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

Molecular and Cellular Proteomics

Volumn 4, Issue 10, 2005, Pages 1614-1625

  Glinski, Mirko ^a   Weckwerth, Wolfram ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHLORIDE; PHOSPHOPEPTIDE; PROTEIN KINASE; SYNTHETASE; SYNTHETIC PEPTIDE; TREHALOSE 6 PHOSPHATE SYNTHETASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLIC REGULATION; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ARABIDOPSIS; CALCIUM; CALIBRATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CONSENSUS SEQUENCE; GLUCOSYLTRANSFERASES; ISOENZYMES; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE LIBRARY; PEPTIDES; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN KINASES; SENSITIVITY AND SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 27644593240     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M500134-MCP200     Document Type: Article

References (48)

1. Roessner, U., Wagner, C., Kopka, J., Trethewey, R. N., and Willmitzer, L. (2000) Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23, 131-142
2. Garcia, A. B., Engler, J., Iyer, S., Gerats, T., Van Montagu, M., and Caplan, A. B. (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 115, 159-169
3. Vogel, G., Fiehn, O., Jean-Richard-dit-Bressel, L., Boller, T., Wiemken, A., Aeschbacher, R. A., and Wingler, A. (2001) Trehalose metabolism in Arabidopsis: occurrence of trehalose and molecular cloning and characterization of trehalose-6-phosphate synthase homologues. J. Exp. Bot. 52, 1817-1826
4. Adams, R. P., Kendall, E., and Kartha, K. K. (1990) Comparison of free sugars in growing desiccated plants of Selaginella-Lepidophylla. Biochem. Syst. Ecol. 18, 107-110
5. Gomez, L. D., Baud, S., and Graham, I. A. (2005) The role of trehalose-6-phosphate synthase in Arabidopsis embryo development. Biochem. Soc. Trans. 33, 280-282
6. van Dijken, A. J., Schluepmann, H., and Smeekens, S. C. (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969-977
7. 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
8. Eastmond, P. J., Li, Y., and Graham, I. A. (2003) Is trehalose-6-phosphate a regulator of sugar metabolism in plants? J. Exp. Bot. 54, 533-537
9. Thimm, O., Biasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, 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
10. Leonhardt, N., Kwak, J. M., Robert, N., Waner, D., Leonhardt, G., and Schroeder, J. I. (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16, 596-615
11. Eastmond, P. J., van Dijken, A. J., Spielman, M., Kerr, A., Tissier, A. F., Dickinson, H. G., Jones, J. D., 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
12. Hrabak, E. M., Chan, C. W., Gribskov, M., Harper, J. F., Choi, J. H., Halford, N., Kudla, J., Luan, S., Nimmo, H. G., Sussman, M. R., Thomas, M., Walker-Simmons, K., Zhu, J. K., and Harmon, A. C. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132, 666-680
13. Bhalerao, R. P., Salchert, K., Bako, L., Okresz, L., Szabados, L., Muranaka, T., Machida, Y., Schell, J., and Koncz, C. (1999) Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl. Acad. Sci. U. S. A. 96, 5322-5327
14. McMichael, R. W., Jr., Bachmann, M., and Huber, S. C. (1995) Spinach leaf sucrose-phosphate synthase and nitrate reductase are phosphorylated/inactivated by multiple protein kinases in vitro. Plant Physiol. 108, 1077-1082
15. Bachmann, M., Shiraishi, N., Campbell, W. H., Yoo, B. C., Harmon, A. C., and Huber, S. C. (1996) Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8, 505-517
16. Toroser, D., McMichael, R., Krause, K. P., Kurreck, J., Sonnewald, U., Stitt, M., and Huber, S. C. (1999) Site-directed mutagenesis of serine 158 demonstrates its role in spinach leaf sucrose-phosphate synthase modulation. Plant J. 17, 407-413
17. Hardin, S. C., Winter, H., and Huber, S. C. (2004) Phosphorylation of the amino terminus of maize sucrose synthase in relation to membrane association and enzyme activity. Plant Physiol. 134, 1427-1438
18. 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
19. Romeis, T., Ludwig, A. A., Martin, R., and Jones, J. D. G. (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556-5567
20. Romeis, T. (2001) Protein kinases in the plant defence response. Curr. Opin. Plant Biol. 4, 407-414
21. Laurie, S., and Halford, N. G. (2001) The role of protein kinases in the regulation of plant growth and development. Plant Growth Regul. 34, 253-265
22. MacKintosh, C. (1998) Regulation of cytosolic enzymes in primary metabolism by reversible protein phosphorylation. Curr. Opin. Plant Biol. 1, 224-229
23. Toroser, D., and Huber, S. C. (1997) Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiol. 114, 947-955
24. Shao, J., and Harmon, A. C. (2003) In vivo phosphorylation of a recombinant peptide substrate of CDPK suggests involvement of CDPK in plant stress responses. Plant Mol. Biol. 53, 691-700
25. Hubbard, M. J., and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172-177
26. Cohen, P. (2000) The regulation of protein function by multisite phosphorylation - a 25 year update. Trends Biochem. Sci. 25, 596-601
27. Zolnierowicz, S., and Bollen, M. (2000) Protein phosphorylation and protein phosphatases. De Panne, Belgium, September 19-24, 1999. EMBO J. 19, 483-488
28. Kerk, D., Bulgrien, J., Smith, D. W., Barsam, B., Veretnik, S., and Gribskov, M. (2002) The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol. 129, 908-925
29. Initiative, T. A. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815
30. Sugden, C., Donaghy, P. G., Halford, N. G., and Hardie, D. G. (1999) Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol. 120, 257-274
31. 2+ ions. Biochem. J. 325, 101-109
32. Huber, S. C., and Huber, J. L. (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 431-444
33. Thelander, M., Olsson, T., and Ronne, H. (2004) Snf1-related protein kinase 1 is needed for growth in a normal day-night light cycle. EMBO J. 23, 1900-1910
34. Zhang, Y., Shewry, P. R., Jones, H., Barcelo, P., Lazzeri, P. A., and Halford, N. G. (2001) Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J. 28, 431-441
35. Halford, N. G., Hey, S., Jhurreea, D., Laurie, S., McKibbin, R. S., Paul, M., and Zhang, Y. (2003) Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J. Exp. Bot. 54, 467-475
36. Toroser, D., Plaut, Z., and Huber, S. C. (2000) Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol. 123, 403-412
37. Annan, R. S., and Carr, S. A. (1997) The essential role of mass spectrometry in characterizing protein structure: mapping posttranslational modifications. J. Protein Chem. 16, 391-402
38. Neubauer, G., and Mann, M. (1999) Mapping of phosphorylation sites of gel-isolated proteins by nanoelectrospray tandem mass spectrometry: potentials and limitations. Anal. Chem. 71, 235-242
39. Steen, H., Kuster, B., and Mann, M. (2001) Quadrupole time-of-flight versus triple-quadrupole mass spectrometry for the determination of phosphopeptides by precursor ion scanning. J. Mass Spectrom. 36, 782-790
40. Schlosser, A., Pipkorn, R., Bossemeyer, D., and Lehmann, W. D. (2001) Analysis of protein phosphorylation by a combination of elastase digestion and neutral loss tandem mass spectrometry. Anal. Chem. 73, 170-176
41. DeGnore, J. P., and Qin, J. (1998) Fragmentation of phosphopeptides in an ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 9, 1175-1188
42. Glinski, M., Romeis, T., Witte, C. P., Wienkoop, S., and Weckwerth, W. (2003) Stable isotope labeling of phosphopeptides for multilparallel kinase target analysis and identification of phosphorylation sites. Rapid Commun. Mass Spectrom. 17, 1579-1584
43. Mann, M., Ong, S. E., Gronborg, M., Steen, H., Jensen, O. N., and Pandey, A. (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20, 261-268
44. Kratzer, R., Eckerskom, C., Karas, M., and Lottspeich, F. (1998) Suppression effects in enzymatic peptide ladder sequencing using ultraviolet-matrix assisted law desorption/ionization-mass spectrometry. Electrophoresis 19, 1910-1919
45. Bradford, M. M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248-254
46. Matuszewski, B. K., Constanzer, M. L., and Chavez-Eng, C. M. (2003) Strategies for the assessment of matrix effect in quantitative bioanalytical methods based on HPLC-MS/MS. Anal. Chem. 75, 3019-3030
47. Halford, N. G., and Hardie, D. G. (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol. Biol. 37, 735-748
48. Kang, Y. K., Jhon, J. S., and Han, S. J. (1999) Conformational study of Ac-Xaa-Pro-NHMe dipeptides: proline puckering and trans/cis imide bond. J. Pept. Res. 53, 30-40