Abstract
Nucleotide metabolism in potato (Solanum tuberosum) mitochondria was studied using 31P-nuclear magnetic resonance spectroscopy and the O2 electrode. Immediately following the addition of ADP, ATP synthesis exceeded the rate of oxidative phosphorylation, fueled by succinate oxidation, due to mitochondrial adenylate kinase (AK) activity two to four times the maximum activity of ATP synthase. Only when the AK reaction approached equilibrium was oxidative phosphorylation the primary mechanism for net ATP synthesis. A pool of sequestered ATP in mitochondria enabled AK and ATP synthase to convert AMP to ATP in the presence of exogenous inorganic phosphate. During this conversion, AK activity can indirectly influence rates of oxidation of both succinate and NADH via changes in mitochondrial ATP. Mitochondrial nucleoside diphosphokinase, in cooperation with ATP synthase, was found to facilitate phosphorylation of nucleoside diphosphates other than ADP at rates similar to the maximum rate of oxidative phosphorylation. These results demonstrate that plant mitochondria contain all of the machinery necessary to rapidly regenerate nucleoside triphosphates from AMP and nucleoside diphosphates made during cellular biosynthesis and that AK activity can affect both the amount of ADP available to ATP synthase and the level of ATP regulating electron transport.
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- Bomsel J. L., Pradet A. Study of adenosine 5'-mono-,di- and triphosphates in plant tissues. IV. Regulation of the level of nucleotides, in vivo, by adenylate kinase: theoretical and experimental study. Biochim Biophys Acta. 1968 Aug 20;162(2):230–242. doi: 10.1016/0005-2728(68)90105-9. [DOI] [PubMed] [Google Scholar]
- Brdiczka D. Contact sites between mitochondrial envelope membranes. Structure and function in energy- and protein-transfer. Biochim Biophys Acta. 1991 Nov 13;1071(3):291–312. doi: 10.1016/0304-4157(91)90018-r. [DOI] [PubMed] [Google Scholar]
- CHANCE B., WILLIAMS G. R. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134. doi: 10.1002/9780470122624.ch2. [DOI] [PubMed] [Google Scholar]
- Craig D. B., Wallace C. J. Studies of 8-azido-ATP adducts reveal two mechanisms by which ATP binding to cytochrome c could inhibit respiration. Biochemistry. 1995 Feb 28;34(8):2686–2693. doi: 10.1021/bi00008a036. [DOI] [PubMed] [Google Scholar]
- Hooks M. A., Clark R. A., Nieman R. H., Roberts J. K. Compartmentation of Nucleotides in Corn Root Tips Studied by P-NMR and HPLC. Plant Physiol. 1989 Mar;89(3):963–969. doi: 10.1104/pp.89.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- KUBY S. A., MAHOWALD T. A., NOLTMANN E. A. Studies on adenosine triphosphate transphosphorylases. IV. Enzyme-substrate interactions. Biochemistry. 1962 Sep;1:748–762. doi: 10.1021/bi00911a004. [DOI] [PubMed] [Google Scholar]
- Lienhard G. E., Secemski I. I. P 1 ,P 5 -Di(adenosine-5')pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J Biol Chem. 1973 Feb 10;248(3):1121–1123. [PubMed] [Google Scholar]
- Martins O. B., Salgado-Martins I., Grieco M. A., Gómez-Puyou A., de Gómez-Puyou M. T. Binding of adenine nucleotides to the F1-inhibitor protein complex of bovine heart submitochondrial particles. Biochemistry. 1992 Jun 30;31(25):5784–5790. doi: 10.1021/bi00140a014. [DOI] [PubMed] [Google Scholar]
- Neuburger M., Douce R. Effect of bicarbonate and oxaloacetate on malate oxidation by spinach leaf mitochondria. Biochim Biophys Acta. 1980 Feb 8;589(2):176–189. doi: 10.1016/0005-2728(80)90036-5. [DOI] [PubMed] [Google Scholar]
- Neuburger M., Journet E. P., Bligny R., Carde J. P., Douce R. Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch Biochem Biophys. 1982 Aug;217(1):312–323. doi: 10.1016/0003-9861(82)90507-0. [DOI] [PubMed] [Google Scholar]
- Neuburger M., Rébeillé F., Jourdain A., Nakamura S., Douce R. Mitochondria are a major site for folate and thymidylate synthesis in plants. J Biol Chem. 1996 Apr 19;271(16):9466–9472. doi: 10.1074/jbc.271.16.9466. [DOI] [PubMed] [Google Scholar]
- Oestreicher G., Hogue P., Singer T. P. Regulation of Succinate Dehydrogenase in Higher Plants: II. Activation by Substrates, Reduced Coenzyme Q, Nucleotides, and Anions. Plant Physiol. 1973 Dec;52(6):622–626. doi: 10.1104/pp.52.6.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rasmusson A. G., Møller I. M. NADP-Utilizing Enzymes in the Matrix of Plant Mitochondria. Plant Physiol. 1990 Nov;94(3):1012–1018. doi: 10.1104/pp.94.3.1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rusness D. G., Still G. G. Simultaneous measurement of oxidative phosphorylation and adenylate kinase in plant mitochondria. Arch Biochem Biophys. 1973 Nov;159(1):279–291. doi: 10.1016/0003-9861(73)90454-2. [DOI] [PubMed] [Google Scholar]
- Saglio P. H., Raymond P., Pradet A. Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia: CONTROL BY SOLUBLE SUGARS. Plant Physiol. 1980 Dec;66(6):1053–1057. doi: 10.1104/pp.66.6.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singer T. P., Kearney E. B., Kenney W. C. Succinate dehydrogenase. Adv Enzymol Relat Areas Mol Biol. 1973;37:189–272. doi: 10.1002/9780470122822.ch4. [DOI] [PubMed] [Google Scholar]
- Veuthey A. L., Stucki J. The adenylate kinase reaction acts as a frequency filter towards fluctuations of ATP utilization in the cell. Biophys Chem. 1987 Apr;26(1):19–28. doi: 10.1016/0301-4622(87)80003-0. [DOI] [PubMed] [Google Scholar]
- Vignais P. V., Douce R., Lauquin G. J., Vignais P. M. Binding of radioactively labeled carboxyatractyloside, atractyloside and bongkrekic acid to the ADP translocator of potato mitochondria. Biochim Biophys Acta. 1976 Sep 13;440(3):688–696. doi: 10.1016/0005-2728(76)90051-7. [DOI] [PubMed] [Google Scholar]
- Whitehouse D. G., Fricaud A. C., Moore A. L. Role of nonohmicity in the regulation of electron transport in plant mitochondria. Plant Physiol. 1989 Oct;91(2):487–492. doi: 10.1104/pp.91.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]