Magnesium and cell energetics in plants under anoxia

Biochemical Journal

Volumn 437, Issue 3, 2011, Pages 373-379

  Igamberdiev, Abir U ^a   Kleczkowski, Leszek A ^b  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Adenylate equilibrium; Adenylate kinase (AK); Free magnesium; Phosphate dikinase (PPDK); Pyrophosphate (PP i); Pyruvate; Thermodynamic buffering

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ALCOHOL; CALCIUM ION; MAGNESIUM ION; PYRUVATE KINASE; PYRUVATE PHOSPHATE DIKINASE; SUCROSE;

ANOXIA; CALCIUM SIGNALING; CELL ENERGY; ENERGY RESOURCE; ENZYME SUBSTRATE; FEEDBACK SYSTEM; GLYCOLYSIS; NONHUMAN; PLANT CELL; PLANT STRESS; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; REVIEW;

CALCIUM SIGNALING; ENERGY METABOLISM; MAGNESIUM; OXYGEN; PHOSPHORUS; PLANTS;

EID: 79956020204     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110213     Document Type: Review

References (78)

1. Hochacka, P. W. and Somero, G. N. (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution, Oxford University Press, Oxford
2. Allègre, A., Silvestre, J., Morard, P., Kallerhoff, J. and Pinelli, E. (2004) Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J. Exp. Bot. 55, 2625-2634
3. Saglio, P. H., Drew, M. C. and Pradet, A. (1988) Metabolic acclimation to anoxia induced by low (2-4 kPa partial pressure) oxygen pretreatment (hypoxia) in root tips of Zea mays. Plant Physiol. 86, 61-66
4. Stoimenova, M., Igamberdiev, A. U., Gupta, K. J. and Hill, R. D. (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226, 465-474
5. 2+ are interconnected via adenylate kinase equilibrium in plant cells. Biochim. Biophys. Acta 1607, 111-119
6. Marschner, H. (1995) Mineral Nutrition in Higher Plants, Academic Press, San Diego
7. Igamberdiev, A. U. and Kleczkowski, L. A. (2001) Implications of adenylate kinase-governed equilibrium of adenylates on contents of free magnesium in plant cells and compartments. Biochem. J. 360, 225-231
8. Peller, L. (1977) Thermodynamic limits on size and size distribution of nucleic acids synthesized in vitro - role of pyrophosphate hydrolysis. Biochemistry 16, 387-395
9. Hemalatha, K. P. and Prasad, D. S. (2002) Purification, physicochemical properties, and subcellular location of alkaline inorganic pyrophosphatase from sesame (Sesamum indicum L.) cotyledons. Biochem. Cell Biol. 80, 215-224
10. Stitt, M. (1998) Pyrophosphate as an energy donor in the cytosol of plant cells: an enigmatic alternative to ATP. Bot. Acta 111, 167-175
11. Huang, S. B., Greenway, H., Colmer, T. D. and Millar, A. H. (2005) Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. Ann. Bot. 96, 703-715
12. Huang, S. B., Colmer, T. D. and Millar, A. H. (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci. 13, 221-227
13. Lasanthi-Kudahettige, R., Magneschi, L., Loreti, E., Gonzali, S., Licausi, F., Novi, G., Beretta, O., Vitulli, F., Alpi, A. and Perata, P. (2007) Transcript profiling of anoxic rice coleoptile. Plant Physiol. 144, 218-231 (Pubitemid 46941626)
14. Narsai, R., Howell, K. A., Carroll, A., Ivanova, A., Millar, A. H. and Whelan, J. (2009) Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol. 151, 306-322
15. 2+ binding activates adenylate kinase from Escherichia coli. J. Biol. Chem. 284, 3306-3313
16. Blair, J. M. D. (1969) Magnesium and aconitase equilibrium - determination of apparent stability constants of magnesium substrate complexes from equilibrium data. Eur. J. Biochem. 8, 287-291
17. Igamberdiev, A. U. and Gardeström, P. (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta 1606, 117-125
18. Kleczkowski, L. A. and Randall, D. D. (1991) Equilibration of adenylates by maize leaf adenylate kinase: effects of magnesium on apparent and true equilibria. J. Exp. Bot. 42, 537-540
19. Raymond, P. and Pradet, A. (1980) Stabilization of adenine nucleotide ratios at various values by an oxygen limitation of respiration in germinating lettuce (Lactuca sativa ) seeds. Biochem. J. 190, 39-44
20. Drew, M. C., Saglio, P. H. and Pradet, A. (1985) Larger adenylate energy charge and ATP/ADP ratios in aerenchymatous roots of Zea mays in anaerobic media as a consequence of improved internal oxygen transport. Planta 165, 51-58
21. + nutrition on fermentation, nitrate reductase activity and adenylate energy charge of roots of Carex pseudocyperus L. and Carex sylvatica Huds. exposed to anaerobic nutrient solutions. Plant Soil 166, 221-230
22. Igamberdiev, A. U. and Kleczkowski, L. A. (2006) Equilibration of adenylates in the mitochondrial intermembrane space maintains respiration and regulates cytosolic metabolism. J. Exp. Bot. 57, 2133-2141
23. Gilli, R., Lafitte, D., Lopez, C., Kilhoffer, M., Makarov, A., Briand, C. and Haiech, J. (1998) Thermodynamic analysis of calcium and magnesium binding to calmodulin. Biochemistry 37, 5450-5456 (Pubitemid 28241925)
24. Malmendal, A., Linse, S., Evenas, J., Forsen, S. and Drakenberg, T. (1999) Battle for the EF-hands: magnesium-calcium interference in calmodulin. Biochemistry 38, 11844-11850
25. Subbaiah, C. C., Zhang, J. and Sachs, M. M. (1994) Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiol. 105, 369-376
26. 2+ as a second messenger within mitochondria. Trends Biochem. Sci. 11, 258-262
27. Møller, I. M. and Rasmusson, A. G. (1998) The role of NADP in the mitochondrial matrix. Trends Plant Sci. 3, 21-27
28. Zielinski, R. E. (1998) Calmodulin and calmodulin-binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 697-725
29. Vincent, A. and Blair, J. M. (1970) The coupling of the adenylate kinase and creatine kinase equilibria. Calculation of substrate and feedback signal levels in muscle. FEBS Lett. 7, 239-244
30. Sillen, L. G. and Martell, A. E. (1964) Stability Constants of Metal Ion Complexes, Chemical Society, London
31. Aurisano, N., Bertani, A. and Reggiani, R. (1995) Involvement of calcium and calmodulin in protein and amino acid metabolism in rice roots under anoxia. Plant Cell Physiol. 36, 1525-1529 (Pubitemid 3024326)
32. + -pyrophosphatase - the roles of magnesium, pyrophosphate, and their complexes as substrates, activators, and inhibitors. Plant Physiol. 100, 1698-1705
33. Rasmusson, A. G. and Møller, I. M. (1991) Effect of calcium ions and inhibitors on internal NAD(P)H dehydrogenases in plant mitochondria. Eur. J. Biochem. 202, 617-623
34. 2+ concentrations and pHs. Plant Cell Physiol. 45, 1371-1379
35. Davies, J., Poole, R. and Sanders, D. (1993) The computed free energy change of hydrolysis of inorganic pyrophosphate and ATP - apparent significance for inorganic pyrophosphate-driven reactions of intermediary metabolism. Biochim. Biophys. Acta 1141, 29-36
36. Baltscheffsky, M. (1967) Inorganic pyrophosphate as an energy donor in photosynthetic and respiratory electron transport phosphorylation systems. Biochem. Biophys. Res. Commun. 28, 270-276
37. Kleczkowski, L. A. (1996) Back to the drawing board: redefining starch synthesis in cereals. Trends Plant Sci. 1, 363-364
38. Horder, M. (1974) Complex formation of inorganic pyrophosphate with magnesium - influence of ionic strength, supporting medium and temperature. Biochim. Biophys. Acta 358, 319-328
39. Martell, A. E. and Smith, R. (1976) Critical Stability Constants, Plenum Press, New York
40. O'Sullivan, W. J. and Smithers, G. W. (1979) Stability constants for biologically important metal-ligand complexes. Methods Enzymol. 63, 294-336
41. Airas, R. K. (1996) Differences in the magnesium dependences of the class I and class II aminoacyl-tRNA synthetases from Escherichia coli. Eur. J. Biochem. 240, 223-231
42. +-pyrophosphatase. Biochim. Biophys. Acta 1465, 37-51
43. Nilima, K. and Vinay, S. (2008) V-PPase in plants: an overview. Res. J. Biotechnol. 3, 57-63
44. + -pyrophosphatase by free calcium - a reaction kinetic analysis. Plant Physiol. 100, 1706-1715
45. Davies, J. M. (1997) Vacuolar energization: Pumps, shunts and stress. J. Exp. Bot. 48, 633-641
46. Kumari, N. and Sharma, V. (2010) Stress-mediated alteration in V-ATPase and V-PPase of Butea monosperma . Protoplasma 245, 125-132
47. + -translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol. 108, 641-649
48. Patel, R. C. and Taylor, R. S. (1973) Kinetics of binding of pyrophosphate to magnesium ions. J. Phys. Chem. 77, 2318-2323
49. Felle, H. H. (2005) pH regulation in anoxic plants. Ann. Bot. 96, 519-532
50. Farré, E. M., Tech, S., Trethewey, R. N., Fernie, A. R. and Willmitzer, L. (2006) Subcellular pyrophosphate metabolism in developing tubers of potato (Solanum tuberosum). Plant Mol. Biol. 62, 165-179 (Pubitemid 44372895)
51. 2+ -dependent soluble inorganic pyrophosphatases in potato and phylogenetic analysis. Plant Mol. Biol. 39, 449-461
52. Xu, D. P., Sung, S. J. S., Alvarez, C. A. and Black, C. C. (1986) Pyrophosphate-dependent sucrose metabolism and its activation by fructose 2,6-bisphosphate in sucrose importing plant tissues. Biochem. Biophys. Res. Commun. 141, 440-445
53. Igamberdiev, A. U. and Kleczkowski, L. A. (2009) Metabolic systems maintain stable non-equilibrium via thermodynamic buffering. BioEssays 31, 1091-1098
54. Dancer, J., Veith, R., Feil, R., Komor, E. and Stitt, M. (1990) Independent changes of inorganic pyrophosphate and the ATP/ADP or UTP/UDP ratios in plant cell suspension cultures. Plant Sci. 66, 59-63
55. Mustroph, A., Albrecht, G., Hajirezaei, M., Grimm, B. and Biemelt, S. (2005) Low levels of pyrophosphate in transgenic potato plants expressing E. coli pyrophosphatase lead to decreased vitality under oxygen deficiency. Ann. Bot. 96, 717-726
56. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K. and Eppenberger, H. M. (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 281, 21-40
57. Kawai, M., Umeda, M. and Uchimiya, H. (1998) Stimulation of adenylate kinase in rice seedlings under submergence stress. J. Plant Physiol. 152, 533-539 (Pubitemid 28244562)
58. Kleczkowski, L. A. and Randall, D. D. (1986) Maize leaf adenylate kinase: purification and partial characterization. Plant Physiol. 81, 1110-1114
59. Hardie, D. G. and Hawley, S. A. (2001) AMP-activated protein kinase: the energy charge hypothesis revisited. BioEssays 23, 1112-1119
60. Geigenberger, P., Fernie, A. R., Gibon, Y., Christ, M. and Stitt, M. (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol. Chem. 381, 723-740
61. Geigenberger, P., Riewe, D. and Fernie, A. R. (2010) The central regulation of plant physiology by adenylates. Trends Plant Sci. 15, 98-105
62. i-mediated activation of pyruvate, Pi dikinase. Arch. Biochem. Biophys. 237, 490-503
63. Budde, R. J. A., Ernst, S. M. and Chollet, R. (1986) Substrate specificity and regulation of the maize (Zea mays) leaf ADP: protein phosphotransferase catalyzing phosphorylation/inactivation of pyruvate, orthophosphate dikinase. Biochem. J. 236, 579-584
64. Chastain, C. J., Xu, W., Parsley, K., Sarath, G., Hibberd, J. M. and Chollet, R. (2008) The pyruvate, orthophosphate dikinase regulatory proteins of Arabidopsis possess a novel, unprecedented Ser/Thr protein kinase primary structure. Plant J. 53, 854-863 (Pubitemid 351495863)
65. Fridlyand, L. E. and Scheibe, R. (2000) Regulation in metabolic systems under homeostatic flux control. Arch. Biochem. Biophys. 374, 198-206
66. Igamberdiev, A. U. and Kleczkowski, L. A. (2011) Optimization of CO2 fixation in photosynthetic cells via thermodynamic buffering. BioSystems 103, 224-229
67. Hagedorn, P. H., Flyvbjerg, H. and Møller, I. M. (2004) Modelling NADH turnover in plant mitochondria. Physiol. Plant. 120, 370-385
68. MacDougall, A. J. and ApRees, T. (1991) Control of the Krebs cycle in Arum spadix. J. Plant Physiol. 137, 683-690
69. Mechin, V., Thevenot, C., Le Guilloux, M., Prioul, J. L. and Damerval, C. (2007) Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol. 143, 1203-1219 (Pubitemid 46941538)
70. Martin, M., Plaxton, W. C. and Podestá, F. E. (2007) Activity and concentration of non-proteolyzed phosphoenolpyruvate carboxykinase in the endosperm of germinating castor oil seeds: effects of anoxia on its activity. Physiol. Plant. 130, 484-494
71. Alonso, A. P., Raymond, P., Rolin, D. and Dieuaide-Noubhani, M. (2007) Substrate cycles in the central metabolism of maize root tips under hypoxia. Phytochemistry 68, 2222-2231 (Pubitemid 47211192)
72. Kowalczyk, S. and Maslowski, P. (1984) Oxidation-linked formation of inorganic pyrophosphate in maize shoot mitochondria. Biochim. Biophys. Acta 766, 570-575
73. Casolo, V., Micolini, S., Macri, F. and Vianello, A. (2002) Pyrophosphate import and synthesis by plant mitochondria. Physiol. Plant. 114, 516-523
74. Vianello, A. and Macri, F. (1999) Proton pumping pyrophosphatase from higher plant mitochondria. Physiol. Plant. 105, 763-768
75. Koch, K. (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, 235-246
76. Bieniawska, Z., Barratt, D. H. P., Garlick, A. P., Thole, V., Kruger, N. J., Martin, C., Zrenner, R. and Smith, A. M. (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J. 49, 810-828
77. Kleczkowski, L. A., Kunz, S. and Wilczynska, M. (2010) Mechanisms of UDP-glucose synthesis in plants. Crit. Rev. Plant Sci. 29, 191-203
78. Plaxton, W. C. and Podestá, F. E. (2006) The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 25, 159-198