Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling

Plant Cell

Volumn 19, Issue 11, 2007, Pages 3723-3738

  Graham, James W A ^a   Williams, Thomas C R ^a   Morgan, Megan ^a   Fernie, Alisdair R ^b   Ratcliffe, R George ^a   Sweetlove, Lee J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT CELL CULTURE; RESPIRATORY MECHANICS; TISSUE;

DUAL LOCALIZATION; GLYCOLYSIS; MITOCHONDRIA;

ENZYMES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; SOLANUM TUBEROSUM;

EID: 37849026162     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.053371     Document Type: Article

References (55)

1. Achnine, L., Blancaflor, E.B., Rasmussen, S., and Dixon, R.A. (2004). Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16: 3098-3109.
2. Averill, R.H., Bailey-Serres, J., and Kruger, N.J. (1998). Co-operation between cytosolic and plastidic oxidative pentose phosphate pathways revealed by 6-phosphogluconate dehydrogenase-deficient genotypes of maize. Plant J. 14: 449-457.
3. Cho, Y.H., Yoo, S.D., and Sheen, J. (2006). Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127: 579-589.
4. Claeyssen, E., and Rivoal, J. (2007). Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochemistry 68: 709-731.
5. Clegg, J.S., and Jackson, S.A. (1990). Glucose metabolism and the channeling of glycolytic intermediates in permeabilized L-929 cells. Arch. Biochem. Biophys. 278: 452-460.
6. Considine, M.J., Goodman, M., Echtay, K.S., Laloi, M., Whelan, J., Brand, M.D., and Sweetlove, L.J. (2003). Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. J. Biol. Chem. 278: 22298-22302.
7. Czichi, U., and Kindl, H. (1977). Phenylalanine ammonia-lyase and cinnamic acid hydroxylases as assembled consecutive enzymes on microsomal membranes of cucumber cotyledons: Cooperation and subcellular distribution. Planta 134: 133-143.
8. Damari-Weissler, H., Ginzburg, A., Gidoni, D., Mett, A., Krassovskaya, I., Weber, A.P., Belausov, E., and Granot, D. (2007). Spinach SoHXK1 is a mitochondria-associated hexokinase. Planta 226: 1053-1058.
9. Damari-Weissler, H., Kandel-Kfir, M., Gidoni, D., Mett, A., Belausov, E., and Granot, D. (2006). Evidence for intracellular spatial separation of hexokinases and fructokinases in tomato plants. Planta 224: 1495-1502.
10. da-Silva, W.S., Gomez-Puyou, A., de Gomez-Puyou, M.T., Moreno-Sanchez, R., De Felice, F.G., de Meis, L., Oliveira, M.F., and Galina, A. (2004). Mitochondrial bound hexokinase activity as a preventive antioxidant defense: Steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J. Biol. Chem. 279: 39846-39855.
11. da-Silva, W.S., Rezende, G.L., and Galina, A. (2001). Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation. J. Exp. Bot. 52: 1191-1201.
12. Dry, I.B., Nash, D., and Wiskich, T.J. (1983). The mitochondrial localization of hexokinase in pea leaves. Planta 158: 152-156.
13. Felle, H., and Bentrup, F.W. (1977). A study of the primary effect of the uncoupler carbonyl cyanide m-chlorophenylhydrazone on membrane potential and conductance in Riccia fluitans. Biochim. Biophys. Acta 464: 179-187.
14. Fox, G.G., Ratcliffe, R.G., and Southon, T.E. (1989). Airlift systems for in vivo NMR spectroscopy of plant tissues. J. Magn. Reson. 82: 360-366.
15. 14C] gluconate. Planta 216: 265-272.
16. Giegé, P., Heazlewood, J.L., Roessner-Tunali, U., Millar, A.H., Fernie, A.R., Leaver, C.J., and Sweetlove, L.J. (2003). Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15: 2140-2151.
17. Grigoriev, A. (2003). On the number of protein-protein interactions in the yeast proteome. Nucleic Acids Res. 31: 4157-4161.
18. Hackett, D.P., Haas, D.W., Griffiths, S.K., and Niederpruem, D.J. (1960). Studies on development of cyanide-resistant respiration in potato tuber slices. Plant Physiol. 35: 8-19.
19. Haggie, P.M., and Verkman, A.S. (2002). Diffusion of tricarboxylic acid cycle enzymes in the mitochondrial matrix in vivo. Evidence for restricted mobility of a multienzyme complex. J. Biol. Chem. 277: 40782-40788.
20. Han, J.D., Bertin, N., Hao, T., Goldberg, D.S., Berriz, G.F., Zhang, L.V., Dupuy, D., Walhout, A.J., Cusick, M.E., Roth, F.P., and Vidal, M. (2004). Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 430: 88-93.
21. Heazlewood, J.L., Howell, K.A., and Millar, A.H. (2003). Mitochondrial complex I from Arabidopsis and rice: Orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim. Biophys. Acta 1604: 159-169.
22. Hodgson, R.J., and Plaxton, W.C. (1998). Purification and characterization of cytosolic fructose-1,6-bisphosphate aldolase from endosperm of germinated castor oil seeds. Arch. Biochem. Biophys. 355: 189-196.
23. Holtgrawe, D., Scholz, A., Altmann, B., and Scheibe, R. (2005). Cytoskeleton-associated, carbohydrate-metabolizing enzymes in maize identified by yeast two-hybrid screening. Physiol. Plant. 125: 141-156.
24. Jeffery, C.J. (2003). Moonlighting proteins: Old proteins learning new tricks. Trends Genet. 19: 415-417.
25. Jorgensen, K., Rasmussen, A.V., Morant, M., Nielsen, A.H., Bjarnholt, N., Zagrobelny, M., Bak, S., and Moller, B.L. (2005). Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8: 280-291.
26. Junker, B.H., Wuttke, R., Tiessen, A., Geigenberger, P., Sonnewald, U., Willmitzer, L., and Fernie, A.R. (2004). Temporally regulated expression of a yeast invertase in potato tubers allows dissection of the complex metabolic phenotype obtained following its constitutive expression. Plant Mol. Biol. 56: 91-110.
27. Kim, M., Lim, J.H., Ahn, C.S., Park, K., Kim, G.T., Kim, W.T., and Pai, H.S. (2006). Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18: 2341-2355.
28. Knowles, V.L., Greyson, M.F., and Dennis, D.T. (1990). Characterization of ATP-dependent fructose 6-phosphate 1-phosphotransferase isozymes from leaf and endosperm tissues of Ricinus communis. Plant Physiol. 92: 155-159.
29. Martin, S.W., Glover, B.J., and Davies, J.M. (2005). Lipid microdomains - Plant membranes get organized. Trends Plant Sci. 10: 263-265.
30. Matic, S., Geisler, D.A., Moller, I.M., Widell, S., and Rasmusson, A.G. (2005). Alamethicin permeabilizes the plasma membrane and mitochondria but not the tonoplast in tobacco (Nicotiana tabacum L. cv Bright Yellow) suspension cells. Biochem. J. 389: 695-704.
31. May, M., and Leaver, C. (1993). Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 103: 621-627.
32. Millar, A.H., Sweetlove, L.J., Giege, P., and Leaver, C.J. (2001). Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127: 1711-1727.
33. Moller, B.L., and Conn, E.E. (1980). The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (linn) Moench. J. Biol. Chem. 255: 3049-3056.
34. Moorhead, G.B., and Plaxton, W.C. (1988). Binding of glycolytic enzymes to a particulate fraction in carrot and sugar beet storage roots. Plant Physiol. 86: 348-351.
35. Moorhead, G.B., and Plaxton, W.C. (1992). Evidence for an interaction between cytosolic aldolase and the ATP- and pyrophosphate-dependent phosphofructokinases in carrot storage roots. FEBS Lett. 313: 277-280.
36. Mustroph, A., Sonnewald, U., and Biemelt, S. (2007). Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana. FEBS Lett. 581: 2401-2410.
37. Noltmann, E. (1972). Group transfer, synthesis coupled to cleavage. In The Enzymes, P.D. Boyer, ed (New York: Academic Press), pp. 271-354.
38. Norris, V., Gascuel, P., Guespin-Michel, J., Ripoll, C., and Saier, M.H., Jr. (1999). Metabolite-induced metabolons: The activation of transporter-enzyme complexes by substrate binding. Mol. Microbiol. 31: 1592-1595.
39. Ovadi, J., and Srere, P.A. (2000). Macromolecular compartmentation and channeling. Int. Rev. Cytol. 192: 255-280.
40. Plaxton, W.C., and Podesta, F.E. (2006). The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 25: 1-40.
41. Podesta, F.E., and Plaxton, W.C. (1992). Plant cytosolic pyruvate kinase: A kinetic study. Biochim. Biophys. Acta 1160: 213-220.
42. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., and Fernie, A.R. (2001). Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29.
43. Rolland, F., Baena-Gonzalez, E., and Sheen, J. (2006). Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu. Rev. Plant Biol. 57: 675-709.
44. Schnarrenberger, C., and Kruger, I. (1986). Distinction between cytosol and chloroplast fructose-bisphosphate aldolases from pea, wheat, and corn leaves. Plant Physiol. 80: 301-304.
45. 2 in intact Escherichia coli. FEBS J. 272: 3260-3269.
46. Smith, A.M.O., Ratcliffe, R.G., and Sweetlove, L.J. (2004). Activation and function of mitochondrial uncoupling protein in plants. J. Biol. Chem. 279: 51944-51952.
47. Sonnewald, U., Hajirezaei, M.R., Kossmann, J., Heyer, A., Trethewey, R.N., and Willmitzer, L. (1997). Increased potato tuber size resulting from apoplastic expression of a yeast invertase. Nat. Biotechnol. 15: 794-797.
48. Srere, P.A. (1987). Complexes of sequential metabolic enzymes. Annu. Rev. Biochem. 56: 89-124.
49. Sweetlove, L.J., and Fernie, A.R. (2005). Regulation of metabolic networks: Understanding metabolic complexity in the systems biology era. New Phytol. 168: 9-24.
50. Taylor, S.W., Fahy, E., Zhang, B., Glenn, G.M., Warnock, D.E., Wiley, S., Murphy, A.N., Gaucher, S.P., Capaldi, R.A., Gibson, B.W., and Ghosh, S.S. (2003). Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21: 281-286.
51. Tomlinson, J.D., and Turner, J.F. (1979). Pea seed triose phosphate isomerase. Plant Physiol 18: 1959-1962.
52. Uhrig, J.F. (2006). Protein interaction networks in plants. Planta 224: 771-781.
53. Villani, G., and Attardi, G. (2007). Polarographic assays of respiratory chain complex activity. In Mitochondria, L.A. Pon and E.A. Schon, eds (New York: Academic Press), pp. 121-132.
54. Wilson, J.E. (2003). Isozymes of mammalian hexokinase: Structure, subcellular localization and metabolic function. J. Exp. Biol. 206: 2049-2057.
55. Winkel, B.S.J. (2004). Metabolic channeling in plants. Annu. Rev. Plant Biol. 55: 85-107.