Abstract
Mitochondrial respiration provides energy necessary to drive the cellular metabolism in all living organisms. From ubiquinone mitochondrial respiratory electron transport chain (ETC) of plants, many fungi and protozoans branch into cyanide-sensitive and cyanide-insensitive pathways. The first one named cytochrome pathway (CP) used cytochrome c oxidase (COX) as terminal oxidase while the second named alternative pathway (AP) utilises an alternative oxidase (AOX) as terminal oxidase. COX reduces O2 to H2O and couples to H+-gradient generation used to make ATP. AOX reduces O2 upon oxidation of ubiquinol (UQH2) without coupling to ATP production. Despite its role as energy-dissipating pathway, AP also plays a key role in coordinated responses of cells to both abiotic and biotic stresses. In this context, when effectiveness of CP becomes limited by stress condition, AP allows a stress-dependent flexibility of respiratory ETC leading to an enhanced fitness of stressed plants. Residual respiration (Rresp), insensitive to cyanide and salicylhydroxamic acid (SHAM), not mediated either by CP or AP, also occurs in living plants. Although nature of this unique respiration is unknown, some new evidences seem to suggest that it plays an important role in abiotic stress responses. Thus, it is becoming clear that both AP, through the AOX activity, and Rresp constitute key components of orchestrated mitochondrial events, occurring in plants exposed to unfavourable environmental conditions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abas L, Bogoyevitch MA, Guppy M (2000) Mitochondrial ATP production is necessary for activation of the extracellular-signal regulated kinases during ischaemia/reperfusion in rat myocyte-derived H9c2 cells. Biochem J 349:119–126
Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci U S A 100:5968–5973
Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29:380–395
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York
Albrecht G, Mustroph A (2003) Localization of sucrose synthase in wheat roots: increased in situ activity of sucrose synthase correlates with cell wall thickening by cellulose deposition under hypoxia. Planta 217:252–260
Albury MS, Affourtit C, Crichton PG, Moore AL (2002) Structure of the plant alternative oxidase. Site-directed mutagenesis provides new information on the active site and membrane topology. J Biol Chem 277:1190–1194
Albury MS, Elliott C, Moore AL (2009) Towards a structural elucidation of the alternative oxidase in plants. Physiol Plant 137:316–327
Albury MS, Elliott C, Moore AL (2010) Ubiquinol-binding site in the alternative oxidase: mutagenesis reveals features important for substrate binding and inhibition. Biochim Biophys Acta 1797:1933–1939
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390
Almeida AM, Jarmuszkiewicz W, Khomsi H, Arruda P, Vercesi AE, Sluse FE (1999) Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiol 119:1323–1329
Almeida AM, Navet R, Jarmuszkiewicz W, Vercesi AE, Sluse-Goffart CM, Sluse FE (2002) The energy-conserving and energy-dissipating processes in mitochondria isolated from wild type and nonripening tomato fruits during development on the plant. J Bioenerg Biomembr 34:487–498
Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 27:1436–1448
Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–2513
Andersson ME, Nordlund P (1999) A revised model of the active site of alternative oxidase. FEBS Lett 449:17–22
Angelini R, Federico R (1989) Histochemical evidence of polyamine oxidation and hydrogen peroxide generation in the cell wall. J Plant Physiol 135:212–217
Araújo WL, Nunes-Nesi A, Nikoloski Z, Sweetlove LJ, Fernie AR (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ 35:1–21
Araújo WL, Nunes-Nesi A, Fernie AR (2013) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynth Res. doi:10.1007/s11120-013-9807-4
Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci U S A 101:7805–7808
Armstrong AF, Badger MR, Day DA, Barthet MM, Smith PMC, Millar AH, Whelan J, Atkin OK (2008) Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant Cell Environ 31:1156–1169
Arnholdt-Schmitt B, Costa JH, Fernandes de Melo D (2006) AOX—a functional marker for efficient cell reprogramming under stress? Trends Plant Sci 11:282–287
Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597
Atkin OK, Zhang Q, Wiskich JT (2002) Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox poise of the quinone pool. Plant Physiol 128:212–222
Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659
Backert S, Nielsen BL, Börner T (1997) The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci 2:477–483
Bae H, Herman E, Bailey B, Bae HJ, Sicher R (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol Plant 125:114–126
Baena-González EB (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3:300–313
Bako SP (2006) Effects of plant age, ascorbate and kinetin applications on integrity of the photosynthetic pigment complex in maize (Zea mays L.) plants grown under heat stress. Asian J Plant Sci 5:357–362
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744
Bartoli CG, Gomez F, Gergoff G, Guiamét JJ, Puntarulo S (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J Exp Bot 56:1269–1276
Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, Bellance N, Delage JP, Casteilla L, Letellier T, Rossignol R (2006) Physiological diversity of mitochondrial oxidative phosphorylation. Am J Physiol Cell Physiol 291:C1172–C1182
Bernards MA, Summerhurst DK, Razem FA (2004) Oxidases, peroxidases and hydrogen peroxide: the suberin connection. Phytochem Rev 3:113–126
Berthold DA, Andersson ME, Nordlund P (2000) New insight into the structure and function of the alternative oxidase. Biochim Biophys Acta 1460:241–254
Berthold DA, Voevodskaya N, Stenmark P, Gräslund A, Nordlund P (2002) EPR studies of the mitochondrial alternative oxidase—evidence for a diiron carboxylate center. J Biol Chem 277:43608–43614
Bhate RH, Ramasarma T (2009) Evidence for H2O2 as the product of reduction of oxygen by alternative oxidase in mitochondria from potato tubers. Arch Biochem Biophys 486:165–169
Bianchi C, Genova ML, Parenti Castelli G, Lenaz G (2004) The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem 279:36562–36569
Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462
Boekema EJ, Braun HP (2007) Supramolecular structure of the mitochondrial oxidative phosphorylation system. J Biol Chem 282:1–4
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546
Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780
Borecký J, Vercesi AE (2005) Plant uncoupling mitochondrial protein and alternative oxidase: energy metabolism and stress. Biosci Rep 35:271–286
Braun HP, Schmitz UK (1995) Are the ‘core’ proteins of the mitochondrial bc1 complex evolutionary relics of a processing protease? Trends Biochem Sci 20:171–175
Bullerwell CE, Gray MW (2004) Evolution of the mitochondrial genome: protist connections to animals, fungi and plants. Curr Opin Microbiol 7:528–534
Carrie C, Murcha MW, Giraud E, Ng S, Zhang MF, Narsai R, Whelan J (2012) How do plants make mitochondria? Planta. doi:10.1007/s00425-012-1762-3
Castandet B, Araya A (2011) RNA editing in plant organelles. Why make it easy? Biochemistry (Mosc) 76:924–931
Castro-Guerrero NA, Rodríguez-Zavala JS, Marín-Hernández A, Rodríguez-Enríquez S, Moreno-Sánchez R (2008) Enhanced alternative oxidase and antioxidant enzymes under Cd2+ stress in Euglena. J Bioenerg Biomembr 40:227–235
Chance B, Williams GR (1955) A method for the localization of sites for oxidative phosphorylation. Nature 176:250–254
Chang S, Wang Y, Lu J, Gai J, Li J, Chu P, Guan R, Zhao T (2013) The mitochondrial genome of soybean reveals complex genome structures and gene evolution at intercellular and phylogenetic levels. PLoS One 8:e56502. doi:10.1371/journal.pone.0056502
Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877
Clifton R, Millar AH, Whelan J (2006) 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 1757:730–741
Collins TJ, Berridge MJ, Lipp P, Bootman MD (2002) Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J 21:1616–1627
Cooper CE (2003) Competitive, reversible, physiological? Inhibition of mitochondrial cytochrome oxidase by nitric oxide. IUBMB Life 55:591–597
Corpas FJ, Fernández-Ocaña A, Carreras A, Valderrama R, Luque F, Esteban FJ, Rodríguez-Serrano M, Chaki M, Pedrajas JR, Sandalio ML, del Río LA, Barroso JB (2006) The expression of different superoxide dismutase forms is cell-type dependent in olive (Olea europaea L.) leaves. Plant Cell Physiol 47:984–994
Cortassa S, O’Rourke B, Winslow RL, Aon MA (2009) Control and regulation of integrated mitochondrial function in metabolic and transport networks. Int J Mol Sci 10:1500–1513
Costa JH, Fernandes de Melo D, Gouveia Z, Cardoso HG, Peixe A, Arnholdt-Schmitt B (2009) The alternative oxidase family of Vitis vinifera reveals an attractive model to study the importance of genomic design. Physiol Plant 137:553–565
Coueé I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
Crichton PG, Albury MS, Affourtit C, Moore AL (2010) Mutagenesis of the plant alternative oxidase reveals features important for oxygen binding and catalysis. Biochim Biophys Acta 1797:732–737
Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39
Cvetkovska M, Vanlerberghe GC (2013) Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ 36:721–732
Daems WT, Wisse E (1966) Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria. J Ultrastruct Res 16:123–140
Dai H, Lo YS, Litvinchuk A, Wang YT, Jane WN, Hsiao LJ, Chiang KS (2005) Structural and functional characterizations of mung bean mitochondrial nucleoids. Nucleic Acids Res 33:4725–4739
Dassa EP, Dufour E, Gonçalves S, Jacobs HT, Rustin P (2009) The alternative oxidase, a tool for compensating cytochrome c oxidase deficiency in human cells. Physiol Plant 137:427–434
Devi R, Munjral N, Gupta AK, Kaur N (2007) Cadmium induced changes in carbohydrate status and enzymes of carbohydrate metabolism, glycolysis and pentose phosphate pathway in pea. Environ Exp Bot 61:167–174
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097
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
Dzeja PP, Terzic A (1998) Phosphotransfer reactions in the regulation of ATP-sensitive K+ channels. FASEB J 12:523–529
Dzeja PP, Holmuhamedov EL, Ozcan C, Pucar D, Jahangir A, Terzic A (2001) Mitochondria gateway for cytoprotection. Circ Res 89:744–746
Edreva A, Velikova V, Tsonev T, Dagnon S, Gürel A, Aktaş L, Gesheva E (2008) Stress-protective role of secondary metabolites: diversity of functions and mechanisms. Gen Appl Plant Physiol 34:67–78
Elhafez D, Murcha MW, Clifton R, Soole KL, Day DA, Whelan J (2006) Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol 47:43–54
Elthon TE, McIntosh L (1987) Identification of the alternative terminal oxidase of higher plant mitochondria. Proc Natl Acad Sci U S A 84:8399–8403
Elthon TE, Stewart CR, Mc Coy CA, Bonner WD Jr (1986) Alternative respiratory path capacity in plant mitochondria effect of growth temperature, the electrochemical gradient, and assay pH. Plant Physiol 80:378–383
Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol 89:1311–1317
Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630
Essmann J, Bones P, Weis E, Scharte J (2008) Leaf carbohydrate metabolism during defense. Intracellular sucrose-cleaving enzymes do not compensate repression of cell wall invertase. Plant Signal Behav 3:885–887
Eubel H, Jänsch 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
Fauron C, Allen J, Clifton S, Newton K (2004) Plant mitochondrial genomes. In: Daniell H, Chase C (eds) Molecular biology and biotechnology of plant organelles. Chloroplasts and mitochondria. Springer, Dordrecht, pp 151–177
Fecht-Christoffers MM, Führs H, Braun HP, Horst WJ (2006) The role of hydrogen peroxide-producing and hydrogen peroxide-consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiol 140:1451–1463
Fernández-Ayala DJM, Sanz A, Vartiainen S, Kemppainen K, Babusiak M, Mustalahti E, Costa R, Tuomela T, Zeviani M, Chung J, O’Dell KMC, Rustin P, Jacobs HT (2009) Expression of the Ciona intestinalis alternative oxidase (AOX) in Drosophila complements defects in mitochondrial oxidative phosphorylation. Cell Metab 9:449–460
Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254–261
Fiorani F, Umbach AL, Siedow JN (2005) The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1 a transgenic plants. Plant Physiol 139:1795–1805
Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127:343–352
Fresneau C, Ghashghaie J, Cornic G (2007) Drought effect on nitrate reductase and sucrose-phosphate synthase activities in wheat (Triticum durum L.): role of leaf internal CO2. J Exp Bot 58:2983–2992
Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319–324
Friedrich T, Steinmüller K, Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 479:1–5
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442
Fung RWM, Wang CY, Smith DL, Gross KC, Tian MS (2004) MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Sci 166:711–719
Gandin A, Lapointe L, Dizengremel P (2009) The alternative respiratory pathway allows sink to cope with changes in carbon availability in the sink-limited plant Erythronium americanum. J Exp Bot 60:4235–4248
Garesse R, Vallejo CG (2001) Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene 263:1–16
Garlid KD, Jabůrek M, Ježek P, Vařecha M (2000) How do uncoupling proteins uncouple? Biochim Biophys Acta 1459:383–389
Gas E, Flores-Pérez U, Sauret-Güeto S, Rodríguez-Concepción M (2009) Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21:18–23
Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101
Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256
Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577
Geigenberger P, Reimholz R, Deiting U, Sonnewald U, Stitt M (1999) Decreased expression of sucrose phosphate synthase strongly inhibits the water stress-induced synthesis of sucrose in growing potato tubers. Plant J 19:119–129
Geisler DA, Broselid C, Hederstedt L, Rasmusson AG (2007) Ca2+-binding and Ca2+-independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J Biol Chem 282:28455–28464
Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Gunnar W, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot JP (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci U S A 101:14545–14550
Gilbert GA, Wilson C, Madore MA (1997) Root-zone salinity alters raffinose oligosaccharide metabolism and transport in Coleus. Plant Physiol 115:1267–1276
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
González-Meler MA, Giles L, Thomas RB, Siedow JN (2001) Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply. Plant Cell Environ 24:205–215
Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci 4:44. doi:10.3389/fpls.2013.00044
Greishaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53
Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776
Gupta KJ, Zabalza A, van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2010) On the origins of nitric oxide. Trends Plant Sci 16:160–168
Gupta KJ, Igamberdiev AU, Mur LA (2012a) NO and ROS homeostasis in mitochondria: a central role for alternative oxidase. New Phytol 195:1–3
Gupta KJ, Shah JK, Brotman Y, Jahnke K, Willmitzer L, Kaiser WM, Bauwe H, Igamberdiev AU (2012b) 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 63:1773–1784
Gustafsson AB, Gottlieb RA (2008) Heart mitochondria: gates of life and death. Cardiovasc Res 77:334–343
Guy RD, Vanlerberghe GC (2005) Partitioning of respiratory electrons in the dark in leaves of transgenic tobacco with modified levels of alternative oxidase. Physiol Plant 125:171–180
Hackenbrock CR (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 30:269–297
Hackenbrock CR, Chazotte B, Gupte SS (1986) The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr 18:331–368
Hakkaart GA, Dassa EP, Jacobs HT, Rustin P (2006) Allotopic expression of a mitochondrial alternative oxidase confers cyanide resistance to human cell respiration. EMBO Rep 7:341–345
Halestrap AP, Brosnan JT (2008) From metabolic cycles to compartmentation: another first for Krebs. Biochemist 30:24–28
Hanqing F, Kun S, Mingquan L, Hongyu L, Xin L, Yan L, Yifeng W (2010) The expression, function and regulation of mitochondrial alternative oxidase under biotic stresses. Mol Plant Pathol 11:429–440
Hansford RG (1994) Role of calcium in respiratory control. Med Sci Sports Exerc 26:44–51
Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015–1069
Havelund JF, Thelen JJ, Møller IM (2013) Biochemistry, proteomics, and phosphoproteomics of plant mitochondria from non-photosynthetic cells. Front Plant Sci 4:51. doi:10.3389/fpls.2013.00051
Hilal M, Castagnaro A, Moreno H, Massa EM (1997) Specific localization of the respiratory alternative oxidase in meristematic and xylematic tissues from developing soybean roots and hypocotyls. Plant Physiol 115:1499–1503
Hilal M, Zenoff AM, Ponessa G, Moreno H, Massa EM (1998) Saline stress alters the temporal patterns of xylem differentiation and alternative oxidase expression in developing soybean roots. Plant Physiol 117:695–701
Ho SL, Chao YC, Tong WF, Yu SM (2001) Sugar coordinately and differentially regulates growth- and stress-related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol 125:877–890
Ho LHM, Giraud E, Lister R, Thirkettle-Watts D, Low J, Clifton R, Howell KA, Carrie C, Donald T, Whelan J (2007) Characterization of the regulatory and expression context of an alternative oxidase gene provides insights into cyanide-insensitive respiration during growth and development. Plant Physiol 143:1519–1533
Ho LHM, Giraud E, Uggalla V, Lister R, Glen A, Thirkettle-Watts D, Van Aken O, Whelan J (2008) Identification of regulatory pathways controlling gene expression of stress responsive mitochondrial components in Arabidopsis. Plant Physiol 147:1858–1873
Hoefnagel MHN, Rich PR, Zhang Q, Wiskich JT (1997) Substrates kinetics of the plant mitochondrial alternative oxidase and the effects of pyruvate. Plant Physiol 115:1145–1153
Hourton-Cabassa C, Matos AR, Zachowski A, Moreau F (2004) The plant uncoupling protein homologues: a new family of energy-dissipating proteins in plant mitochondria. Plant Physiol Biochem 42:283–290
Howell KA, Millar AH, Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with promitochondrial structures rich in components of the protein import apparatus. Plant Mol Biol 60:201–223
Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181
Hurry VM, Malmberg G, Gardestrom P, Öquist G (1994) Effects of a short-term shift to low temperature and of long-term cold hardening on photosynthesis and ribulose-l,5-bisphosphate carboxylase/oxygenase and sucrose phosphate synthase activity in leaves of winter rye (Secale cereale L.). Plant Physiol 106:983–990
Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34
Jacoby RP, Li L, Huang S, Lee CP, Millar AH, Taylor NL (2012) Mitochondrial composition, function and stress response in plants. J Integr Plant Biol 54:887–906
Jarmuszkiewicz W, Wagner AM, Wagner MJ, Hryniewiecka L (1997) Immunological identification of the alternative oxidase of Acanthamoeba castellanii mitochondria. FEBS Lett 411:110–114
Jarmuszkiewicz W, Almeida AM, Vercesi AE, Sluse FE, Sluse-Goffart CM (2000) Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzohydroxamic acid-resistant state 3 respiration in tomato fruit mitochondria. J Biol Chem 275:13315–13320
Jarmuszkiewicz W, Hryniewiecka L, Sluse FE (2002) The effect of pH on the alternative oxidase activity in isolated Acanthamoeba castellanii mitochondria. J Bioenerg Biomembr 34:221–226
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 Cell Physiol 292:689–697
Johnson BN, Charan RA, LaVoie MJ (2012) Recognizing the cooperative and independent mitochondrial functions of Parkin and PINK1. Cell Cycle 11:2775–2776
Johnson-Flanagan AM, Owens JN (1985) Peroxidase activity in relation to suberization and respiration in white spruce (Picea glauca [Moench] Voss) seedling roots. Plant Physiol 79:103–107
Jørgensen K, Rasmussen AV, Morant M, Nielsen AH, Bjarnholt N, Zagrobelny M, Bak S, Møller BL (2005) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr Opin Plant Biol 8:280–291
Justine Y, Yip H, Vanlerberghe GC (2001) 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 112:327–333
Karlsson M, Melzer M, Prokhorenko I, Johansson T, Wingsle G (2005) Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans. J Exp Bot 56:2085–2093
Keurentjes JJB, Sulpice R, Gibon Y, Steinhauser MC, Fu J, Koornneef M, Stitt M, Vreugdenhil D (2008) Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biol 9:R129
Kleczkowski LA, Geisler M, Ciereszko I, Johansson H (2004) UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol 134:912–918
Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246
Koch KE, Wu V, Xu J (1996) Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing. J Exp Bot 47:1179–1185
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14
Lee CP, Eubel H, Millar AH (2010) Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis. Mol Cell Proteomics 9:2125–2139
Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL (2001) Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 33:1065–1089
Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice ALTERNATIVE OXIDASE 1 genes. Plant Cell Environ 36:775–788
Liao YW, Shi K, Fu LJ, Zhang S, Li X, Dong DK, Jiang YP, Zhou YH, Xia XJ, Liang WS, Yu JQ (2012) The reduction of reactive oxygen species formation by mitochondrial alternative respiration in tomato basal defense against TMV infection. Planta 235:225–238
Lima-Júnior A, Fernandes de Melo D, Costa JH, Orellano EG, Jolivet Y, Jarmuszkiewicz W, Sluse F, Dizengremel P, Silva Lima M (2000) Effect of pH on CN-resistant respiratory activity and regulation on Vigna unguiculata mitochondria. Plant Physiol Biochem 38:765–771
Liu YJ, Norberg FE, Szilagyi A, De Paepe R, Akerlund HE, Rasmusson AG (2008) The mitochondrial external NADPH dehydrogenase modulates the leaf NADPH/NADP+ ratio in transgenic Nicotiana sylvestris. Plant Cell Physiol 49:251–263
Livingston DP III, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66:2007–2023
Logan DC (2006) The mitochondrial compartment. J Exp Bot 57:1225–1243
Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672
Logan DC, Scott I, Tobin AK (2003) The genetic control of plant mitochondrial morphology and dynamics. Plant J 36:500–509
Lonsdale DM, Brears T, Hodge TP, Melville SE, Rottmann WH (1988) The plant mitochondrial genome: homologous recombination as a mechanism for generating heterogeneity. Philos Trans R Soc Lond B 319:149–163
Magalhães PJ, Andreu AL, Schon SA (1998) Evidence for the presence of 5S rRNA in mammalian mitochondria. Mol Biol Cell 9:2375–2382
Mannella CA (1992) The ‘ins’ and ‘outs’ of mitochondrial membrane channels. Trends Biochem Sci 17:315–320
Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762:140–147
Maréchal A, Kido Y, Kita K, Moore AL, Rich PR (2009) Identification of three redox states of recombinant Trypanosoma brucei alternative oxidase by FTIR spectroscopy and electrochemistry. J Biol Chem 284:31827–31833
Marques I, Dencher NA, Videira A, Krause F (2007) Supramolecular organization of the respiratory chain in Neurospora crassa mitochondria. Eukaryot Cell 6:2391–2405
Martí MC, Florez-Sarasa I, Camejo D, Ribas-Carbó M, Lázaro JJ, Sevilla F, Jiménez A (2011) Response of mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to salinity in pea (Pisum sativum L.) leaves. J Exp Bot 62:3863–3874
Matos AR, Mendes AT, Scotti-Campos P, Arrabaça JD (2009) Study of the effects of salicylic acid on soybean mitochondrial lipids and respiratory properties using the alternative oxidase as a stress-reporter protein. Physiol Plant 137:485–497
Matus-Ortega MG, Salmerón-Santiago KG, Flores-Herrera O, Guerra-Sánchez G, Martínez F, Rendón JL, Pardo JP (2011) The alternative NADH dehydrogenase is present in mitochondria of some animal taxa. Comp Biochem Physiol D 6:256–263
Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276
McDonald AE, Vanlerberghe GC (2004) Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 56:333–341
McDonald AE, Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Physiol D 1:357–364
McDonald AE, Vanlerberghe GC, Staples JF (2009) Alternative oxidase in animals: unique characteristics and taxonomic distribution. J Exp Biol 212:2627–2634
Meeuse BJD (1975) Thermogenic respiration in aroids. Annu Rev Plant Physiol 26:117–126
Menz RI, Day DA (1996) Identification and characterization of an inducible NAD(P)H dehydrogenase from red beetroot mitochondria. Plant Physiol 112:607–613
Menze MA, Boswell L, Toner M, Hand SC (2009) Occurrence of mitochondria-targeted late embryogenesis abundant (LEA) gene in animals increases organelle resistance to water stress. J Biol Chem 284:10714–10719
Mhadhbi H, Fotopoulos V, Mylona PV, Jebara M, Aouani ME, Polidoros AN (2013) Alternative oxidase Aox1 gene expression in roots of Medicago truncatula is a genotype-specific component of salt stress tolerance. J Plant Physiol 170:111–114
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
Millar AH, Atkin OK, Menz RI, Henry B, Farquhar G, Day DA (1998) Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiol 117:1083–1093
Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104
Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5:2–15
Millenaar FF, Benschop JJ, Wagner AM, Lambers H (1998) The role of the alternative oxidase in stabilizing the in vivo reduction state of the ubiquinone pool and the activation state of the alternative oxidase. Plant Physiol 118:599–607
Millenaar FF, Gonzalez-Meler MA, Siedow JN, Wagner AM, Lambers H (2002) Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots. J Exp Bot 53:1081–1088
Mishra P, Dubey RS (2008) Effect of aluminium on metabolism of starch and sugars in growing rice seedlings. Acta Physiol Plant 30:265–275
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591
Møller IM, Berczi A, van der Plas LHW, Lambers H (1988) Measurement of the activity and capacity of the alternative pathway in intact tissues: identification and problems and possible solutions. Physiol Plant 73:642–649
Møller IM, Rasmusson AG, Siedow JN, Vanlerberghe GC (2010) The product of the alternative oxidase is still H2O. Arch Biochem Biophys 495:93–94
Moore AL, Siedow JN (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059:121–140
Moore AL, Umbach AL, Siedow JN (1995) Structure-function relationships of the alternative oxidase of plant mitochondria: a model of the active site. J Bioenerg Biomembr 27:367–377
Moore AL, Albury MS, Crichton PG, Affourtit C (2002) Function of the alternative oxidase: is it still a scavenger? Trends Plant Sci 7:478–481
Mower JP, Sloan DB, Alverson AJ (2012) Plant mitochondrial genome diversity: the genomics revolution. In: Wendel JH (ed) Plant genome diversity volume 1: plant genomes, their residents, and their evolutionary dynamics. Springer, New York, pp 123–144
Navet R, Douette P, Puttine-Marique F, Sluse-Goffart CM, Jarmuszkiewicz W, Sluse FE (2005) Regulation of uncoupling protein activity in phosphorylating potato tuber mitochondria. FEBS Lett 579:4437–4442
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379
Nelson DL, Cox MM (2008) Lehninger principles of biochemistry, 5th edn. W.H. Freeman & Co, New York
Newcomb W (1990) Mitochondrial structure. In: Dennis DT, Turpin DH (eds) Plant physiology, biochemistry and molecular biology. Longman Scientific & Technical, England, pp 103–105
Nunes-Nesi A, Sulpice R, Gibon Y, Fernie AR (2008) The enigmatic contribution of mitochondrial function in photosynthesis. J Exp Bot 59:1675–1684
O’Donnell VB, Smith GCM, Jones OTG (1994) Involvement of phenyl radicals in iodonium compound inhibition of flavoenzymes. Mol Pharmacol 46:778–785
Osorio S, Vallarino JG, Szecowka M, Ufaz S, Tzin V, Angelovici R, Galili G, Fernie AR (2013) Alteration of the interconversion of pyruvate and malate in the plastid or cytosol of ripening tomato fruit invokes diverse consequences on sugar but similar effects on cellular organic acid, metabolism, and transitory starch accumulation. Plant Physiol 161:628–643
Padmasree K, Padmavathi L, Raghavendra AS (2002) Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Crit Rev Biochem Mol Biol 37:71–119
Palade G (1952) The fine structure of mitochondria. Anat Rec 114:427–451
Panda SK, Sahoo L, Katsuhara M, Matsumoto H (2013) Overexpression of alternative oxidase gene confers aluminum tolerance by altering the respiratory capacity and the response to oxidative stress in tobacco cells. Mol Biotechnol. doi:10.1007/s12033-012-9595-7
Pasqualini S, Paolocci F, Borgogni A, Morettini R, Ederli L (2007) The overexpression of an alternative oxidase gene triggers ozone sensitivity in tobacco plants. Plant Cell Environ 30:1545–1556
Pastore D, Trono D, Laus MN, Di Fonzo N, Passarella S (2001) Alternative oxidase in durum wheat mitochondria. Activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant Cell Physiol 42:1373–1382
Peckmann K, von Willert DJ, Martin CE, Herppich WB (2012) Mitochondrial espiration in ME-CAM, PEPCK-CAM, and C3 succulents: comparative operation of the cytochrome, alternative, and rotenone-resistant pathways. J Exp Bot 63:2909−2919
Perkins GA, Frey TG (2000) Recent structural insight into mitochondria gained by microscopy. Micron 31:97–111
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
Pizarro LC, Bisigato AJ (2010) Allocation of biomass and photoassimilates in juvenile plants of six Patagonian species in response to five water supply regimes. Ann Bot 106:297–307
Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246
Poulton JE (1990) Cyanogenesis in plants. Plant Physiol 94:401–405
Prado C (2012) Respuestas bioquímicas y anatomofisiólogicas de Salvinia minima al cromo. Su potencial uso como agente fitorremediador de ambientes acuáticos. PhD thesis, Universidad Nacional de Tucumán, Tucumán
Prado C, Rodríguez-Montelongo L, González JA, Pagano EA, Hilal M, Prado FE (2010) Uptake of chromium by Salvinia minima: effect on plant growth, leaf respiration and carbohydrate metabolism. J Hazard Mater 177:546–553
Prado C, Podazza G, Pagano E, Prado FE, Rosa M (2011) Heavy metals—functional and metabolic interactions between carbohydrates and secondary metabolites in plants. A review. In: Brar SK (ed) Hazardous materials: types, risks and control. Nova, New York, pp 1–52
Prado C, Rosa M, Pagano E, Prado FE (2013) Metabolic interconnectivity among alternative respiration, residual respiration, carbohydrates and phenolics in leaves of Salvinia minima exposed to Cr(VI). Environ Exp Bot 87:32–38
Proels RK, Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J Exp Bot 60:1555–1567
Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–553
Rakhmankulova ZF, Fedyaev VV, Podashevka OA, Usmanov IY (2003) Alternative respiration pathways and secondary metabolism in plants with different adaptive strategies under mineral deficiency. Russ J Plant Physiol 50:206–212
Ralph J, Bunzel M, Marita MJ, Hatfield RD, Lu F, Kim H, Schatz PF, Grabber JH, Steinhart H (2004) Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochem Rev 3:79–96
Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731
Ramírez-Aguilar SJ, Keuthe M, Rocha M, Fedyaev VV, Kramp K, Gupta KJ, Rasmusson AG, Schulze WX, van Dongen JT (2011) The composition of plant mitochondrial supercomplexes changes with oxygen availability. J Biol Chem 286:43045–43053
Ranathunge K, Schreiber L, Franke R (2011) Suberin research in the genomics era—new interest for an old polymer. Plant Sci 180:399–413
Rasmusson AG, Møller IM (2011) Mitochondrial electron transport and plant stress. In: Kempken F (ed) Plant mitochondria: advances in plant biology volume, 1st edn. Springer, New York, pp 357–381
Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 55:23–39
Rasmusson AG, Geisler DA, Møller IM (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8:47–60
Rasmusson AG, Fernie AR, van Dongen JT (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiol Plant 137:371–382
Rathinasabapathi B (2000) Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Ann Bot 86:709–716
Rhoads DM, Umbach AL, Sweet CR, Lennon AM, Rauch GS, Siedow JN (1998) 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 273:30750–30756
Ribas-Carbó M, Lennon AM, Robinson SA, Giles L, Berry JA, Siedow JN (1997) The regulation of electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiol 113:903–911
Ribas-Carbó M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J (2005) Effects of water stress on respiration in soybean leaves. Plant Physiol 139:466–473
Ribas-Carbó M, Giles L, Flexas J, Briggs W, Berry JA (2008) Phytochrome-driven changes in respiratory electron transport partitioning in soybean (Glycine max. L.) cotyledons. Plant Biol 10:281–287
Rigoulet M, Aguilaniu H, Avéret N, Bunoust O, Camougrand N, Grandier-Vazeille X, Larsson C, Pahlman IL, Manon S, Gustafsson L (2004) Organization and regulation of the cytosolic NADH metabolism in the yeast Saccharomyces cerevisiae. Mol Cell Biochem 256–257:73–81
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
Roberts TH, Fredlund KM, Møller IM (1995) Direct evidence for the presence of two external NAD(P)H dehydrogenases coupled to the electron transport chain in plant mitochondria. FEBS Lett 373:307–309
Roberts CW, Roberts F, Henriquez FL, Akiyoshi D, Samuel BU, Richards TA, Mihous W, Kyle D, McIntosh L, Hill GC, Chaudhuri M, Tzipori S, McLeod R (2004) Evidence for mitochondrial-derived alternative oxidase in the apicomplexan parasite Cryptosporidium parvum: a potential anti-microbial agent target. Int J Parasitol 34:297–308
Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol 129:1908–1920
Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613
Ros Barceló A (1997) Lignification in plant cell walls. Int Rev Cytol 176:87–132
Ros Barceló A, Pomar F, Lópes-Serrano M, Martinez P, Pendreño MA (2002) Developmental regulation of the H2O2-producing system and basic peroxidase isoenzyme in the Zinnia elegans lignifying xylem. Plant Physiol Biochem 40:325–332
Rosa M, Hilal M, González JA, Prado FE (2009a) Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiol Biochem 47:300–307
Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009b) Soluble sugars: metabolism, sensing, and abiotic stress. A complex network in the life of plants. Plant Signal Behav 4:388–393
Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955
Runswick MJ, Fearnley IM, Skehel JM, Walker JE (1991) Presence of an acyl carrier protein in NADH-ubiquinone oxidoreductase from bovine heart mitochondria. FEBS Lett 286:121–124
Rustin P, Jacobs HT (2009) Respiratory chain alternative enzymes as tools to better understand and counteract respiratory chain deficiencies in human cells and animals. Physiol Plant 137:362–370
Santos Macedo E, Sircar D, Cardoso HG, Peixe A, Arnholdt-Schmitt B (2012) Involvement of alternative oxidase (AOX) in adventitious rooting of Olea europaea L. microshoots is linked to adaptive phenylpropanoid and lignin metabolism. Plant Cell Rep 31:1581–1590
Sanz A, Fernández-Ayala DJM, Stefanatos RK, Jacobs HT (2010) Mitochondrial ROS production correlates with, but does not directly regulate lifespan in drosophila. Aging 2:220–223
Schäfer E, Seelert H, Reifschneider NH, Krause F, Dencher NA, Vonck J (2006) Architecture of active mammalian respiratory chain supercomplexes. J Biol Chem 281:15370–15375
Schägger H, de Coo R, Bauer MF, Hofmann S, Godinot C, Brandt U (2004) Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J Biol Chem 279:36349–36353
Searle SY, Turnbull MH (2011) Seasonal variation of leaf respiration and the alternative pathway in field-grown Populus×canadensis. Physiol Plant 141:332–342
Seigler DS (1998) Plant secondary metabolism. Kluwer Academic, Boston
Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264
Shen WY, Wei YD, Dauk M, Tan YF, Taylor DC, Selvaraj G, Zou JT (2006) Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18:422–441
Shi K, Fu LJ, Dong DK, Zhou YH, Yu JQ (2008) Decreased energy synthesis is partially compensated by a switch to sucrose synthase pathway of sucrose degradation in restricted root of tomato plants. Plant Physiol Biochem 46:1040–1044
Shugaeva NA, Vyskrebentseva EI, Orekhova SO, Shugaev AG (2007) Effect of water deficit on respiration of conducting bundles in leaf petioles of sugar beet. Russ J Plant Physiol 54:329–335
Siedow JN, Umbach AL (2000) The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta 1459:432–439
Siedow JN, Umbach AL, Moore AL (1995) The active site of the cyanide resistant oxidase from plant mitochondria contains a binuclear iron center. FEBS Lett 362:10–14
Sieger SM, Kristensen BK, Robson CA, Amirsadeghi W, Eng SE, Abdel-Mesih A, Møller IM, Vanlerberghe GC (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56:1499–1515
Sjostrand FS (1953) Electron microscopy of mitochondria and cytoplasmic double membranes. Nature 171:30–31
Skórzyńska-Polit E, Drążkiewicz M, Wianowska D, Maksymiec W, Dawidowicz AL, Tukiendorf A (2004) The influence of heavy metal stress on the level of some flavonols in the primary leaves of Phaseolus coccineus. Acta Physiol Plant 26:247–254
Skutnik M, Rychter AM (2009) Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. J Plant Physiol 166:926–937
Sluse FE, Almeida AM, Jarmuszkiewicz W, Vercesi AE (1998) Free fatty acids regulate the uncoupling protein and alternative oxidase activities in plant mitochondria. FEBS Lett 433:237–240
Smith CA, Melino VJ, Sweetman C, Soole KL (2009) Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiol Plant 137:459–472
Smith CA, Barthet M, Melino V, Smith P, Day D, Soole K (2011) 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 52:1222–1237
Solomos T, Laties GG (1975) The mechanism of ethylene and cyanide action in triggering the rise in respiration in potato tubers. Plant Physiol 55:73–78
Stenmark P, Nordlund P (2003) A prokaryotic alternative oxidase present in the bacterium Novosphingobium aromaticivorans. FEBS Lett 552:189–192
Stobrawa K, Lorenc-Plucińska G (2007) Changes in carbohydrate metabolism in fine roots of the native European black poplar (Populus nigra L.) in a heavy-metal-polluted environment. Sci Total Environ 373:157–165
Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407
Subbaiah CC, Palaniappan A, Duncan K, Rhoads DM, Huber SC, Sachs MM (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 281:15625–15635
Sugie A, Naydenov N, Mizuno N, Nakamura C, Takumi S (2006) 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 81:349–354
Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272:603–615
Sunderhaus S, Klodmann J, Lenz C, Braun HP (2010) Supramolecular structure of the OXPHOS system in highly thermogenic tissue of Arum maculatum. Plant Physiol Biochem 48:265–272
Suzuki T, Nihei C, Yabu Y, Hashimoto T, Suzuki M, Yoshida A, Nagai K, Hosokawa T, Minagawa N, Suzuki S, Kita K, Ohta N (2004) Molecular cloning and characterization of Trypanosoma vivax alternative oxidase (AOX) gene, a target of the trypanocide ascofuranone. Parasitol Int 53:235–245
Sweetlove LJ, Fait A, Nunes-Nesi A, Williams T, Fernie AR (2007) The mitochondrion: an integration point of cellular metabolism and signalling. Crit Rev Plant Sci 26:17–43
Szarka A, Horemans N, Passarella S, Tarcsay Á, Örsi F, Salgó A, Bánhegyi G (2008) Demonstration of an intramitochondrial invertase activity and the corresponding sugar transporters of the inner mitochondrial membrane in Jerusalem artichoke (Helianthus tuberosus L.) tubers. Planta 228:765–775
Szarka A, Bánhegyi G, Asard H (2013) The inter-relationship of ascorbate transport, metabolism and mitochondrial, plastidic respiration. Antioxid Redox Signal. doi:10.1089/ars.2012.5059
Takahama U, Oniki T, Hirota S (2001) Phenolic compounds of brown scales of onion bulbs produce hydrogen peroxide by autooxidation. J Plant Res 114:395–402
Talianova M, Janousek B (2011) What can we learn from tobacco and other solanaceae about horizontal DNA transfer? Am J Bot 98:1231–1242
Tang W, Fei Y, Page M (2012) Biological significance of RNA editing in cells. Mol Biotechnol 52:91–100
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
Tischner R, Planchet E, Kaiser WM (2004) Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett 576:151–155
Uchida K (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 42:318–343
Umbach AL, Siedow JN (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol 103:845–854
Umbach AL, Wiskich JT, Siedow JN (1994) Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Lett 348:181–184
Umbach AL, González-Meler MA, Sweet CR, Siedow JN (2002) Activation of the plant mitochondrial alternative oxidase: insights from site-directed mutagenesis. Biochim Biophys Acta 1554:118–128
Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139:1806–1820
Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61
Van Aken O, Giraud E, Clifton R, Whelan J (2009a) Alternative oxidase: a target and regulator of stress responses. Physiol Plant 137:354–361
Van Aken O, Zhang B, Carrie C, Uggalla V, Paynter E, Giraud E, Whelan J (2009b) Defining the mitochondrial stress response in Arabidopsis thaliana. Mol Plant 2:1310–1324
van Dongen JT, Gupta KJ, Ramírez-Aguilar SJ, Araújo WL, Nunes-Nesi A, Fernie AR (2011) Regulation of respiration in plants: a role for alternative metabolic pathways. J Plant Physiol 168:1434–1443
Vander Heiden MG, Chandel NS, Li XX, Schumacker PT, Colombini M, Thompson CB (2000) Outer membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci U S A 97:4666–4671
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905
Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847
Vanlerberghe GC, McIntosh L (1997) Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48:703–734
Vanlerberghe GC, Robson CA, Yip JYH (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol 129:1829–1842
Vanlerberghe GC, Cvetkovska M, Wang J (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plant 137:392–406
Vargas WA, Pontis HG, Salerno GL (2008) New insights on sucrose metabolism: evidence for an active A/N-Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 227:795–807
Vercesi AE, Borecký J, de Godoy MI, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 57:383–404
Vidal G, Ribas-Carbó M, Garmier M, Dubertret G, Rasmusson AG, Mathieu C, Foyer CH, De Paepe R (2007) Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signalling during elicitor-induced cell death in tobacco. Plant Cell 19:640–655
Wagner AM (1995) A role for active oxygen species as second messenger in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett 368:339–342
Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283:1482–1488
Wang J, Vanlerberghe GC (2013) A lack of mitochondrial alternative oxidase compromises capacity to recover from severe drought stress. Physiol Plant. doi:10.1111/ppl.12059
Wang D, Rousseau-Gueutin M, Timmis JN (2012a) Plastid sequences contribute to some plant mitochondrial genes. Mol Biol Evol 29:1707–1711
Wang H, Huang J, Liang X, Bi Y (2012b) Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus. Planta 235:53–67
Winkel BS (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19:31–67
Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiol 115:1405–1412
Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P, Tosa Y, Mayama S (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J 30:567–579
Yoshida K, Terashima I, Noguchi K (2006) Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant Cell Physiol 47:22–31
Yoshida K, Watanabe C, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49:592–603
Yoshida K, Watanabe CK, Terashima I, Noguchi K (2011) Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Environ 34:1890–1899
Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54:875–892. doi:10.1093/pcp/pct037
Yukioka H, Inagaki S, Tanaka R, Katoh K, Miki N, Mizutani A, Masuko M (1998) Transcriptional activation of the alternative oxidase gene of the fungus Magnaporthe grisea by a respiratory-inhibiting fungicide and hydrogen peroxide. Biochim Biophys Acta 1442:161–169
Zhang Y, Marcillat O, Giulivi C, Ernster L, Davies KJ (1990) The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265:16330–16336
Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng QW (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40. doi:10.1186/1471-2229-12-40
Zottini M, Mandolino G, Zannoni D (1993) Oxidation of external NAD(P)H by mitochondria from taproots and tissue cultures of sugar beet (Beta vulgaris). Plant Physiol 102:579–585
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
Zsigmond L, Rigó G, Szarka A, Székely G, Ötvös K, Darula Z, Medzihradszky KF, Koncz C, Koncz Z, Szabado L (2008) Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 146:1721–1737
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media New York
About this chapter
Cite this chapter
Chocobar-Ponce, S., Prado, C., González, R., Rosa, M., Prado, F.E. (2014). Mitochondrial Respiration: Involvement of the Alternative Respiratory Pathway and Residual Respiration in Abiotic Stress Responses. In: Ahmad, P., Wani, M. (eds) Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8591-9_12
Download citation
DOI: https://doi.org/10.1007/978-1-4614-8591-9_12
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-8590-2
Online ISBN: 978-1-4614-8591-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)