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. 1996 Jun;111(2):589–595. doi: 10.1104/pp.111.2.589

Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria.

G C Vanlerberghe 1, L McLntosh 1
PMCID: PMC157870  PMID: 12226312

Abstract

Suspension cells of tobacco (Nicotiana tabacum L. cv Bright Yellow) were used to investigate signals regulating the expression of the nuclear gene Aox1 encoding the mitochondrial alternative oxidase (AOX) protein responsible for cyanide-resistant respiration in plants. We found that an increase in the tricarboxylic acid cycle intermediate citrate (either after its exogenous supply to cells or after inhibition of aconitase by monofluoroacetate) caused a rapid and dramatic increase in the steady-state level of Aox1 mRNA and AOX protein. This led to a large increase in the capacity for AOX respiration, defined as the amount of salicylhydroxamic acid-sensitive O2 uptake by cells in the presence of potassium cyanide. The results indicate that citrate may be an important signal metabolite regulating Aox1 gene expression. A number of other treatments were also identified that rapidly induced the level of Aox1 mRNA and AOX capacity. These included short-term incubation of cells with 10 mM acetate, 2 [mu]M antimycin A, 5 mM H2O2, or 1 mM cysteine. For some of these treatments, induction of AOX occurred without an increase in cellular citrate level, indicating that other signals (possibly related to oxidative stress conditions) are also important in regulating Aox1 gene expression. The signals influencing Aox1 gene expression are discussed with regard to the potential function(s) of AOX to modulate tricarboxylic acid cycle metabolism and/or to prevent the generation of active oxygen species by the mitochondrial electron transport chain.

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Selected References

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  1. Boveris A., Cadenas E., Stoppani A. O. Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J. 1976 May 15;156(2):435–444. doi: 10.1042/bj1560435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  3. Conley C. A., Hanson M. R. Tissue-Specific Protein Expression in Plant Mitochondria. Plant Cell. 1994 Jan;6(1):85–91. doi: 10.1105/tpc.6.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Day D. A., Wiskich J. T. Regulation of alternative oxidase activity in higher plants. J Bioenerg Biomembr. 1995 Aug;27(4):379–385. doi: 10.1007/BF02110000. [DOI] [PubMed] [Google Scholar]
  5. Graham I. A., Denby K. J., Leaver C. J. Carbon Catabolite Repression Regulates Glyoxylate Cycle Gene Expression in Cucumber. Plant Cell. 1994 May;6(5):761–772. doi: 10.1105/tpc.6.5.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Green P. J. Control of mRNA Stability in Higher Plants. Plant Physiol. 1993 Aug;102(4):1065–1070. doi: 10.1104/pp.102.4.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hill S. A., Grof C. P., Bryce J. H., Leaver C. J. Regulation of Mitochondrial Function and Biogenesis in Cucumber (Cucumis sativus L.) Cotyledons during Early Seedling Growth. Plant Physiol. 1992 May;99(1):60–66. doi: 10.1104/pp.99.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hiser C., McIntosh L. Alternative Oxidase of Potato Is an Integral Membrane Protein Synthesized de Novo during Aging of Tuber Slices. Plant Physiol. 1990 May;93(1):312–318. doi: 10.1104/pp.93.1.312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hoefnagel M. H., Millar A. H., Wiskich J. T., Day D. A. Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria. Arch Biochem Biophys. 1995 Apr 20;318(2):394–400. doi: 10.1006/abbi.1995.1245. [DOI] [PubMed] [Google Scholar]
  10. Hérouart D., Van Montagu M., Inzé D. Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3108–3112. doi: 10.1073/pnas.90.7.3108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kapulnik Y., Yalpani N., Raskin I. Salicylic Acid induces cyanide-resistant respiration in tobacco cell-suspension cultures. Plant Physiol. 1992 Dec;100(4):1921–1926. doi: 10.1104/pp.100.4.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kearns A., Whelan J., Young S., Elthon T. E., Day D. A. Tissue-specific expression of the alternative oxidase in soybean and siratro. Plant Physiol. 1992 Jun;99(2):712–717. doi: 10.1104/pp.99.2.712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leprince O., Atherton N. M., Deltour R., Hendry GAF. The Involvement of Respiration in Free Radical Processes during Loss of Desiccation Tolerance in Germinating Zea mays L. (An Electron Paramagnetic Resonance Study). Plant Physiol. 1994 Apr;104(4):1333–1339. doi: 10.1104/pp.104.4.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McIntosh L. Molecular biology of the alternative oxidase. Plant Physiol. 1994 Jul;105(3):781–786. doi: 10.1104/pp.105.3.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moore A. L., Siedow J. N. The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta. 1991 Aug 23;1059(2):121–140. doi: 10.1016/s0005-2728(05)80197-5. [DOI] [PubMed] [Google Scholar]
  16. Prasad T. K., Anderson M. D., Martin B. A., Stewart C. R. Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide. Plant Cell. 1994 Jan;6(1):65–74. doi: 10.1105/tpc.6.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Siedow J. N., Umbach A. L. Plant Mitochondrial Electron Transfer and Molecular Biology. Plant Cell. 1995 Jul;7(7):821–831. doi: 10.1105/tpc.7.7.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Smart C. J., Monéger F., Leaver C. J. Cell-specific regulation of gene expression in mitochondria during anther development in sunflower. Plant Cell. 1994 Jun;6(6):811–825. doi: 10.1105/tpc.6.6.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Stewart C. R., Martin B. A., Reding L., Cerwick S. Seedling growth, mitochondrial characteristics, and alternative respiratory capacity of corn genotypes differing in cold tolerance. Plant Physiol. 1990 Mar;92(3):761–766. doi: 10.1104/pp.92.3.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Thomas B. R., Rodriguez R. L. Metabolite Signals Regulate Gene Expression and Source/Sink Relations in Cereal Seedlings. Plant Physiol. 1994 Dec;106(4):1235–1239. doi: 10.1104/pp.106.4.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Vanlerberghe G. C., McIntosh L. Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco. Plant Physiol. 1994 Jul;105(3):867–874. doi: 10.1104/pp.105.3.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Vanlerberghe G. C., Vanlerberghe A. E., McIntosh L. Molecular Genetic Alteration of Plant Respiration (Silencing and Overexpression of Alternative Oxidase in Transgenic Tobacco). Plant Physiol. 1994 Dec;106(4):1503–1510. doi: 10.1104/pp.106.4.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Verniquet F., Gaillard J., Neuburger M., Douce R. Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J. 1991 Jun 15;276(Pt 3):643–648. doi: 10.1042/bj2760643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Virbasius J. V., Scarpulla R. C. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1309–1313. doi: 10.1073/pnas.91.4.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wagner A. M. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 1995 Jul 17;368(2):339–342. doi: 10.1016/0014-5793(95)00688-6. [DOI] [PubMed] [Google Scholar]
  26. Walker J. L., Oliver D. J. Light-induced increases in the glycine decarboxylase multienzyme complex from pea leaf mitochondria. Arch Biochem Biophys. 1986 Aug 1;248(2):626–638. doi: 10.1016/0003-9861(86)90517-5. [DOI] [PubMed] [Google Scholar]
  27. Wilson S. B. The switching of electron flux from the cyanide-insensitive oxidase to the cytochrome pathway in mung-bean (Phaseolus aureus L.) mitochondria. Biochem J. 1988 Jan 1;249(1):301–303. doi: 10.1042/bj2490301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Winde J. H., Grivell L. A. Global regulation of mitochondrial biogenesis in Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol. 1993;46:51–91. doi: 10.1016/s0079-6603(08)61018-1. [DOI] [PubMed] [Google Scholar]

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