Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation

Plant, Cell and Environment

Volumn 29, Issue 8, 2006, Pages 1606-1617

  Röhrig, Horst ^a   Schmidt, Jürgen ^b   Colby, Thomas ^b   Bräutigam, Anne ^b   Hufnagel, Peter ^c   Bartels, Dorothea ^a  

^a UNIVERSITY OF BONN   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c BRUKER DALTONIK GMBH   (Germany)

Author keywords

Coiled coil domains; Desiccation tolerance; LEA proteins; Phosphorylation site mapping

Indexed keywords

LATE EMBRYOGENESIS ABUNDANT PROTEIN, PLANT; VEGETABLE PROTEIN; WATER;

ABSCISIC ACID; DEHYDRATION; KINETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PLANT; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CRATEROSTIGMA; DESICCATION; DIMERIZATION; GENETICS; KINETICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHOSPHORYLATION; PROTEIN MOTIF; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CHROMATOGRAPHY, LIQUID; CRATEROSTIGMA; DESICCATION; DIMERIZATION; KINETICS; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHOSPHORYLATION; PLANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; WATER;

CRATEROSTIGMA; CRATEROSTIGMA PLANTAGINEUM; SELAGINELLA PILIFERA;

EID: 33748489098     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2006.01537.x     Document Type: Article

References (41)

1. Alsheikh M.K., Heyen B.J. & Randall S.K. (2003) Ion-binding properties of the dehydrin ERD14 are dependent upon phosphorylation. Journal of Biological Chemistry 278, 40882-40889.
2. Alsheikh M.K., Svensson J.T. & Randall S.K. (2005) Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant, Cell & Environment 28, 1114-1122.
3. Bartels D. (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integrative and Comparative Biology 45, 696-701.
4. Bartels D. & Salamini F. (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiology 127, 1346-1353.
5. Bartels D. & Sunkar R. (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23-58.
6. Bernacchia G., Schwall G., Lottspeich F., Salamini F. & Bartels D. (1995) The transketolase gene family of the resurrection plant Craterostigma plantagineum: differential expression during the rehydration phase. EMBO Journal 14, 610-618.
7. Close T.J. (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiologia Plantarum 97, 795-803.
8. Cuming A. (1999) LEA proteins. In Seed Proteins (eds P.R. Shewry & R. Casey) pp. 753-780. Kluwer Academic Publisher, Dordrecht, the Netherlands.
9. Fengfeng Z., Yu X., Guoliang C. & Xuebiao Y. (2004) GPS: a novel group-based phosphorylation predicting and scoring method. Biochemical and Biophysical Research Communications 325, 1443-1448.
10. Gaff D.F. (1971) Desiccation-tolerant flowering plants in Southern Africa. Science 174, 1033-1034.
11. Goday A., Sánchez-Martínez D., Gómez J., Puigdomènech P. & Pagès M. (1988) Gene expression in developing Zea mays embryos. Regulation by abscisic acid of a highly phosphorylated 23- to 25-kD group of proteins. Plant Physiology 88, 564-569.
12. Goday A., Jensen A.B., Culianez-Macià F.B., Albà M.M., Figueras M., Serratosa J., Torrent M. & Pagès M. (1994) The maize abscisic acid-responsive protein Rab17 is located in the nucleus and interacts with nuclear localization signals. Plant Cell 6, 351-360.
13. Goyal K., Tisi L., Basran A., Browne J., Burnell A., Zurdo J. & Tunnacliffe A. (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. Journal of Biological Chemistry 278, 12977-12984.
14. Goyal K., Walton L.J. & Tunnacliffe A. (2005) LEA proteins prevent protein aggregation due to water stress. Biochemical Journal 388, 151-157.
15. Guermeur Y., Geourjon C., Gallinari P. & Deleage G. (1999) Improved performance in protein secondary structure prediction by inhomogeneous score combination. Bioinformatics 15, 413-421.
16. Guy C.L. & Haskell D. (1989) Preliminary characterization of high molecular mass proteins associated with cold acclimation in spinach. Plant Physiology and Biochemistry 27, 777-784.
17. Heyen B.J., Alsheikh M.K., Smith E.A., Torvik C.F., Seals D.F. & Randall S.K. (2002) The calcium-binding activity of a vacuole-associated, dehydrin like activity is regulated by phosphorylation. Plant Physiology 47, 675-687.
18. Huber S.C. & Hardin S.C. (2004) Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Current Opinion in Plant Biology 7, 319-322.
19. Jiang X. & Wang Y. (2004) β-elimination coupled with tandem mass spectrometry for the identification of in vivo and in vitro phosphorylation sites in maize dehydrin DHN1 protein. Biochemistry 43, 15567-15576.
20. John M., Schmidt J., Wieneke U., Kondorosi E., Kondorosi A. & Schell J. (1985) Expression of the nodulation gene nod C of Rhizobium meliloti in Escherichia coli: role of the nod C gene product in nodulation. EMBO Journal 4, 2425-2430.
21. Kaye C., Neven L., Hofig A., Li Q.B., Haskell D. & Guy C. (1998) Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. Plant Physiology 116, 1367-1377.
22. Kruger C., Berkowitz O., Stephan U.W. & Hell R. (2002) A metal-binding member of the late embryogenesis abundant protein family transports iron into the phloem of Ricinus communis L. Journal of Biological Chemistry 277, 25062-25069.
23. Laemmli (1970) Cleavage of structural proteins during the assembly of the head of maize bacteriophage T4. Nature 227, 680-685.
24. Liang W., Warrick H.M. & Spudich J.A. (1999) A structural model for phosphorylation control of Dictyostelium myosin II thick filament assembly. Journal of Cell Biology 147, 1039-1048.
25. Lisse T., Bartels D., Kalbitzer H.R. & Jaenicke R. (1996) The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biological Chemistry 377, 555-561.
26. Makrantoni V., Antrobus R., Botting C.H. & Coote P.J. (2005) Rapid enrichment and analysis of yeast phosphoproteins using affinity chromatography, 2D-PAGE and peptide mass fingerprinting. Yeast 22, 401-414.
27. Mason J.M. & Arndt K.M. (2004) Coiled coil domains: stability, specificity, and biological implications. Chembiochem 5, 170-176.
28. Meggio F., Marin O. & Pinna L.A. (1994) Substrate specificity of protein kinase CK2. Cellular and Molecular Biology Research 40, 401-409.
29. Metodiev M.V., Timanova A. & Stone D.E. (2004) Differential phosphoproteome profiling by affinity capture and tandem matrix-assisted laser desorption/ionization mass spectrometry. Proteomics 4, 1433-1438.
30. Pawson T. & Scott J.D. (2005) Protein phosphorylation in signaling - 50 years and counting. Trends in Biochemical Sciences 30, 286-290.
31. Reyes J.L., Rodrigo M.-J., Colmenero-Flores J.M., Gil J.-V., Garay-Arroyo A., Campos F., Salamini F., Bartels D. & Covarrubias A.A. (2005) Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant, Cell & Environment 28, 709-718.
32. Riera M., Figueras M., López C., Goday A. & Pagès M. (2004) Protein kinase CK2 modulates developmental functions of the abscisic acid responsive protein Rab17 from maize. Proceedings of the National Academy of Sciences of the USA 101, 9879-9884.
33. Saavedra L., Svensson J., Carballo V., Izmendi D., Welin B. & Vidal S. (2006) A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant Journal 45, 237-249.
34. Schneider K., Wells B., Schmelzer E., Salamini F. & Bartels D. (1993) Desiccation leads to a rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum. Planta 189, 120-131.
35. Shevchenko A., Wilm M., Vorm O. & Mann M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Analytical Chemistry 68, 850-858.
36. Steinmetz M.O., Jahnke W., Towbin H., García-Echeverría C., Voshol H., Müller D. & van Oostrum J. (2001) Phosphorylation disrupts the central helix in Op18/stathmin and suppresses binding to tubulin. EMBO Reports 2, 505-510.
37. Svensson J., Ismail A.M., Palva E.T. & Close T.J. (2002) Dehydrins. In Cell and Molecular Responses to Stress: Sensing, Signaling and Cell Adaption (eds K.B. Storey & J. M. Storey) pp. 155-171. Elsevier Press, Amsterdam, the Netherlands.
38. Towbin H., Staehelin T. & Gordon J. (1979) Electrophoretic transfer of proteins to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the USA 76, 4350-4354.
39. Velasco R., Salamini F. & Bartels D. (1998) Gene structure and expression analysis of the drought-induced and abscisic acid-responsive CDeT11-24 gene family from the resurrection plant Craterostigma plantagineum Hochst. Planta 204, 459-471.
40. Wang W., Scali M., Vignani R., Spadafora A., Sensi E., Mazzuca S. & Cresti M. (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24, 2369-2375.
41. Wise M.J. & Tunnacliffe A. (2004) POPP the question: what do LEA proteins do? Trends in Plant Science 9, 13-17.