Exploring the molecular nature of alternative oxidase regulation and catalysis

Plant mitochondria contain a non‐protonmotive alternative oxidase (AOX) that couples the oxidation of ubiquinol to the complete reduction of oxygen to water. In this paper we review theoretical and experimental studies that have contributed to our current structural and mechanistic understanding of the oxidase and to the clarification of the molecular nature of post‐translational regulatory phenomena. Furthermore, we suggest a catalytic cycle for AOX that involves at least one transient protein‐derived radical. The model is based on the reviewed information and on recent insights into the mechanisms of cytochrome c oxidase and the hydroxylase component of methane monooxygenase.

[1]  A. Moore,et al.  Structure and Function of the Plant Alternative Oxidase: Its Putative Role in the Oxygen Defence Mechanism , 1997, Bioscience reports.

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

[3]  P. Rich,et al.  A motif for quinone binding sites in respiratory and photosynthetic systems. , 2000, Journal of molecular biology.

[4]  K. Krab.  Kinetic and regulatory aspects of the function of the alternative oxidase in plant respiration , 1995, Journal of bioenergetics and biomembranes.

[5]  P. Finnegan,et al.  A single amino acid change in the plant alternative oxidase alters the specificity of organic acid activation , 1999, FEBS letters.

[6]  C. Sweet,et al.  Regulation of the Cyanide-resistant Alternative Oxidase of Plant Mitochondria , 1998, The Journal of Biological Chemistry.

[7]  Maarten Merkx,et al.  Dioxygen Activation and Methane Hydroxylation by Soluble Methane Monooxygenase: A Tale of Two Irons and Three Proteins. , 2001, Angewandte Chemie.

[8]  P. Rich.  Quinol oxidation in Arum maculatum mitochondria and its application to the assay, solubilisation and partial purification of the alternative oxidase , 1978 .

[9]  Molecular Localization of a Redox-Modulated Process Regulating Plant Mitochondrial Electron Transport , 1998, Plant Cell.

[10]  M. Kuntz,et al.  Electron Flow between Photosystem II and Oxygen in Chloroplasts of Photosystem I-deficient Algae Is Mediated by a Quinol Oxidase Involved in Chlororespiration* , 2000, The Journal of Biological Chemistry.

[11]  Q. Zhang,et al.  Substrate Kinetics of the Plant Mitochondrial Alternative Oxidase and the Effects of Pyruvate , 1997, Plant physiology.

[12]  R. Sessions,et al.  New sequence data enable modelling of the fungal alternative oxidase and explain an absence of regulation by pyruvate , 2000, FEBS letters.

[13]  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.

[14]  J. Berry,et al.  The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen , 1994 .

[15]  J. M. Palmer,et al.  Isolation of a cyanide‐resistant duroquinol oxidase from arum maculatum mitochondria , 1978, FEBS letters.

[16]  J. Siedow,et al.  The Reaction of the Soybean Cotyledon Mitochondrial Cyanide-resistant Oxidase with Sulfhydryl Reagents Suggests That α-Keto Acid Activation Involves the Formation of a Thiohemiacetal* , 1996, The Journal of Biological Chemistry.

[17]  B. Fox,et al.  Peroxodiferric intermediate of stearoyl-acyl carrier protein delta 9 desaturase: oxidase reactivity during single turnover and implications for the mechanism of desaturation. , 1998, Biochemistry.

[18]  A. Moore,et al.  The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. , 1991, Biochimica et biophysica acta.

[19]  A. Moore,et al.  The active site of the plant alternative oxidase: structural and mechanistic considerations , 2000 .

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

[21]  A. Moore,et al.  Structure-function relationships of the alternative oxidase of plant mitochondria: A model of the active site , 1995, Journal of bioenergetics and biomembranes.

[22]  A. Moore,et al.  A kinetic model for the regulation of electron transfer through the cyanide-resistant pathway in plant mitochondria , 1993 .

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

[24]  H. Blum,et al.  Studies on the mechanism of inhibition of redox enzymes by substituted hydroxamic acids. , 1978, Biochimica et biophysica acta.

[25]  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.

[26]  John D. Lipscomb,et al.  Dioxygen Activation by Enzymes Containing Binuclear Non-Heme Iron Clusters. , 1996, Chemical reviews.

[27]  M. Kuntz,et al.  Mutations in the Arabidopsis Gene IMMUTANS Cause a Variegated Phenotype by Inactivating a Chloroplast Terminal Oxidase Associated with Phytoene Desaturation , 1999, Plant Cell.

[28]  K. Krab,et al.  Control of plant mitochondrial respiration. , 2001, Biochimica et biophysica acta.

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

[30]  D. Voytas,et al.  The IMMUTANS Variegation Locus of Arabidopsis Defines a Mitochondrial Alternative Oxidase Homolog That Functions during Early Chloroplast Biogenesis , 1999, Plant Cell.

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

[32]  J. Siedow,et al.  The cyanide-resistant alternative oxidases from the fungi Pichia stipitis and Neurospora crassa are monomeric and lack regulatory features of the plant enzyme. , 2000, Archives of biochemistry and biophysics.

[33]  D. A. Berthold,et al.  New insight into the structure and function of the alternative oxidase. , 2000, Biochimica et biophysica acta.

[34]  D. Hollomon,et al.  Characterization of a Split Respiratory Pathway in the Wheat “Take-all” Fungus, Gaeumannomyces graminis var.tritici * , 1998, The Journal of Biological Chemistry.

[35]  A. Moore,et al.  Measurements of membrane potentials in plant mitochondria with the safranine method. , 1982, Plant physiology.

[36]  S. Lippard,et al.  Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath). , 1999, Biochemistry.

[37]  G. Babcock,et al.  Oxygen activation and the conservation of energy in cell respiration , 1992, Nature.

[38]  D. A. Berthold.  Isolation of mutants of the Arabidopsis thaliana alternative oxidase (ubiquinol:oxygen oxidoreductase) resistant to salicylhydroxamic acid. , 1998, Biochimica et biophysica acta.

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

[40]  P. Rich,et al.  The determination of the proton-motive force during cyanide-insensitive respiration in plant mitochondria. , 1978, Archives of biochemistry and biophysics.

[41]  G. C. Hill,et al.  Biochemical and molecular properties of the Trypanosoma brucei alternative oxidase. , 1998, Molecular and biochemical parasitology.

[42]  J. Wiskich,et al.  Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria , 1994, FEBS letters.

[43]  A. Moore,et al.  A Highly Conserved Glutamate Residue (Glu-270) Is Essential for Plant Alternative Oxidase Activity* , 1998, The Journal of Biological Chemistry.

[44]  J. Siedow,et al.  The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. , 2000, Biochimica et biophysica acta.

[45]  J. Klinman,et al.  Oxygen Kinetic Isotope Effects in Soluble Methane Monooxygenase* , 2001, The Journal of Biological Chemistry.

[46]  C. DeMaso,et al.  Oxygen activation and reduction in respiration: involvement of redox-active tyrosine 244. , 2000, Science.