, K. The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defense systems in Arabidopsis thaliana leaves. Plant Cell Environ. 2008, 31, 1190-1202.
152. Umbach, A.L.; Lacey, E.P.; Richter, S.J. Temperature-Sensitive alternative oxidase protein content and its relationship to floral reflectance in natural Plantago lanceolata populations. New Phytol. 2009, 181, 662-671.
153. Wang, H.; Huang, J.; Liang, X.; Bi, Y. Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus. Planta 2012, 235, 53-67.
154. Shi, K.; Fu, L.-J.; Zhang, S.; Li, X.; Liao, Y.-W.-K.; Xia, X.-J.; Zhou, Y.-H.; Wang, R.-Q.; Chen, Z.-X.; Yu, J.-Q. Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants. Planta 2013, 237, 589-601.
155. MacFarlane, C.; Hansen, L.D.; Florez-Sarasa, I.; Ribas-Carbo, M. Plant mitochondria electron partitioning is independent of short-term temperature changes. Plant Cell Environ. 2009, 32, 585-591.
156. Ribas-Carbo, M.; Aroca, R.; Gonzàlez-Meler, M.A.; Irigoyen, J.J.; Sánchez-Díaz, M. The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol. 2000, 122, 199-204.
157. Searle, S.Y.; Thomas, S.; Griffin, K.L.; Horton, T.; Kornfeld, A.; Yakir, D.; Hurry, V.; Turnbull, M.H. Leaf respiration and alternative oxidase in field-grown alpine grasses respond to natural changes in temperature and light. New Phytol. 2011, 189, 1027-1039.
158. Rachmilevitch, S.; Xu, Y.; Gonzalez-Meler, M.A.; Huang, B.; Lambers, H. Cytochrome and alternative pathway activity in roots of thermal and non-thermal Agrostis species in response to high soil temperature. Physiol. Plant. 2007, 129, 163-174.
159. Searle, S.Y.; Turnbull, M.H. Seasonal variation of leaf respiration and the alternative pathway in field-grown Populus × canadensis. Physiol. Plant. 2011, 141, 332-342.
160. Searle, S.Y.; Bitterman, D.S.; Thomas, S.; Griffin, K.L.; Atkin, O.K.; Turnbull, M.H. Respiratory alternative oxidase responds to both low-and high-temperature stress in Quercus rubra leaves along an urban-rural gradient in New York. Funct. Ecol. 2011, 25, 1007-1017.
161. Murakami, Y.; Toriyama, K. Enhanced high temperature tolerance in transgenic rice seedlings with elevated levels of alternative oxidase, OsAOX1a. Plant Biotechnol. 2008, 25, 361-364.
162. Flexas, J.; Bota, J.; Galmés, J.; Medrano, H.; Ribas-Carbo, M. Keeping a positive carbon balance under adverse conditions: Responses of photosynthesis and respiration to water stress. Physiol. Plant. 2006, 127, 343-352.
163. Atkin, O.K.; Macherel, D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 2009, 103, 581-597.
164. Lawlor, D.W.; Tezara, W. Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: A critical evaluation of mechanisms and integration of processes. Ann. Bot. 2009, 103, 561-579.
165. Bartoli, C.G.; Gomez, F.; Gergoff, G.; Guiamét, J.J.; Puntarulo, S. Up-Regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J. Exp. Bot. 2005, 56, 1269-1276.
166. Vassileva, V.; Simova-Stoilova, L.; Demirevska, K.; Feller, U. Variety-specific response of wheat (Triticum aestivum, L.) leaf mitochondria to drought stress. J. Plant Res. 2009, 122, 445-454.
167. Ribas-Carbo, M.; Taylor, N.L.; Giles, L.; Busquets, S.; Finnegan, P.M.; Day, D.A.; Lambers, H.; Medrano, H.; Berry, J.A.; Flexas, J. Effects of water stress on respiration in soybean leaves. Plant Physiol. 2005, 139, 466-473.
168. Filippou, P.; Antoniou, C.; Fotopoulos, V. Effect of drought and rewatering on the cellular status and antioxidant response of Medicago trunculata plants. Plant Signal. Behav. 2011, 6, 270-277.
169. Galle, A.; Florez-Sarasa, I.; Thameur, A.; de Paepe, R.; Flexas, J.; Ribas-Carbo, M. Effects of drought stress and subsequent rewatering on photosynthesis and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII. J. Exp. Bot. 2010, 61, 765-775.
170. Juszczuk, I.M.; Wagner, A.M.; Rychter, A.M. Regulation of alternative oxidase activity during phosphate deficiency in bean roots (Phaseolus vulgaris). Physiol. Plant. 2001, 113, 185-192.
171. Gonzàlez-Meler, M.A.; Giles, L.; Thomas, R.B.; Siedow, J.N. Metabolic regulation of leaf respiration and alternative oxidase activity in response to phosphate supply. Plant Cell Environ. 2001, 24, 205-215.
172. Parsons, H.L.; Yip, J.Y.H.; Vanlerberghe, G.C. Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol. 1999, 121, 1309-1320.
173. Vijayraghavan, V.; Soole, K. Effect of short-and long-term phosphate stress on the non-phosphorylating pathway of mitochondrial electron transport in Arabidopsis thaliana. Funct. Plant Biol. 2010, 37, 455-466.
174. Rychter, A.M.; Mikulska, M. The relationship between phosphate status and cyanide-resistant respiration in bean roots. Physiol. Plant. 1990, 79, 663-667.
175. Theodorou, M.E.; Plaxton, W.C. Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol. 1993, 101, 339-344.
176. Sieger, S.M.; Kristensen, B.K.; Robson, C.A.; Amirsadeghi, S.; Eng, E.W.Y.; Abdel-Mesih, A.; Møller, I.M.; Vanlerberghe, G.C. The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J. Exp. Bot. 2005, 56, 1499-1515.
177. Yip, J.Y.H.; Vanlerberghe, G.C. Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol. Plant. 2001, 112, 327-333.
178. Noguchi, K.; Terashima, I. Responses of spinach leaf mitochondria to low N availability. Plant Cell Environ. 2006, 29, 710-719.
179. Kornfeld, A.; Heskel, M.; Atkin, O.K.; Gough, L.; Griffin, K.L.; Horton, T.W.; Turnbull, M.H. Respiratory flexibility and efficiency are affected by simulated global change in Arctic plants. New Phytol. 2013, 197, 1161-1172.
180. Mittova, V.; Tal, M.; Volokita, M.; Guy, M. Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ. 2003, 26, 845-856.
181. Mittova, V.; Guy, M.; Tal, M.; Volokita, M. Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J. Exp. Bot. 2004, 55, 1105-1113.
182. Chen, X.; Wang, Y.; Li, J.; Jiang, A.; Cheng, Y.; Zhang, W. Mitochondrial proteome during salt stress-induced programmed cell death in rice. Plant Physiol. Biochem. 2009, 47, 407-415.
183. Zsigmond, L.; Szepesi, A.; Tari, I.; Rigό, G.; Király, A.; Szabados, L. Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci. 2012, 182, 87-93.
184. Andronis, E.A.; Roubelakis-Angelakis, K.A. Short-Term salinity stress in tobacco leads to the onset of animal-like PCD hallmarks in planta in contrast to long-term stress. Planta 2010, 231, 437-448.
185. Kreps, J.A.; Wu, Y.; Chang, H.-S.; Zhu, T.; Wang, X.; Harper, J.F. Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress. Plant Physiol. 2002, 130, 2129-2141.
186. Seki, M.; Narusaka, M.; Ishida, J.; Nanjo, T.; Fijita, M.; Oono, Y.; Kamiya, A.; Nakajima, M.; Enju, A.; Sakurai, T.; et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 2002, 31, 279-292.
187. Marti, M.C.; Florez-Sarasa, I.; Camejo, D.; Ribas-Carbό, M.; Lázaro, J.J.; Sevilla, F.; Jiménez, A. Response of mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to salinity in pea (Pisum sativum, L.) leaves. J. Exp. Bot. 2011, 62, 3863-3874.
188. Ottow, E.A.; Brinker, M.; Teichmann, T.; Fritz, E.; Kaiser, W.; Brosché, M.; Kangasjärvi, J.; Jiang, X.; Polle, A. Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol. 2005, 139, 1762-1772.
189. Wang, H.; Liang, X.; Huang, J.; Zhang, D.; Lu, H.; Liu, Z.; Bi, Y. Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol. 2010, 51, 1754-1765.
190. Ederli, L.; Morettini, R.; Borgogni, A.; Wasternack, C.; Miersch, O.; Reale, L.; Ferranti, F.; Tosti, N.; Pasqualini, S. Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol. 2006, 142, 595-608.
191. Pasqualini, S.; Reale, L.; Calderini, O.; Pagiotti, R.; Ederli, L. Involvement of protein kinases and calcium in the NO-signalling cascade for defence-gene induction in ozonated tobacco plants. J. Exp. Bot. 2012, 63, 4485-4496.
192. 3-treated Arabidopsis plants. Plant Cell Environ. 2006, 29, 1686-1702.
193. Kristensen, B.K.; Askerlund, P.; Bykova, N.V.; Egsgaard, H.; Møller, I.M. Identification of oxidized proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 2004, 65, 1839-1851.
194. Tan, Y.-F.; O'Toole, N.; Taylor, N.L.; Millar, A.H. Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol. 2010, 152, 747-761.
195. Yamamoto, Y.; Kobayashi, Y.; Devi, S.R.; Matsumoto, H. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol. 2002, 128, 63-72.
196. Li, Z.; Xing, D. Mechanistic study of mitochondria-dependent programmed cell death induced by aluminum phytotoxicity using fluorescence techniques. J. Exp. Bot. 2011, 62, 331-343.
197. Panda, S.K.; Sahoo, L.; Katsuhara, M.; Matsumoto, H. Overexpression of alternative oxidase gene confers aluminum tolerance by altering the respiratory capacity and the response to oxidative stress in tobacco cells. Mol. Biotechnol. 2013, doi:10.1007/s12033-012-9595-7.
198. 2+ stress in Euglena. J. Bioenerg. Biomembr. 2008, 40, 227-235.
199. Pádua, M.; Aubert, S.; Casimiro, A.; Bligny, R.; Millar, A.H.; Day, D.A. Induction of alternative oxidase by excess copper in sycamore cell suspensions. Plant Physiol. Biochem. 1999, 37, 131-137.
200. 2-induced cell death: possible involvement of peroxidases and of alternative oxidase. FEBS Lett. 2000, 477, 175-180.
201. Tsuji, H.; Nakazono, M.; Saisho, D.; Tsutsumi, N.; Hirai, A. Transcript levels of the nuclear-encoded respiratory genes in rice decrease by oxygen deprivation: Evidence for involvement of calcium in expression of the alternative oxidase 1a gene. FEBS Lett. 2000, 471, 201-204.
202. Klok, E.J.; Wilson, I.W.; Wilson, D.; Chapman, S.C.; Ewing, R.M.; Somerville, S.C.; Peacock, W.J.; Dolferus, R.; Dennis, E.S. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 2002, 14, 2481-2494.
203. Szal, B.; Jolivet, Y.; Hasenfratz-Sauder, M.-P.; Dizengremel, P.; Rychter, A.M. Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia. Physiol. Plant. 2003, 119, 494-502.
204. Liu, F.; VanToai, T.; Moy, L.P.; Bock, G.; Linford, L.D.; Quackenbush, J. Global transcription profiling revelas comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol. 2005, 137, 1115-1129.
205. Kreuzwieser, J.; Hauberg, J.; Howell, K.A.; Carroll, A.; Rennenberg, H.; Millar, A.H.; Whelan, J. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol. 2009, 149, 461-473.
206. Skutnik, M.; Rychter, A.M. Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. J. Plant Physiol. 2009, 166, 926-937.
207. 2 and ethylene. J. Exp. Bot. 2012, 63, 4123-4131.
208. Millar, A.H.; Bergersen, F.J.; Day, D.A. Oxygen affinity of terminal oxidases in soybean mitochondria. Plant Physiol. Biochem. 1994, 32, 847-852.
209. Ribas-Carbo, M.; Berry, J.A.; Azcon-Bieto, J.; Siedow, J.N. The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen. Biochim. Biophys. Acta 1994, 118, 205-212.
210. Leitner, M.; Vandelle, E.; Gaupels, F.; Bellin, D.; Delledonne, M. NO signals in the haze. Nitric oxide signaling in plant defense. Curr. Opin. Plant Biol. 2009, 12, 451-458.
211. Vlot, A.C.; Dempsey, D.A.; Klessig, D.F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 2009, 47, 177-206.
212. Spoal, S.H.; Loake, G.J. Redox-Based protein modifications: The missing link in plant immune signaling. Curr. Opin. Plant Biol. 2011, 14, 358-364.
213. Norman, C.; Howell, K.A.; Millar, A.H.; Whelan, J.M.; Day, D.A. Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 2004, 134, 492-501.
214. Millar, A.H.; Day, D.A. Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase on plant mitochondria. FEBS Lett. 1996, 398, 155-158.
215. Lacomme, C.; Roby, D. Identification of new early markers of the hypersensitive response in Arabidopsis thaliana. FEBS Lett. 1999, 459, 149-153.
216. Simons, B.H.; Millenaar, F.F.; Mulder, L.; van Loon, L.C.; Lambers, H. Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv. tomato. Plant Physiol. 1999, 120, 529-538.
217. Amirsadeghi, S.; Robson, C.A.; Vanlerberghe, G.C. The role of the mitochondrion in plant responses to biotic stress. Physiol. Plant. 2007, 129, 253-266.
218. Sun, A.; Nie, S.; Xing, D. Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides. Plant Physiol. 2012, 160, 1081-1096.
219. Chivasa, S.; Murphy, A.M.; Naylor, M.; Carr, J.P. Salicylic acid interferes with Tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 1997, 9, 547-557.
220. Ordog, S.H.; Higgins, V.J.; Vanlerberghe, G.C. Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol. 2002, 129, 1858-1865.
221. Gilliland, A.; Singh, D.P.; Hayward, J.M.; Moore, C.A.; Murphy, A.M.; York, C.J.; Slator, J.; Carr, J.P. Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol. 2003, 132, 1518-1528.
222. Dutilleul, C.; Garmier, M.; Noctor, G.; Mathieu, C.; Chétrit, P.; Foyer, C.H.; de Paepe, R. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 2003, 15, 1212-1226.
223. Király, L.; Künstler, A.; Höller, K.; Fattinger, M.; Juhász, C.; Müller, M.; Gullner, G.; Zechmann, B. Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response. Plant Physiol. Biochem. 2012, 59, 44-54.
224. Zhu, L.; Li, Y.; Li, L.; Yang, J.; Zhang, M. Ethylene is involved in leafy mustard systemic resistance to Turnip mosaic virus infection through the mitochondrial alternative oxidase pathway. Physiol. Mol. Plant Pathol. 2011, 76, 166-172.
225. Liao, Y.-W.-K.; Shi, K.; Fu, L.-J.; Zhang, S.; Li, X.; Dong, D.-K.; Jiang, Y.-P.; Zhou, Y.-H.; Xia, X.-J.; Liang, W.-S.; et al. The reduction of reactive oxygen species formation by mitochondrial alternative respiration in tomato basal defense against TMV infection. Planta 2012, 235, 225-238.
226. Norman, E.G.; Walton, A.B.; Turpin, D.H. Immediate activation of respiration in Petroselinum crispum, L. in response to the Phytophthora megasperma f. sp. Glycinea elicitor. Plant Physiol. 1994, 106, 1541-1546.
227. Naton, B.; Hahlbrock, K.; Schmelzer, E. Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells. Plant Physiol. 1996, 112, 433-444.
228. Scharte, J.; Schön, H.; Weis, E. Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora. nicotianae. Plant Cell Environ. 2005, 28, 1421-1435.
229. Manzoor, H.; Chiltz, A.; Madani, S.; Vatsa, P.; Schoefs, B.; Pugin, A.; Garcia-Brugger, A. Calcium signatures and signaling in cytosol and organelles of tobacco cells induced by plant defense elicitors. Cell Calcium 2012, 51, 434-444.
230. Ashtamker, C.; Kiss, V.; Sagi, M.; Davydov, O.; Fluhr, R. Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco Bright Yellow-2 cells. Plant Physiol. 2007, 143, 1817-1826.
231. Yao, N.; Tada, Y.; Sakamoto, M.; Nakayashiki, H.; Park, P.; Tosa, Y.; Mayama, S. Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J. 2002, 30, 567-579.
232. Seo, S.; Mitsuhara, I.; Feng, J.; Iwai, T.; Hasegawa, M.; Ohashi, Y. Cyanide, a coproduct of plant hormone ethylene biosynthesis, contributes to the resistance of rice to blast fungus. Plant Physiol. 2011, 155, 502-514.
233. Astier, J.; Besson-Bard, A.; Lamotte, O.; Bertoldo, J.; Bourque, S.; Terenz, H.; Wendehenne, D. Nitric oxide inhibits the ATPase activity of the chaperone-like AAA+ ATPase CDC48, a target for S-nitrosylation in cryptogein signalling in tobacco cells. Biochem. J. 2012, 447, 249-260.
234. Hoefnagel, M.H.N.; Atkin, O.K.; Wiskich, J.T. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta 1998, 1366, 235-255.
235. Raghavendra, A.S.; Padmasree, K. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 2003, 8, 546-553.
236. Noctor, G.; Dutilleul, C.; de Paepe, R.; Foyer, C.H. Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J. Exp. Bot. 2004, 55, 49-57.
237. Noguchi, K.; Yoshida, K. Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 2008, 8, 87-99.
238. Yoshida, K.; Terashima, I.; Noguchi, K. Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant Cell Physiol. 2006, 47, 22-31.
239. Dinakar, C.; Abhaypratap, V.; Yearla, S.R.; Raghavendra, A.S.; Padmasree, K. Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Planta 2010, 231, 461-474.
240. Dinakar, C.; Raghavendra, A.S.; Padmasree, K. Importance of AOX pathway in optimizing photosynthesis under high light stress: Role of pyruvate and malate in activating AOX. Physiol. Plant. 2010, 139, 13-26.
241. Zhang, L.-T.; Zhang, Z.-S.; Gao, H.-Y.; Xue, Z.-C.; Yang, C.; Meng, X.-L. Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex. K-1 leaves. Physiol. Plant. 2011, 143, 396-407.
242. Yoshida, K.; Noguchi, K. Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant Cell Physiol. 2009, 50, 1449-1462.
243. Yoshida, K.; Watanabe, C.K.; Hachiya, T.; Tholen, D.; Shibata, M.; Terashima, I.; Noguchi, K. Distinct responses of the mitochondrial respiratory chain to long-and short-term high-light environments in Arabidopsis thaliana. Plant Cell Environ. 2011, 34, 618-628.
244. Noguchi, K.; Taylor, N.L.; Millar, A.H.; Lambers, H.; Day, D.A. Response of mitochondria to light intensity in the leaves of sun and shade species. Plant Cell Environ. 2005, 28, 760-771.
245. Pastore, D.; Trono, D.; Laus, M.N.; di Fonzo, N.; Passarella, S. Alternative oxidase in durum wheat mitochondria. Activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant Cell Physiol. 2001, 42, 1373-1382.
246. Noguchi, K.; Go, C.-S.; Terashima, I.; Ueda, S.; Yoshinari, T. Activities of the cyanide-resistant respiratory pathway in leaves of sun and shade species. Austr. J. Plant Physiol. 2001, 28, 27-35.
247. Yoshida, K.; Terashima, I.; Noguchi, K. Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol. 2007, 48, 606-614.
248. Rosso, D.; Bode, R.; Li, W.; Krol, M.; Saccon, D.; Wang, S.; Schillaci, L.A.; Rodermel, S.R.; Maxwell, D.P.; Hüner, N.P.A. Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 2009, 21, 3473-3492.
249. Fu, A.; Liu, H.; Yu, F.; Kambakam, S.; Luan, S.; Rodermel, S. Alternative oxidases (AOX1a and AOX2) can functionally substitute for plastid terminal oxidase in Arabidopsis chloroplasts. Plant Cell 2012, 24, 1579-1595.
250. Umbach, A.L.; Fiorani, F.; Siedow, J.N. Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol. 2005, 139, 1806-1820.
251. Zhang, D.-W.; Xu, F.; Zhang, Z.-W.; Chen, Y.-E.; Du, J.-B.; Jia, S.-D.; Yuan, S.; Lin, H.-H. Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. Plant Cell Environ. 2010, 33, 2121-2131.
252. Zidenga, T.; Leyva-Guerrero, E.; Moon, H.; Siritunga, D.; Sayre, R. Extending cassava root shelf life via reduction of reactive oxygen species production. Plant Physiol. 2012, 159, 1396-1407.
253. García, I.; Castellano, J.M.; Vioque, B.; Solano, R.; Gotor, C.; Romero, L.C. Mitochondrial β-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 2010, 22, 3268-3279.
254. Álvarez, C.; García, I.; Romero, L.C.; Gotor, C. Mitochondrial sulfide detoxification requires a functional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol. Plant 2012, 5, 1217-1226.
255. Gapper, C.; Dolan, L. Control of plant development by reactive oxygen species. Plant Physiol. 2006, 141, 341-345.
256. Blom, D.; Fabbri, C.; Eberl, L.; Weisskopf, L. Volatile-Mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl. Environ. Microbiol. 2011, 77, 1000-1008.
257. Pasqualini, S.; Paolocci, F.; Borgogni, A.; Morettini, R.; Ederli, L. The overexpression of an alternative oxidase gene triggers ozone sensitivity in tobacco plants. Plant Cell Environ. 2007, 30, 1545-1556.
258. Zhang, L.; Oh, Y.; Li, H.; Baldwin, I.T.; Galis, I. Alternative oxidase in resistance to biotic stresses: Nicotiana. attenuata AOX contributes to resistance to a pathogen and a piercing-sucking insect but not Manduca. sexta larvae. Plant Physiol. 2012, 160, 1453-1467.
259. Mathy, G.; Cardol, P.; Dinant, M.; Blomme, A.; Gérin, S.; Cloes, M.; Ghysels, B.; DePauw, E.; Leprince, P.; Remacle, C.; et al. Proteomic and functional characterization of a Chlamydomonas. reinhardtii mutant lacking the mitochondrial alternative oxidase 1. J. Proteome Res. 2010, 9, 2825-2838.
260. Millenaar, F.F.; Gonzàlez-Meler, M.A.; Fiorani, F.; Welschen, R.; Ribas-Carbo, M.; Siedow, J.N.; Wagner, A.M.; Lambers, H. Regulation of alternative oxidase in six wild monocotyledonous species. An in vivo study at the whole root level. Plant Physiol. 2001, 126, 376-387.
261. Florez-Sarasa, I.D.; Bouma, T.J.; Medrano, H.; Azcon-Bieto, J.; Ribas-Carbo, M. Contribution of the cytochrome and alternative pathways to growth respiration and maintenance respiration in Arabidopsis thaliana. Physiol. Plant. 2007, 129, 143-151.
262. Chai, T.-T.; Simmonds, D.; Day, D.A.; Colmer, T.D.; Finnegan, P.M. A GmAOX2b antisense gene compromises vegetative growth and seed production in soybean. Planta 2012, 236, 199-207.
263. Skirycz, A.; de Bodt, S.; Obata, T.; de Clercq, I.; Claeys, H.; de Rycke, R.; Andriankaja, M.; van Aken, O.; van Breusegem, F.; Fernie, A.R.; et al. Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged osmotic stress. Plant Physiol. 2010, 152, 226-244.
264. Shiba, T.; Kido, Y.; Sakamoto, K.; Inaoka, D.K.; Tsuge, C.; Tatsumi, R.; Takahashi, G.; Balogun, E.O.; Nara, T.; Aoki, T.; et al. Structure of the trypanosome cyanide-insensitive alternative oxidase. Proc. Natl. Acad. Sci. USA 2013, doi:10.1073/pnas.1218386110.