REVIEW: PART OF A SPECIAL ISSUE ON REACTIVE OXYGEN AND NITROGEN SPECIES Roles of mitochondrial energy dissipation systems in plant development and acclimation to stress

Background Plants are sessile organisms that have the ability to integrate external cues into metabolic and developmental signals. The cues initiate specific signal cascades that can enhance the tolerance of plants to stress, and these mechanisms are crucial to the survival and fitness of plants. The adaption of plants to stresses is a complex process that involves decoding stress inputs as energy-deficiency signals. The process functions through vast metabolic and/or transcriptional reprogramming to re-establish the cellular energy balance. Members of the mitochondrial energy dissipation pathway (MEDP), alternative oxidases (AOXs) and uncoupling proteins (UCPs), act as energy mediators and might play crucial roles in the adaption of plants to stresses. However, their roles in plant growth and development have been relatively less explored. Scope This review summarizes current knowledge about the role of members of the MEDP in plant development as well as recent advances in identifying molecular components that regulate the expression of AOXs and UCPs. Highlighted in particular is a comparative analysis of the expression, regulation and stress responses between AOXs and UCPs when plants are exposed to stresses, and a possible signal cross-talk that orchestrates the MEDP, reactive oxygen species (ROS), calcium signalling and hormone signalling. Conclusions The MEDP might act as a cellular energy/metabolic mediator that integrates ROS signalling, energy signalling and hormone signalling with plant development and stress accumulation. However, the regulation of MEDP members is complex and occurs at transcriptional, translational, post-translational and metabolic levels. How this regulation is linked to actual fluxes through the AOX/UCP in vivo remains elusive.

[1]  A. P. D. Candolle,et al.  Flore française, ou, Descriptions succinctes de toutes les plantes qui croissent naturellement en France : , 2018 .

[2]  J. V. van Dongen,et al.  Oxygen sensing and signaling. , 2015, Annual review of plant biology.

[3]  K. Ross,et al.  Thermogenesis-triggered seed dispersal in dwarf mistletoe , 2015, Nature Communications.

[4]  Juan Pablo Córdoba,et al.  Role of mitochondria during female gametophyte development and fertilization in A. thaliana. , 2014, Mitochondrion.

[5]  Nobuhiro Suzuki,et al.  A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. , 2014, Trends in plant science.

[6]  A. Millar,et al.  What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. , 2014, Plant, cell & environment.

[7]  J. Kangasjärvi,et al.  Specificity in ROS signaling and transcript signatures. , 2014, Antioxidants & redox signaling.

[8]  T. Nägele,et al.  The low energy signaling network , 2014, Front. Plant Sci..

[9]  Keshav Dahal,et al.  Knockdown of mitochondrial alternative oxidase induces the 'stress state' of signaling molecule pools in Nicotiana tabacum, with implications for stomatal function. , 2014, The New phytologist.

[10]  F. Van Breusegem,et al.  Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. , 2014, Molecular plant.

[11]  Simon R. Law,et al.  Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. , 2014, Molecular plant.

[12]  I. Maia,et al.  Overexpression of UCP1 in tobacco induces mitochondrial biogenesis and amplifies a broad stress response , 2014, BMC Plant Biology.

[13]  Simon R. Law,et al.  A Functional Antagonistic Relationship between Auxin and Mitochondrial Retrograde Signaling Regulates Alternative Oxidase1a Expression in Arabidopsis1[W][OPEN] , 2014, Plant Physiology.

[14]  A. Cousins,et al.  Disruption of the mitochondrial alternative oxidase (AOX) and uncoupling protein (UCP) alters rates of foliar nitrate and carbon assimilation in Arabidopsis thaliana , 2014, Journal of experimental botany.

[15]  Jonathan D. G. Jones,et al.  Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. , 2014, Molecular cell.

[16]  T. Romeis,et al.  Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. , 2014, The Plant journal : for cell and molecular biology.

[17]  T. Zhu,et al.  The roles of autophagy in development and stress responses in Arabidopsis thaliana , 2014, Apoptosis.

[18]  S. Smeekens,et al.  Sugar signals and the control of plant growth and development. , 2014, Journal of experimental botany.

[19]  G. Parisi,et al.  UCP2 transports C4 metabolites out of mitochondria, regulating glucose and glutamine oxidation , 2014, Proceedings of the National Academy of Sciences.

[20]  Américo Rodrigues,et al.  ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in Arabidopsis[C][W] , 2013, Plant Cell.

[21]  Simon R. Law,et al.  A Membrane-Bound NAC Transcription Factor, ANAC017, Mediates Mitochondrial Retrograde Signaling in Arabidopsis[W][OPEN] , 2013, Plant Cell.

[22]  N. Suzuki,et al.  Temporal-Spatial Interaction between Reactive Oxygen Species and Abscisic Acid Regulates Rapid Systemic Acclimation in Plants[W][OPEN] , 2013, Plant Cell.

[23]  Sandra Pelletier,et al.  A Regulatory Network-Based Approach Dissects Late Maturation Processes Related to the Acquisition of Desiccation Tolerance and Longevity of Medicago truncatula Seeds1[C][W][OPEN] , 2013, Plant Physiology.

[24]  I. Grosse,et al.  Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination1[W][OPEN] , 2013, Plant Physiology.

[25]  S. Bonnet,et al.  Uncoupling Protein 2 Deficiency Mimics the Effects of Hypoxia and Endoplasmic Reticulum Stress on Mitochondria and Triggers Pseudohypoxic Pulmonary Vascular Remodeling and Pulmonary Hypertension , 2013, Circulation research.

[26]  Ana Confraria,et al.  miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis , 2013, Front. Plant Sci..

[27]  W. Schulze,et al.  Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation , 2013, Proceedings of the National Academy of Sciences.

[28]  A. Moore,et al.  Unraveling the heater: new insights into the structure of the alternative oxidase. , 2013, Annual review of plant biology.

[29]  V. Sundaresan,et al.  oiwa, a Female Gametophytic Mutant Impaired in a Mitochondrial Manganese-Superoxide Dismutase, Reveals Crucial Roles for Reactive Oxygen Species during Embryo Sac Development and Fertilization in Arabidopsis[C][W] , 2013, Plant Cell.

[30]  Yuhong Tang,et al.  Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. , 2013, The Plant journal : for cell and molecular biology.

[31]  A. Sali,et al.  Crystal structure of a eukaryotic phosphate transporter , 2013, Nature.

[32]  G. Vanlerberghe,et al.  Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants , 2013, International journal of molecular sciences.

[33]  Simon R. Law,et al.  AtWRKY40 and AtWRKY63 Modulate the Expression of Stress-Responsive Nuclear Genes Encoding Mitochondrial and Chloroplast Proteins1[W][OA] , 2013, Plant Physiology.

[34]  K. Mishiba,et al.  Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response , 2013, Proceedings of the National Academy of Sciences.

[35]  T. Honma,et al.  Structure of the trypanosome cyanide-insensitive alternative oxidase , 2013, Proceedings of the National Academy of Sciences.

[36]  A. Fernie,et al.  Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. , 2013, The Plant journal : for cell and molecular biology.

[37]  Kenji Hashimoto,et al.  The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. , 2013, Molecular plant.

[38]  H. Kaya,et al.  The CBL-interacting protein kinase CIPK26 is a novel interactor of Arabidopsis NADPH oxidase AtRbohF that negatively modulates its ROS-producing activity in a heterologous expression system. , 2013, Journal of biochemistry.

[39]  X. Xia,et al.  Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants , 2013, Planta.

[40]  Simon R. Law,et al.  Cyclin-dependent Kinase E1 (CDKE1) Provides a Cellular Switch in Plants between Growth and Stress Responses , 2012, The Journal of Biological Chemistry.

[41]  Frank Van Breusegem,et al.  AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis , 2012, Proceedings of the National Academy of Sciences.

[42]  T. Yagi,et al.  The structure of the yeast NADH dehydrogenase (Ndi1) reveals overlapping binding sites for water- and lipid-soluble substrates , 2012, Proceedings of the National Academy of Sciences.

[43]  Hong-hui Lin,et al.  The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene , 2012, Journal of experimental botany.

[44]  G. Vanlerberghe,et al.  Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. , 2012, The New phytologist.

[45]  G. Galili,et al.  Deciphering energy-associated gene networks operating in the response of Arabidopsis plants to stress and nutritional cues. , 2012, The Plant journal : for cell and molecular biology.

[46]  M. Taniguchi,et al.  Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. , 2012, Current opinion in plant biology.

[47]  M. Ohh,et al.  The updated biology of hypoxia‐inducible factor , 2012, The EMBO journal.

[48]  P. Finnegan,et al.  A GmAOX2b antisense gene compromises vegetative growth and seed production in soybean , 2012, Planta.

[49]  N. Suzuki,et al.  ROS and redox signalling in the response of plants to abiotic stress. , 2012, Plant, cell & environment.

[50]  Jianhua Zhu,et al.  Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. , 2012, Biochimica et biophysica acta.

[51]  L. Willmitzer,et al.  Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. , 2012, Journal of experimental botany.

[52]  Xiaofei Li,et al.  UCP2 Inhibits ROS-Mediated Apoptosis in A549 under Hypoxic Conditions , 2012, PloS one.

[53]  U. Sonnewald,et al.  The plastid outer envelope protein OEP16 affects metabolic fluxes during ABA-controlled seed development and germination , 2011, Journal of experimental botany.

[54]  N. Suzuki,et al.  Respiratory burst oxidases: the engines of ROS signaling. , 2011, Current opinion in plant biology.

[55]  Simon R. Law,et al.  In-Depth Temporal Transcriptome Profiling Reveals a Crucial Developmental Switch with Roles for RNA Processing and Organelle Metabolism That Are Essential for Germination in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[56]  Caleb M. Rounds,et al.  Pollen tube energetics: respiration, fermentation and the race to the ovule , 2011, AoB PLANTS.

[57]  S. Harrison,et al.  Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching , 2011, Nature.

[58]  G. Vanlerberghe,et al.  Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. , 2011, Physiologia plantarum.

[59]  K. Vandepoele,et al.  ROS signaling: the new wave? , 2011, Trends in plant science.

[60]  A. Bonner,et al.  Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions , 2011, Proceedings of the National Academy of Sciences.

[61]  A. Moore,et al.  Ubiquinol-binding site in the alternative oxidase: mutagenesis reveals features important for substrate binding and inhibition. , 2010, Biochimica et biophysica acta.

[62]  George W. Bassel,et al.  Germination—Still a mystery , 2010 .

[63]  Hong-hui Lin,et al.  Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. , 2010, Plant, cell & environment.

[64]  P. Benfey,et al.  Transcriptional Regulation of ROS Controls Transition from Proliferation to Differentiation in the Root , 2010, Cell.

[65]  Xiaolei Liang,et al.  Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. , 2010, Plant & cell physiology.

[66]  Xuhui Hong,et al.  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. , 2010, The Plant journal : for cell and molecular biology.

[67]  O. Lamotte,et al.  Cross-talk between ROS and calcium in regulation of nuclear activities. , 2010, Molecular plant.

[68]  F. Sluse,et al.  Mitochondrial uncoupling proteins in unicellular eukaryotes. , 2010, Biochimica et biophysica acta.

[69]  A. S. Raghavendra,et al.  Importance of AOX pathway in optimizing photosynthesis under high light stress: role of pyruvate and malate in activating AOX. , 2010, Physiologia plantarum.

[70]  Rouslan G. Efremov,et al.  The architecture of respiratory complex I , 2010, Nature.

[71]  S. Gilroy,et al.  ROS in plant development. , 2010, Physiologia plantarum.

[72]  Nigel G Halford,et al.  The interface between metabolic and stress signalling. , 2010, Annals of botany.

[73]  A. Fernie,et al.  The central regulation of plant physiology by adenylates. , 2010, Trends in plant science.

[74]  A. Mustroph,et al.  Cross-Kingdom Comparison of Transcriptomic Adjustments to Low-Oxygen Stress Highlights Conserved and Plant-Specific Responses1[W][OA] , 2010, Plant Physiology.

[75]  K. Okawa,et al.  Stomagen positively regulates stomatal density in Arabidopsis , 2010, Nature.

[76]  G. Vanlerberghe,et al.  Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? , 2009, Physiologia plantarum.

[77]  J. Dangl,et al.  The Plant NADPH Oxidase RBOHD Mediates Rapid Systemic Signaling in Response to Diverse Stimuli , 2009, Science Signaling.

[78]  Yuan Qin,et al.  Penetration of the Stigma and Style Elicits a Novel Transcriptome in Pollen Tubes, Pointing to Genes Critical for Growth in a Pistil , 2009, PLoS genetics.

[79]  Mónica Santos Mendoza,et al.  The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. , 2009, The Plant journal : for cell and molecular biology.

[80]  C. Pecqueur,et al.  UCP2, a metabolic sensor coupling glucose oxidation to mitochondrial metabolism? , 2009, IUBMB life.

[81]  M. Estelle,et al.  Recent advances and emerging trends in plant hormone signalling , 2009, Nature.

[82]  J. Whelan,et al.  The Transcription Factor ABI4 Is a Regulator of Mitochondrial Retrograde Expression of ALTERNATIVE OXIDASE1a1[C][W][OA] , 2009, Plant Physiology.

[83]  S. Robinson,et al.  Two Cys or Not Two Cys? That Is the Question; Alternative Oxidase in the Thermogenic Plant Sacred Lotus1[W][OA] , 2009, Plant Physiology.

[84]  H. El-Maarouf-Bouteau,et al.  The Mechanisms Involved in Seed Dormancy Alleviation by Hydrogen Cyanide Unravel the Role of Reactive Oxygen Species as Key Factors of Cellular Signaling during Germination[C][W] , 2009, Plant Physiology.

[85]  Björn Usadel,et al.  Mapping Metabolic and Transcript Temporal Switches during Germination in Rice Highlights Specific Transcription Factors and the Role of RNA Instability in the Germination Process1[W][OA] , 2008, Plant Physiology.

[86]  Charles J H Jang,et al.  Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[87]  Joost T. van Dongen,et al.  Decreased Expression of Cytosolic Pyruvate Kinase in Potato Tubers Leads to a Decline in Pyruvate Resulting in an in Vivo Repression of the Alternative Oxidase1[W][OA] , 2008, Plant Physiology.

[88]  Yi Wang,et al.  Transcriptome Analyses Show Changes in Gene Expression to Accompany Pollen Germination and Tube Growth in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[89]  E. Baena-González,et al.  Convergent energy and stress signaling. , 2008, Trends in plant science.

[90]  Tomas Hruz,et al.  Genevestigator transcriptome meta-analysis and biomarker search using rice and barley gene expression databases. , 2008, Molecular plant.

[91]  M. Sack,et al.  ATF-1 Is a Hypoxia-responsive Transcriptional Activator of Skeletal Muscle Mitochondrial-uncoupling Protein 3* , 2008, Journal of Biological Chemistry.

[92]  A. Millar,et al.  Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. , 2008, Plant, cell & environment.

[93]  K. Noguchi,et al.  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. , 2008, Plant, cell & environment.

[94]  Peter Widmayer,et al.  Genevestigator V3: A Reference Expression Database for the Meta-Analysis of Transcriptomes , 2008, Adv. Bioinformatics.

[95]  R. Lister,et al.  Identification of Regulatory Pathways Controlling Gene Expression of Stress-Responsive Mitochondrial Proteins in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[96]  H. El-Maarouf-Bouteau,et al.  Oxidative signaling in seed germination and dormancy , 2008, Plant signaling & behavior.

[97]  J. Kennis,et al.  Identification of a mechanism of photoprotective energy dissipation in higher plants , 2007, Nature.

[98]  Filip Rolland,et al.  A central integrator of transcription networks in plant stress and energy signalling , 2007, Nature.

[99]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[100]  K. Torii,et al.  The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. , 2007, Genes & development.

[101]  Jianhua Zhu,et al.  Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. , 2007, Current opinion in plant biology.

[102]  K. Noguchi,et al.  Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. , 2007, Plant & cell physiology.

[103]  H. Yoshioka,et al.  Calcium-Dependent Protein Kinases Regulate the Production of Reactive Oxygen Species by Potato NADPH Oxidase [W][OA] , 2007, The Plant Cell Online.

[104]  R. Lister,et al.  Characterization of the Regulatory and Expression Context of an Alternative Oxidase Gene Provides Insights into Cyanide-Insensitive Respiration during Growth and Development1[C][W][OA] , 2007, Plant Physiology.

[105]  Alisdair R Fernie,et al.  Mitochondrial uncoupling protein is required for efficient photosynthesis , 2006, Proceedings of the National Academy of Sciences.

[106]  Magnus Holm,et al.  Opposite Root Growth Phenotypes of hy5 versus hy5 hyh Mutants Correlate with Increased Constitutive Auxin Signaling , 2006, PLoS genetics.

[107]  David L. Smith,et al.  Characterization of alternative oxidase (AOX) gene expression in response to methyl salicylate and methyl jasmonate pre-treatment and low temperature in tomatoes. , 2006, Journal of plant physiology.

[108]  B. Grodzinski,et al.  Energy balance, organellar redox status, and acclimation to environmental stress , 2006 .

[109]  C. Wasternack,et al.  Interaction between Nitric Oxide and Ethylene in the Induction of Alternative Oxidase in Ozone-Treated Tobacco Plants1[W] , 2006, Plant Physiology.

[110]  W. Finch-Savage,et al.  Seed dormancy and the control of germination. , 2006, The New phytologist.

[111]  K. Shinozaki,et al.  Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. , 2006, Current opinion in plant biology.

[112]  A. Millar,et al.  Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. , 2006, Biochimica et biophysica acta.

[113]  L. Dolan,et al.  Control of Plant Development by Reactive Oxygen Species1 , 2006, Plant Physiology.

[114]  J. Schroeder,et al.  The Role of Reactive Oxygen Species in Hormonal Responses1 , 2006, Plant Physiology.

[115]  A. Vercesi,et al.  Plant uncoupling mitochondrial proteins. , 2006, Annual review of plant biology.

[116]  P. Castagnone-Sereno,et al.  Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. , 2006, The New phytologist.

[117]  Russell G. Jones,et al.  Hypoxia-induced energy stress regulates mRNA translation and cell growth. , 2006, Molecular cell.

[118]  J. Siedow,et al.  Regulation of plant alternative oxidase activity: a tale of two cysteines. , 2006, Biochimica et biophysica acta.

[119]  I. Couée,et al.  Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. , 2006, Journal of experimental botany.

[120]  D. Macherel,et al.  Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures1 , 2005, Plant Physiology.

[121]  F. Fiorani,et al.  The Alternative Oxidase of Plant Mitochondria Is Involved in the Acclimation of Shoot Growth at Low Temperature. A Study of Arabidopsis AOX1a Transgenic Plants1[W] , 2005, Plant Physiology.

[122]  A. Igamberdiev,et al.  The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. , 2005, Annals of botany.

[123]  A. Millar,et al.  Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. , 2005, Annals of botany.

[124]  M. Sogin,et al.  Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile , 2005, Journal of Experimental Biology.

[125]  Z. Rao,et al.  Crystal Structure of Mitochondrial Respiratory Membrane Protein Complex II , 2005, Cell.

[126]  E. Bergantino,et al.  Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo‐oxidation , 2005, EMBO reports.

[127]  I. Møller,et al.  The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. , 2005, Journal of experimental botany.

[128]  Yuji Kamiya,et al.  Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. , 2005, The Plant journal : for cell and molecular biology.

[129]  L. Sweetlove,et al.  Activation and Function of Mitochondrial Uncoupling Protein in Plants* , 2004, Journal of Biological Chemistry.

[130]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[131]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[132]  Winfriede Weschke,et al.  Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. , 2004, Journal of experimental botany.

[133]  R. Fung,et al.  MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.) , 2004 .

[134]  J. Hancock,et al.  ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. , 2003, Journal of experimental botany.

[135]  H. Rolletschek,et al.  Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. , 2003, The Plant journal : for cell and molecular biology.

[136]  A. Millar,et al.  A tomato alternative oxidase protein with altered regulatory properties. , 2003, Biochimica et biophysica acta.

[137]  T. Holdaway-Clarke,et al.  Control of pollen tube growth: role of ion gradients and fluxes. , 2003, The New phytologist.

[138]  J. Kangasjärvi,et al.  Reactive oxygen species and hormonal control of cell death. , 2003, Trends in plant science.

[139]  Mark G Tjoelker,et al.  Thermal acclimation and the dynamic response of plant respiration to temperature. , 2003, Trends in plant science.

[140]  P. Geigenberger,et al.  Response of plant metabolism to too little oxygen. , 2003, Current opinion in plant biology.

[141]  R. Mittler.  Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[142]  Mark Stitt,et al.  A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. , 2002, Current opinion in plant biology.

[143]  A. Hirai,et al.  Two uncoupling protein genes of rice (Oryza sativa L.): molecular study reveals the defects in the pre-mRNA processing for the heat-generating proteins of the subtropical cereal , 2002, Planta.

[144]  F. Sluse,et al.  Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects , 2002, FEBS letters.

[145]  J. Stuart,et al.  Superoxide activates mitochondrial uncoupling proteins , 2002, Nature.

[146]  D. Daley,et al.  The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. , 2001, Plant physiology.

[147]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[148]  Naohiro Kato,et al.  Programmed cell death, mitochondria and the plant hypersensitive response , 2001, Nature.

[149]  N. Smirnoff,et al.  BIOSYNTHESIS OF ASCORBIC ACID IN PLANTS: A Renaissance. , 2001, Annual review of plant physiology and plant molecular biology.

[150]  B. Miroux,et al.  Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production , 2000, Nature Genetics.

[151]  Andrew G. W. Leslie,et al.  The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution , 2000, Nature Structural Biology.

[152]  N. Tsutsumi,et al.  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 , 2000, FEBS letters.

[153]  D. Ricquier,et al.  The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. , 2000, The Biochemical journal.

[154]  M. Girvin,et al.  Structural changes linked to proton translocation by subunit c of the ATP synthase , 1999, Nature.

[155]  L. Mcintosh,et al.  The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[156]  P Nordlund,et al.  A revised model of the active site of alternative oxidase , 1999, FEBS letters.

[157]  Vercesi,et al.  Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein-sustained respiration during postharvest ripening of tomato fruit , 1999, Plant physiology.

[158]  T. A. Link,et al.  Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. , 1998, Science.

[159]  T. Tomizaki,et al.  Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. , 1998, Science.

[160]  G. Öquist,et al.  Energy balance and acclimation to light and cold , 1998 .

[161]  S. Naito,et al.  Characterization of the gene family for alternative oxidase from Arabidopsis thaliana , 1997, Plant Molecular Biology.

[162]  M. Ribas-Carbó,et al.  The Effects of Salicylic Acid and Tobacco Mosaic Virus Infection on the Alternative Oxidase of Tobacco , 1997, Plant physiology.

[163]  J. Riesmeier,et al.  A plant cold-induced uncoupling protein , 1997, Nature.

[164]  L. Mcintosh,et al.  ALTERNATIVE OXIDASE: From Gene to Function. , 1997, Annual review of plant physiology and plant molecular biology.

[165]  L. Tartaglia,et al.  Cloning and Characterization of an Uncoupling Protein Homolog: A Potential Molecular Mediator of Human Thermogenesis , 1997, Diabetes.

[166]  G. Vanlerberghe,et al.  Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria , 1996, Plant physiology.

[167]  R. N. Trelease,et al.  Ascorbate Peroxidase (A Prominent Membrane Protein in Oilseed Glyoxysomes) , 1996, Plant physiology.

[168]  C. Somerville,et al.  Direct tests of the role of membrane lipid composition in low-temperature-induced photoinhibition and chilling sensitivity in plants and cyanobacteria. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[169]  N. Murata,et al.  Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[170]  A. Moore,et al.  The active site of the cyanide‐resistant oxidase from plant mitochondria contains a binuclear iron center , 1995, FEBS letters.

[171]  J. Siedow,et al.  Covalent and Noncovalent Dimers of the Cyanide-Resistant Alternative Oxidase Protein in Higher Plant Mitochondria and Their Relationship to Enzyme Activity , 1993, Plant physiology.

[172]  A. Millar,et al.  Organic acid activation of the alterNatlve oxidase of plant mitochondria , 1993, FEBS letters.

[173]  Anuj Kumar,et al.  Arabidopsis alternative oxidase sustains Escherichia coli respiration. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[174]  C. Guy,et al.  Sucrose phosphate synthase and sucrose accumulation at low temperature. , 1992, Plant physiology.

[175]  M. Ehrenshaft,et al.  Respiration and mitochondrial biogenesis in germinating embryos of maize. , 1990, Plant physiology.

[176]  L. Mcintosh,et al.  Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. , 1989, Plant physiology.

[177]  L. Mcintosh,et al.  Characterization and Solubilization of the Alternative Oxidase of Sauromatum guttatum Mitochondria. , 1986, Plant physiology.

[178]  D. Kokkinakis,et al.  Hydrogen Peroxide-mediated Oxidation of Indole-3-acetic Acid by Tomato Peroxidase and Molecular Oxygen. , 1979, Plant physiology.

[179]  B. Meeuse.  Thermogenic Respiration in Aroids , 1975 .

[180]  Hong-hui Lin,et al.  Light intensity affects chlorophyll synthesis during greening process by metabolite signal from mitochondrial alternative oxidase in Arabidopsis. , 2016, Plant, cell & environment.

[181]  Américo Rodrigues,et al.  ABI 1 and PP 2 CA Phosphatases Are Negative Regulators of Snf 1-Related Protein Kinase 1 Signaling in Arabidopsis , 2013 .

[182]  M. Iwaya-Inoue,et al.  Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. , 2013, Annals of botany.

[183]  H. El-Maarouf-Bouteau,et al.  Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. , 2012, Plant & cell physiology.

[184]  T. Horvath,et al.  Mitochondrial uncoupling protein 2 (UCP2) in glucose and lipid metabolism. , 2012, Trends in molecular medicine.

[185]  Xiaolei Liang,et al.  Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus , 2011, Planta.

[186]  F. Song,et al.  Systemic induction and role of mitochondrial alternative oxidase and nitric oxide in a compatible tomato-Tobacco mosaic virus interaction. , 2010, Molecular plant-microbe interactions : MPMI.

[187]  M. Holdsworth,et al.  Post-genomics dissection of seed dormancy and germination. , 2008, Trends in plant science.

[188]  K. Noguchi,et al.  Interaction between photosynthesis and respiration in illuminated leaves. , 2008, Mitochondrion.

[189]  N. Suzuki,et al.  Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction , 2006 .

[190]  L. Vidali,et al.  Polarized cell growth in higher plants. , 2001, Annual review of cell and developmental biology.

[191]  M. Ribas-Carbó,et al.  The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. , 2000, Plant physiology.

[192]  M. Wyss,et al.  Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. , 1992, The Biochemical journal.