Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana

Biochemical Journal

Volumn 397, Issue 1, 2006, Pages 139-148

  Lunn, John E ^a   Feil, Regina ^a   Hendriks, Janneke H M ^a   Gibon, Yves ^a   Morcuende, Rosa ^b   Osuna, Daniel ^a   Scheible, Wolf Rüdiger ^a   Carillo, Petronia ^c   Hajirezaei, Mohammad Reza ^d   Stitt, Mark ^a  

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

^b INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Liquid chromatography MS (LC MS); Redox regulation; Starch; Sucrose; Trehalose 6 phosphate (Tre6P); Triple quadrupole MS (MS Q3)

Indexed keywords

BIOASSAY; CELL CULTURE; LIQUID CHROMATOGRAPHY; REDOX REACTIONS; STARCH; SYNTHESIS (CHEMICAL); TISSUE;

LIQUID CHROMATOGRAPHY-MS (LC-MS); REDOX REGULATION; TREHALOSE 6-PHOSPHATE (TRE6P); TRIPLE QUADRUPOLE MS (MS-Q3);

SUGAR (SUCROSE);

GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE; STARCH; SUCROSE; TREHALOSE; DRUG DERIVATIVE; SUGAR PHOSPHATE; TREHALOSE 6 PHOSPHATE; TREHALOSE-6-PHOSPHATE;

ANION EXCHANGE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; CONTROLLED STUDY; CORRELATION ANALYSIS; FRESH WEIGHT; IN VIVO STUDY; LIGHT DARK CYCLE; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEEDLING; SIGNAL TRANSDUCTION; STARVATION; SYNTHESIS; WILD TYPE; BIOSYNTHESIS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SENSITIVITY AND SPECIFICITY;

ARABIDOPSIS THALIANA;

ARABIDOPSIS; CHROMATOGRAPHY, LIQUID; GLUCOSE-1-PHOSPHATE ADENYLYLTRANSFERASE; OXIDATION-REDUCTION; SEEDLING; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; STARCH; SUCROSE; SUGAR PHOSPHATES; TREHALOSE;

EID: 33745530598     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060083     Document Type: Article

References (39)

1. Cabib, E. and Leloir, L. F. (1958) The biosynthesis of trehalose phosphate. J. Biol. Chem. 231, 259-275
2. Blázquez, M. A., Lagunas, R., Gancedo, C. and Gancedo, J. M. (1993) Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett. 329, 51-54
3. Iturriaga, G., Gaff, D. F. and Zentella, R. (2000) New desiccation-tolerant plants, including a grass, in the central highlands of Mexico, accumulate trehalose. Aust. J. Bot. 48, 153-158
4. Eastmond, P. J., van Dijken, A. J. H., Spielman, M., Kerr, A., Tissier, A. F., Dickinson, H. G., Jones, J. D. G., Smeekens, S. C. and Graham, I. A. (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J. 29, 225-235
5. van Dijken, A. J. H., Schluepmann, H. and Smeekens, S. (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969-977
6. Romero, C., Bellés, J. M., Vayá, J. L., Serrano, R. and Culiáñez-Macià (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201, 293-297
7. Goddijn, O. J. M., Verwoerd, T. C., Voogd, E., Krutwagen, R. W. H. H., de Graaf, P. T. H. M., Poels, J., van Dun, K., Ponstein, A. S., Damm, B. and Pen, J. (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol. 113, 181-190
8. Pilon-Smits, E. A. H., Terry, N., Sears, T., Kim, H., Zayed, A., Hwang, S., van Dun, K., Voogd, E., Verwoerd, T. C., Krutwagen, R. W. H. H. and Goddijn, O. J. M. (1998) Trehalose-producing transgenic tobacco plants show improved performance under drought stress. J. Plant Physiol. 152, 525-532
9. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S. and Paul, M. (2003) Trehalose 6-phosphate is indispensible for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 6849-6854
10. Kolbe, A., Tiessen, A., Schluepmann, H., Paul, M., Ulrich, S. and Geigenberger, P. (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc. Natl. Acad. Sci. U.S.A. 102, 11118-11123
11. Scheible, W.-R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., Schindlasch, D., Thimm, O., Udvardi, M. K. and Stitt, M. (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483-2499
12. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L. A., Rhee, S. Y. and Stitt, M. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939
13. Price, J., Laxmi, A., St. Martin, S. K. and Jang, J.-C. (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16, 2128-2150
14. Schluepmann, H., van Dijken, A., Aghdasi, M., Wobbes, B., Paul, M. and Smeekens, S. (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol. 135, 879-890
15. Wang, R., Okamoto, M., Xing, X. and Crawford, N. M. (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6- phosphate, iron, and sulfate metabolism. Plant Physiol. 132, 556-567
16. Avonce, N., Leyman, B., Mascorro-Gallardo, J. O., van Dijck, P., Thevelein, J. M. and Iturriaga, G. (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signalling. Plant Physiol. 136, 3649-3659
17. Moorhead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Stitt, M., Scarabel, M., Aitken, A. and MacKintosh, C. (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J. 18, 1-12
18. Glinski, M. and Weckwerth, W. (2005) Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana - a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Mol. Cell. Proteomics 4, 1614-1625
19. Gonzali, S., Alpi, A., Blando, F. and de Bellis, L. (2002) Arabidopsis (HXK1 and HXK2) and yeast (HXK2) hexokinases overexpressed in transgenic lines are characterized by different catalytic properties. Plant Sci. 163, 943-954
20. Fu, Y., Ballicora, M. A., Leykam, J. F. and Preiss, J. (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J. Biol. Chem. 273, 25045-25052
21. Tiessen, A., Hendriks, J. H. M., Stitt, M., Branscheid, A., Gibon, Y., Farré, E. M. and Geigenberger, P. (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14, 2191-2213
22. Tiessen, A., Prescha, K., Bransceid, A., Pacios, N., McKibbin, R., Halford, N. G. and Geigenberger, P. (2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J. 35, 490-500
23. Hendriks, J. H. M., Kolbe, A., Gibon, Y., Stitt, M. and Geigenberger, P. (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol. 133, 838-849
24. van Vaeck, C., Wera, S., van Dijck, P. and Thevelein, J. M. (2001) Analysis and modification of trehalose 6-phosphate levels in the yeast Saccharomyces cerevisiae with the use of Bacillus subtilis phosphotrehalase. Biochem. J. 353, 157-162
25. Blázquez, M. A., Gancedo, J. M. and Gancedo, C. (1994) Use of Yarrowia lipolytica hexokinase for the quantitative determination of trehalose 6-phosphate. FEMS Microbiol. Lett. 121, 223-228
26. Caspar, T., Huber, S. C. and Somerville, C. R. (1985) Alterations in growth, photosynthesis and respiration in a starch deficient mutant of Arabidopsis thaliana (L.) Heynh. deficient in chloroplast phosphoglucomutase. Plant Physiol. 79, 11-17
27. Bläsing, O. E., Gibon, Y., Günther, M., Höhne, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.-R. and Stitt, M. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17, 3257-3281
28. Gotsche, S. and Dahl, M. K. (1995) Purification and characterization of the phospho-α(1,1)glucosidase (TreA) of Bacillus subtilis 168. J. Bacteriol. 177, 2721-2726
29. Lunn, J. E. and Hatch, M. D. (1997) The role of sucrose-phosphate synthase in the control of photosynthate partitioning in Zea mays leaves. Aust. J. Plant Physiol. 24, 1-8
30. F-phosphate phosphohydrolase from plants. Proc. Natl. Acad. Sci. U.S.A. 97, 12914-12919
31. Fieulaine, S., Lunn, J. E., Borel, F., and Ferrer, J.-L. (2005) The structure of a cyanobacterial sucrose-phosphatase reveals the sugar tongs that release free sucrose in the cell. Plant Cell 17, 2049-2058
32. Nordström, A., Tarkowski, P., Torkowska, D., Dolezal, K., Åstot, C., Sandberg, G. and Moritz, T. (2004) Derivatization for LC-electrospray ionization-MS: a tool for improving reversed-phase separation and ESI responses of bases, ribosides, and intact nucleotides. Anal. Chem. 76, 2869-2877
33. Oldiges, M., Kunze, M., Degenring, D., Sprenger, G. A. and Takors, R. (2004) Stimulation, monitoring, and analysis of pathway dynamics by metabolic profiling in the aromatic amino acid pathway. Biotechnol. Prog. 20, 1623-1633
34. Bader, A. (1980) A systematic approach to standard addition methods in instrumental analysis. J. Chem. Edu. 57, 703-706
35. Gibon, Y., Vigeolas, H., Tiessen, A., Geigenberger, P. and Stitt, M. (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. Plant J. 30, 221-235
36. Gibon, Y., Bläsing, O., Palacios, N., Pankovic, D., Hendriks, J. H. M., Fisahn, J., Höhne, M., Günter, M. and Stitt, M. (2004) Adjustment of diurnal starch turnover to short days: a transient depletion of sugar towards the end of the night triggers a temporary inhibition of carbohydrate utilisation, leading to accumulation of sugars and post-translational activation of ADP glucose pyrophosphorylase in the following light period. Plant J. 39, 847-862
37. Winter, H., Robinson, D. G. and Heldt, H. W. (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193, 530-535
38. Heineke, D., Wildenberger, K., Sonnewald, U., Willmitzer, L. and Heldt, H. W. (1994) Accumulation of hexoses in leaf vacuoles: Studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194, 29-33
39. Stitt, M., Huber, S. and Kerr, P. (1987) Control of Photosynthetic Sucrose Synthesis. In: The Biochemistry of Plants Vol. 10 (Hatch, M. D. and Boardman, N. K., eds.), pp. 327-409, Academic Press, San Diego