Abiotic stress trigger mitochondrial defense system: A comprehensive review.

محورهای موضوعی : Plant Physiology

Khalil saad-Allah ¹ ( Botany Department, Faculty of Science, Tanta University, Tanta, 31527, Egypt )
Ibrahim Abdelsalam ² ( Botany Department, Faculty of Science, Tanta University, Tanta, 31527, Egypt. )

تاریخ دریافت : 1398/06/19 تاریخ پذیرش : 1399/04/30 تاریخ انتشار : 1399/01/13

کلید واژه: abiotic stress, Mitochondria, uncoupling proteins, mitochondrial retrograde, alternative oxidases,

چکیده مقاله :

Mitochondria are small organelles widely distributed within the cells of living organisms. Its main function is the oxidative phosphorylation-coupled ATP synthesis. Under abiotic stress conditions mitochondrial function is significantly affected triggering the mitochondrial stress response. However, the stressful conditions could increase the chance of ROS generation in various cellular organelles. Plant cells struggle ROS generation through the induction of specific enzymatic and non-enzymatic defense systems. Nevertheless, the excessive accumulation of ROS within mitochondria induce mitochondrial signaling and the cellular responses to mitochondrial dysfunction in a process known as mitochondrial retrograde regulation. The exclusive accumulation of ROS cause severe disorders in ROS homoeostasis that stimulate progremmed cell death. The inner mitochondrial membrane have uncoupling mitochondrial proteins (UMP) to keep mitochondrial integrity and function at both normal and stress conditions. Mitochondria can perform nonphosphorylating respiration under the stress conditions, like the presence of respiration inhibitors, by the help of specific proteins called alternative oxidases (AOX). The expression of AOX or its mRNA has been reported to be induced by various abiotic stress conditions. The expression of AOX play an important role in acclimation to many stress conditions like salinity, temperature and drought in various plant species.

منابع و مأخذ:

Amirsadeghi, S., C. A. Robson, A. E. McDonald and G. C. Vanlerberghe, 2006. 'Changes in plant mitochondrial electron transport alter cellular levels of reactive oxygen species and susceptibility to cell death signaling molecules'. Plant and Cell Physiology, 47 (11):1509–1519.

Andreyev, A. Y., Y. E. Kushnareva and A. A. Starkov, 2005. 'Mitochondrial metabolism of reactive oxygen species'. Biochemistry (Moscow), 70 (2):200–214.

Asada, K. 1987. 'Production and scavenging of active oxygen in photosynthesis'; Pp. 227–287. In Photoinhibition, 9th ed. D. J. Kyle,, C. B. Osmond, and C. J. Arntzen, eds, Elsevier, Amsterdam, Netherlands.

Bais, H. P., R. Vepachedu, S. Gilroy, R. M. Callaway and J. M. Vivanco, 2003. 'Allelopathy and exotic plant invasion: From molecules and genes to species interactions'. Science, 301 (5638):1377–1380.

Bartoli, C. G., F. Gomez, G. Gergoff, J. J. Guiamét and S. Puntarulo, 2005. 'Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions'. Journal of Experimental Botany, 56 (415):1269–1276.

Begcy, K., E. D. Mariano, L. Mattiello, A. V. Nunes, P. Mazzafera, I. G. Maia and M. Menossi, 2011. 'An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants'. PLoS ONE, 6 (8).

Bereiter-Hahn, J. and M. Vöth, 1994. 'Dynamics of mitochondria in living cells: Shape changes, dislocations, fusion, and fission of mitochondria'. Microscopy Research and Technique, 27 (3):198–219.

Bhattacharjee, S, 2005. 'Reactive oxygen species and oxidative burst: Roles in stress, senescence and signal transduction in plants'. Current Science, 89 (7):1113–1121.

Bleazard, W., J. M. McCaffery, E. J. King, S. Bale, A. Mozdy, Q. Tieu, J. Nunnari and J. M. Shaw, 1999. 'The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast'. Nature Cell Biology, 1 (5):298–304.

Borecký, J., F. T. S. Nogueira, K. A. P. De Oliveira, I. G. Maia, A. E. Vercesi and P. Arruda, 2006. 'The plant energy-dissipating mitochondrial systems: Depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots'. Journal of Experimental Botany, 57 (4):849–864.

Brandalise, M., I. G. Maia, J. Borecký, A. E. Vercesi and P. Arruda, 2003. 'Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress'. Journal of Bioenergetics and Biomembranes, 35 (3):203–209.

Braun, H. P. and E. Zabaleta, 2007. 'Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants'. Physiologia Plantarum, 129 (1):114–122.

Cecchini, G, 2003. 'Function and structure of complex II of the respiratory chain'. Annual Review of Biochemistry, 72 (1):77–109.

Chen, H., A. Chomyn and D. C. Chan, 2005. 'Disruption of fusion results in mitochondrial heterogeneity and dysfunction'. Journal of Biological Chemistry, 280 (28):26185–26192.

Chen, H., S. A. Detmer, A. J. Ewald, E. E. Griffin, S. E. Fraser and D. C. Chan, 2003. 'Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development'. The Journal of Cell Biology, 160 (2):189–200.

Chen, X., Y. Wang, J. Li, A. Jiang, Y. Cheng and W. Zhang, 2009. 'Mitochondrial proteome during salt stress-induced programmed cell death in rice'. Plant Physiology and Biochemistry, 47 (5):407–415.

Chool Boo, Y. and J. Jung, 1999. 'Water deficit-induced oxidative stress and antioxidative defenses in rice plants'. Journal of Plant Physiology, 155 (2):255–261.

Christ, G. H., G. M. Bonanno, R. Alkinson, S. Rubin, K. Ohtsu, Y. Ito, H. Saika, M. Nakazono, N. Tsutsumi and A. Hirai, 2002. 'ABA-independent expression of rice alternative oxidase genes under environmental stresses'. Plant Biotechnology, 19 (3):187–190.

Considine, M. J., R. C. Holtzapffel, D. A. Day, J. Whelan and A. H. Millar, 2002. 'Molecular distinction between alternative oxidase from monocots and dicots'. Plant Physiology, 129 (3): 949-953.

Csordás, G., A. P. Thomas and G. Hajnóczky, 1999. 'Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria'. EMBO Journal, 18 (1): 96–108.

Cvetkovska, M. and G. C. Vanlerberghe, 2012. 'Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide'. New Phytologist, 195 (1): 32–39.

Dalton, T. P., H. G. Shertzer and A. Puga, 1999. 'Regulation of gene expression by reactive oxygen'. Annual Review of Pharmacology and Toxicology, 39 (1): 67–101.

Del Pozo, O. and E. Lam, 1998. 'Caspases and programmed cell death in the hypersensitive response of plants to pathogens'. Current Biology, 8 (20): 1129–1132.

Dojcinovic, D., J. Krosting, A. J. Harris, D. J. Wagner and D. M. Rhoads, 2005. 'Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression'. Plant Molecular Biology, 58 (2): 159–175.

Dudkina, N. V, J. Heinemeyer, S. Sunderhaus, E. J. Boekema and H.-P. Braun, 2006. 'Respiratory chain supercomplexes in the plant mitochondrial membrane'. Trends in Plant Science, 11 (5): 232–240.

Echtay, K. S, 2007. 'Mitochondrial uncoupling proteins-What is their physiological role?'. Free Radical Biology and Medicine, 43 (10): 1351–1371.

Echtay, K. S., D. Roussel, J. St-Pierre, M. B. Jekabsons, S. Cadenas, J. A. Stuart, J. A. Harper, S. J. Roebuck, A. Morrison, S. Pickering and J. C. Clapham, 2002. 'Superoxide activates mitochondrial uncoupling proteins'. Nature, 415 (6867): 96–99.

Eubel, H, 2003. 'New insights into the respiratory chain of plant mitochondria. supercomplexes and a unique composition of complex II'. Plant Physiology, 133 (1): 274–286.

Fernie, A. R., F. Carrari and L. J. Sweetlove, 2004. 'Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport'. Current Opinion in Plant Biology, 7 (3): 254–261.

Filippou, P., C. Antoniou and V. Fotopoulos, 2011. 'Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants'. Plant Signaling & Behavior, 6 (2): 270–277.

Finkel, T, 2011. 'Signal transduction by reactive oxygen species'. The Journal of Cell Biology, 194 (1): 7–15.

Foyer, C. H, 2005. 'Redox Homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses'. The Plant Cell Online, 17 (7): 1866–1875.

Foyer, C. H., H. Lopez-Delgado, J. F. Dat and I. M. Scott, 1997. 'Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling'. Physiologia Plantarum, 100 (2): 241–254.

Fujita, M., Y. Fujita, Y. Noutoshi, F. Takahashi, Y. Narusaka, K. Yamaguchi-Shinozaki and K. Shinozaki, 2006. 'Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks'. Current Opinion in Plant Biology, 9 (4): 436–442.

Garmier, M., A. J. Carroll, E. Delannoy, C. Vallet, D. A. Day, I. D. Small and A. H. Millar, 2008. 'Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis'. Plant Physiology, 148 (3): 1324–1341.

Geisler, D. A., C. Papke, T. Obata, A. Nunes-Nesi, A. Matthes, K. Schneitz, E. Maximova, W. L. Araujo, A. R. Fernie and S. Persson, 2012. 'Downregulation of the  δ-subunit reduces mitochondrial atp synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis'. The Plant Cell, 24 (7): 2792–2811.

Giraud, E., L. H. M. Ho, R. Clifton, A. Carroll, G. Estavillo, Y.-F. Tan, K. A. Howell, A. Ivanova, B. J. Pogson, A. H. Millar and J. Whelan, 2008. 'The absence of alternative oxidase1a in Arabidopsis results in acute sensitivity to combined light and drought stress'. Plant Physiology, 147 (2): 595–610.

Giraud, E., O. Van Aken, L. H. M. Ho and J. Whelan, 2009. 'The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of alternative oxidase1a'. Plant Physiology, 150 (3): 1286–1296.

Green, D. R. and J. C. Reed, 1998. 'Mitochondria and apoptosis'. Science, 281 (5381): 1309–1312.

Guzy, R. D., B. Hoyos, E. Robin, H. Chen, L. Liu, K. D. Mansfield, M. C. Simon, U. Hammerling and P. T. Schumacker, 2005. 'Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing'. Cell Metabolism, 1 (6): 401–408.

Hales, K. G. and M. T. Fuller, 1997. 'Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase'. Cell, 90 (1) :121–129.

Huang, S., N. L. Taylor, R. Narsai, H. Eubel, J. Whelan and A. H. Millar, 2008. 'Experimental analysis of the rice mitochondrial proteome, its biogenesis, and heterogeneity'. Plant Physiology, 149 (2): 719–734.

Islam, M. S. and S. Takagi, 2010. 'Co-localization of mitochondria with chloroplasts is a light-dependent reversible response'. Plant Signaling & Behavior, 5 (2): 146–147.

Ito, J., N. L. Taylor, I. Castleden, W. Weckwerth, A. H. Millar and J. L. Heazlewood, 2009. 'A survey of the Arabidopsis thaliana mitochondrial phosphoproteome'. Proteomics, 9 (17): 4229–4240.

James, D. I., P. A. Parone, Y. Mattenberger and J.-C. Martinou, 2003. 'hFis1, a novel component of the mammalian mitochondrial fission machinery'. Journal of Biological Chemistry, 278 (38): 36373–36379.

Jevzek, P., A. D. T. Costa and A. E. Vercesi, 1996. 'Evidence for anion-translocating plant uncoupling mitochondrial protein in potato mitochondria'. Journal of Biological Chemistry, 271 (51): 32743–32748.

Karray-Bouraoui, N., F. Harbaoui, M. Rabhi, I. Jallali, R. Ksouri, H. Attia, N. Msilini and M. Lachaâl, 2011. 'Different antioxidant responses to salt stress in two different provenances of Carthamus tinctorius L. Acta Physiologiae Plantarum, 33 (4): 1435–1444.

Kornfeld, A., O. K. Atkin, K. L. Griffin, T. W. Horton, D. Yakir and M. H. Turnbull, 2013. 'Modulation of respiratory metabolism in response to nutrient changes along a soil chronosequence'. Plant, Cell and Environment, 36 (6): 1120–1134.

Kreps, J. A, 2002. 'Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress'. Plant Physiology, 130 (4): 2129–2141.

Kunji, E. R. S, 2004. 'The role and structure of mitochondrial carriers'. FEBS Letters, 564 (3): 239–244.

Lam, E., N. Kato and M. Lawton, 2001. 'Programmed cell death, mitochondria and the plant hypersensitive response'. Nature, 411 (6839): 848–853.

Lambers, H, 1982. 'Cyanid-resistant respiration: A non-phosphorylating electron transport pathway acting as an energy overflow'. Physiologia Plantarum, 55 (4): 478–485.

Lang, B. F., G. Burger, C. J. O’kelly, R. Cedergren, G. B. Golding, C. Lemieux, D. Sankoff, M. Turmel and M. W. Gray, 1997. 'An ancestral mitochondrial DNA resembling a eubacterial genome in miniature'. Nature, 387 (6632): 493–497.

Lee, C. P., H. Eubel, N. O’Toole and A. H. Millar, 2008. Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism'. Molecular & Cellular Proteomics, 7 (7): 1297–1316.

Li, C. R., D. D. Liang, J. Li, Y. B. Duan, H. Li, Y. C. Yang, R. Y. Qin, L. Li, P. C. Wei and J. B. Yang, 2013. 'Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice alternative oxidase 1 genes'. Plant, Cell and Environment, 36 (4): 775–788.

Lodish, H., D. Baltimore, A. Berk, S. Zipursky, P. Matsudaira and J. Darnell, 1995. Molecular Cell Biology, 3rd ed. Scientific American Books, New York.

Logan, D. C, 2010. 'Mitochondrial fusion, division and positioning in plants: Figure 1'. Biochemical Society Transactions, 38 (3): 789–795.

Logan, D. C. and C. J. Leaver, 2000. 'Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells'. Journal of Experimental Botany, 51 (346): 865–871.

Lombardi, L., N. Ceccarelli, P. Picciarelli and R. Lorenzi, 2007. 'Caspase-like proteases involvement in programmed cell death of Phaseolus coccineus suspensor'. Plant Science, 172 (3): 573–578.

Mannella, C. A, 2006. 'Structure and dynamics of the mitochondrial inner membrane cristae'. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1763 (5-6): 542–548.

Martí, M. C., I. Florez-Sarasa, D. Camejo, M. Ribas-Carbó, J. J. Lázaro, F. Sevilla and A. Jiménez, 2011. 'Response of mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to salinity in pea (Pisum sativum L.) leaves'. Journal of Experimental Botany, 62 (11): 3863–3874.

Maxwell, D. P., Y. Wang and L. McIntosh, 1999. 'The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells'. Proceedings of The National Academy of Sciences of The United States of America, 96 (14): 8271–8276.

Meyer, E. H., N. L. Taylor and A. H. Millar, 2008. 'Resolving and identifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis'. The Journal of Proteome Research, 7 (2): 786–794.

Mishra, P., K. Bhoomika and R. S. Dubey, 2013. 'Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings'. Protoplasma, 250 (1): 3–19.

Mittler, R., S. Vanderauwera, M. Gollery and F. Van Breusegem, 2004. 'Reactive oxygen gene network of plants'. Trends in Plant Science, 9 (10): 490–498.

Møller, I. M, 2001. 'Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species'. Annual Review of Plant Physiology and Plant Molecular Biology, 52: 561–591.

Moore, A. L. and J. N. Siedow, 1991. 'The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria'. BBA - Bioenergetics, 1059 (2): 121–140.

Ordog, S. H., V. J. Higgins and G. C. Vanlerberghe, 2002. 'Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response'. Plant Physiology, 129 (4): 1858–1865.

Pan, Y., E. A. Schroeder, A. Ocampo, A. Barrientos and G. S. Shadel, 2011. 'Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling'. Cell Metabolism, 13 (6): 668–678.

Parsons, H. L., J. Y. Yip and G. C. Vanlerberghe, 1999. 'Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase'. Plant Physiology, 121 (4): 1309–1320.

Pastore, D., D. Trono, M. N. Laus, N. Di Fonzo and Z. Flagella, 2007. 'Possible plant mitochondria involvement in cell adaptation to drought stress: a case study: durum wheat mitochondria'. Journal of Experimental Botany, 58 (2): 195–210.

Patten, D. a, V. N. Lafleur, G. a Robitaille, D. a Chan, A. J. Giaccia and D. E. Richard, 2010. 'Hypoxia-inducible factor-1 activation in nonhypoxic conditions: the essential role of mitochondrial-derived reactive oxygen species'. Molecular Biology of the Cell, 21 (18): 3247–3257.

Picault, N., M. Hodges, L. Palmieri and F. Palmieri, 2004. 'The growing family of mitochondrial carriers in Arabidopsis'. Trends in Plant Science, 9 (3): 138–146.

Pinto, M. de, F. Tommasi, L. De Gara, R. Singal and S. R. Grimes, 2002. 'Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species'. Plant Physiology, 130: 698–708.

Polidoros, A. N., P. V. Mylona and B. Arnholdt-Schmitt, 2009. 'Aox gene structure, transcript variation and expression in plants'. Physiologia Plantarum, 137 (4): 342–353.

Puntarulo, S., R. a Sánchez and  a Boveris, 1988. 'Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination'. Plant Physiology, 86 (2): 626–630.

Rasmusson, A. G., K. L. Soole and T. E. Elthon, 2004. Alternative NAD(P)H dehydrogenases of plant mitochondria'. Annual Review of Plant Biology, 55 (1): 23–39.

Rasmusson, A. G., D. A. Geisler and I. M. Moller, 2008. 'The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria'. Mitochondrion, 8 (1): 47–60.

Rasmusson, A. G., A. R. Fernie and J. T. Van Dongen, 2009. 'Alternative oxidase: A defence against metabolic fluctuations? '. Physiologia Plantarum, 137 (4): 371–382.

Reape, T. J. and P. F. McCabe, 2008. 'Apoptotic-like programmed cell death in plants'. New Phytologist, 180 (1): 13–26.

Reape, T. J. and P. F. McCabe, 2010. 'Apoptotic-like regulation of programmed cell death in plants'. Apoptosis, 15 (3): 249–256.

Rhoads, D. M, 2011. Plant mitochondrial retrograde regulation; Pp. 411–437. In Plant Mitochondria. Springer.

Rhoads, D. M. and C. C. Subbaiah, 2007. 'Mitochondrial retrograde regulation in plants'. Mitochondrion, 7 (3):177–194.

Rhoads, D. M., A. L. Umbach, C. C. Subbaiah and J. N. Siedow, 2006. 'Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling'. Plant Physiology, 141 (2): 357–366.

Ribas-carbo, M., N. L. Taylor, L. Giles, S. Busquets, P. M. Finnegan, D. A. Day, J. A. Berry, J. Flexas, H. Lambers, U. De, I. Balears and U. De Barcelona, 2005. 'Effects of water stress on respiration in soybean leaves'. Plant Physiology, 139: 466–473.

Ribas-Carbo, M., J. A. Berry, D. Yakir, L. Giles, S. A. Robinson, A. M. Lennon and J. N. Siedow, 1995. 'Electron partitioning between the cytochrome and alternative pathways in plant mitochondria'. Plant Physiology, 109 (3): 829–837.

Rizzuto, R., P. Bernardi and T. Pozzan, 2000. 'Mitochondria as all-round players of the calcium game'. The Journal of Physiology, 529 (1): 37–47.

Robson, C. A. and G. C. Vanlerberghe, 2002. 'Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria dependent and independent pathways of programmed cell death'. Plant Physiology, 129 (4): 1908–1920.

Sairam, R. K., P. S. Deshmukh and D. C. Saxena, 1998. 'Role of antioxidant systems in wheat genotypes tolerance to water stress'. Biologia Plantarum, 41 (3): 387–394.

Sanjuán-Pla, A., A. M. Cervera, N. Apostolova, R. Garcia-Bou, V. M. Víctor, M. P. Murphy and K. J. McCreath, 2005. 'A targeted antioxidant reveals the importance of mitochondrial reactive oxygen species in the hypoxic signaling of HIF-1α'. FEBS Letters, 579 (12): 2669–2674.

Seki, M., M. Narusaka, J. Ishida, T. Nanjo, M. Fujita, Y. Oono, A. Kamiya, M. Nakajima, A. Enju, T. Sakurai, M. Satou, K. Akiyama, T. Taji, K. Yamaguchi-Shinozaki, P. Carninci, J. Kawai, Y. Hayashizaki and K. Shinozaki, 2002. 'Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray'. Plant Journal, 31 (3): 279–292.

Sharma, P. and R. S. Dubey, 2005. 'Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings'. Plant Growth Regulation, 46 (3): 209–221.

Sheahan, M. B., D. W. McCurdy and R. J. Rose, 2005. 'Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion'. The Plant Journal, 44 (5): 744–755.

Sjöstrand, F. S, 1953. 'Electron microscopy of mitochondria and cytoplasmic double membranes: Ultra-structure of rod-shaped mitochondria'. Nature, 171 (4340): 30–31.

Smirnova, E., L. Griparic, D.-L. Shurland and A. M. Van Der Bliek, 2001. 'Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells'. Molecular Biology of the Cell, 12 (8): 2245–2256.

Smith, R. A. and M. J. Ord, 1983. 'Mitochondrial form and function relationships in vivo: Their potential in toxicology and pathology'. International Review of Cytology, 83 (C): 63–134.

Stone, J. M., J. E. Heard, T. Asai and F. M. Ausubel, 2000. 'Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants'. The Plant Cell, 12 (10): 1811–22.

St-Pierre, J., S. Drori, M. Uldry, J. M. Silvaggi, J. Rhee, S. Jäger, C. Handschin, K. Zheng, J. Lin, W. Yang, D. K. Simon, R. Bachoo and B. M. Spiegelman, 2006. 'Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators'. Cell, 127 (2): 397–408.

Sweetlove, L. J. and C. H. Foyer, 2004. Roles for reactive oxygen species and antioxidants in plant mitochondria; Pp. 307–320. In Plant mitochondria: from genome to function. Springer.

Sweetlove, L. J., A. Lytovchenko, M. Morgan, A. Nunes-Nesi, N. L. Taylor, C. J. Baxter, I. Eickmeier and A. R. Fernie, 2006. 'Mitochondrial uncoupling protein is required for efficient photosynthesis'. Proceedings of the National Academy of Sciences, 103 (51): 19587–19592.

Thirkettle-Watts, D., T. C. McCabe, R. Clifton, C. Moore, P. M. Finnegan, D. A. Day and J. Whelan, 2003. 'Analysis of the alternative oxidase promoters from soybean'. Plant Physiology, 133 (3): 1158–1169.

Tronconi, M. A., H. Fahnenstich, M. C. Gerrard Weehler, C. S. Andreo, U.-I. Flugge, M. F. Drincovich and V. G. Maurino, 2008. 'Arabidopsis NAD-malic enzyme functions as a homodimer and heterodimer and has a major impact on nocturnal metabolism. Plant Physiology, 146 (4): 1540–1552.

Umbach, A. L., J. Zarkovic, J. Yu, M. E. Ruckle, L. McIntosh, J. J. Hock, S. Bingham, S. J. White, R. M. George, C. C. Subbaiah and D. M.Rhoads, 2012. 'Comparison of intact Arabidopsis thaliana leaf transcript profiles during treatment with inhibitors of mitochondrial electron transport and TCA cycle'. PLoS One, 7 (9): e44339.

Unseld, M., J. R. Marienfeld, P. Brandt and A. Brennicke, 1997. 'The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides'. Nature Genetics, 15 (1): 57–61.

Van Aken, O., E. Giraud, R. Clifton and J. Whelan, 2009a. 'Alternative oxidase: A target and regulator of stress responses'. Physiologia Plantarum, 137 (4): 354–361.

Van Aken, O., B. Zhang, C. Carrie, V. Uggalla, E. Paynter, E. Giraud and J. Whelan, 2009b. 'Defining the mitochondrial stress response in Arabidopsis thaliana'. Molecular Plant, 2 (6): 1310–1324.

Vanlerberghe, G. C., C. A. Robson and J. Y. H. Yip, 2002. 'Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death'. Plant Physiology, 129 (4): 1829–1842.

Vassileva, V., L. Simova-Stoilova, K. Demirevska and U. Feller, 2009. 'Variety-specific response of wheat (Triticum aestivum L.) leaf mitochondria to drought stress'. Journal of Plant Research, 122 (4): 445–454.

Wang, H., X. Liang, J. Huang, D. Zhang, H. Lu, Z. Liu and Y. Bi, 2010. 'Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses'. Plant and Cell Physiology, 51 (10): 1754–1765.

Watanabe, C. K., T. Hachiya, I. Terashima and K. Noguchi, 2008. '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 defence systems in Arabidopsis thaliana leaves'. Plant, Cell and Environment, 31 (8): 1190–1202.

Watanabe, C. K., T. Hachiya, K. Takahara, M. Kawai-Yamada, H. Uchimiya, Y. Uesono, I. Terashima and K. Noguchi, 2010. 'Effects of AOX1a deficiency on plant growth, gene expression of respiratory components and metabolic profile under low-nitrogen stress in Arabidopsis thaliana'. Plant and Cell Physiology, 51 (5): 810–822.

Westermann, B, 2010. 'Mitochondrial fusion and fission in cell life and death'. Nature Reviews Molecular Cell Biology, 11 (12): 872–884.

Whelan, J.,  a H. Millar and D. a Day, 1996. 'The alternative oxidase is encoded in a multigene family in soybean'. Planta, 198: 197–201.

Zarkovic, J., S. L. Anderson and D. M. Rhoads, 2005. 'A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis'. Plant Molecular Biology, 57 (6): 871–888.

Zhang, D. W., F. Xu, Z. W. Zhang, Y. E. Chen, J. B. Du, S. D. Jia, S. Yuan and H. H. Lin, 2010. 'Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings'. Plant, Cell and Environment, 33 (12): 2121–2131.

Zhu, Y., J. Lu, J. Wang, F. Chen, F. Leng and H. Li, 2011. 'Regulation of thermogenesis in plants: the interaction of alternative oxidase and plant uncoupling mitochondrial protein. Journal of Integrative Plant Biology, 53 (1): 7–13.

Zsigmond, L., Á. Szepesi, I. Tari, G. Rigó, A. Király and L. Szabados, 2012. 'Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis'. Plant Science, 182 (1): 87–93.