Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Science Signaling - Call for Papers

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Logo for

PLANT CELL 16 (9): 2394-2405

Copyright © 2004 by the American Society of Plant Physiologists.

Phosphoproteomics of the Arabidopsis Plasma Membrane and a New Phosphorylation Site Database{fx1}

Thomas S. Nühsea, Allan Stensballeb, Ole N. Jensenb, and Scott C. Pecka,1

a Sainsbury Laboratory, John Innes Centre, Norwich NR4 7UH, United Kingdom
b Department of Biochemistry and Molecular Biology, University of Southern Denmark, DK-5230 Odense M, Denmark

1 To whom correspondence should be addressed. E-mail scott.peck{at}sainsbury-laboratory.ac.uk; fax 44-01603-450011.

Abstract: Functional genomic technologies are generating vast amounts of data describing the presence of transcripts or proteins in plant cells. Together with classical genetics, these approaches broaden our understanding of the gene products required for specific responses. Looking to the future, the focus of research must shift to the dynamic aspects of biology: molecular mechanisms of function and regulation. Phosphorylation is a key regulatory factor in all aspects of plant biology; but it is difficult, if not impossible, for most researchers to identify in vivo phosphorylation sites within their proteins of interest. We have developed a large-scale strategy for the isolation of phosphopeptides and identification by mass spectrometry (Nühse et al., 2003b). Here, we describe the identification of more than 300 phosphorylation sites from Arabidopsis thaliana plasma membrane proteins. These data will be a valuable resource for many fields of plant biology and overcome a major impediment to the elucidation of signal transduction pathways. We present an analysis of the characteristics of phosphorylation sites, their conservation among orthologs and paralogs, and the existence of putative motifs surrounding the sites. These analyses yield general principles for predicting other phosphorylation sites in plants and provide indications of specificity determinants for responsible kinases. In addition, more than 50 sites were mapped on receptor-like kinases and revealed an unexpected complexity of regulation. Finally, the data also provide empirical evidence on the topology of transmembrane proteins. This information indicates that prediction programs incorrectly identified the cytosolic portion of the protein in 25% of the transmembrane proteins found in this study. All data are deposited in a new searchable database for plant phosphorylation sites maintained by PlantsP (http://plantsp.sdsc.edu) that will be updated as the project expands to encompass additional tissues and organelles.

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Multiple Phosphorylations in the C-terminal Tail of Plant Plasma Membrane Aquaporins: Role in Subcellular Trafficking of AtPIP2;1 in Response to Salt Stress.
S. Prak, S. Hem, J. Boudet, G. Viennois, N. Sommerer, M. Rossignol, C. Maurel, and V. Santoni (2008)
Mol. Cell. Proteomics 7, 1019-1030
   Abstract »    Full Text »    PDF »
Nano Scale Proteomics Revealed the Presence of Regulatory Proteins Including Three FT-Like proteins in Phloem and Xylem Saps from Rice.
T. Aki, M. Shigyo, R. Nakano, T. Yoneyama, and S. Yanagisawa (2008)
Plant Cell Physiol. 49, 767-790
   Abstract »    Full Text »    PDF »
An Arabidopsis Protein Phosphorylated in Response to Microbial Elicitation, AtPHOS32, Is a Substrate of MAP Kinases 3 and 6.
G. Merkouropoulos, E. Andreasson, D. Hess, T. Boller, and S. C. Peck (2008)
J. Biol. Chem. 283, 10493-10499
   Abstract »    Full Text »    PDF »
The Phosphoproteome of a Chlamydomonas reinhardtii Eyespot Fraction Includes Key Proteins of the Light Signaling Pathway.
V. Wagner, K. Ullmann, A. Mollwo, M. Kaminski, M. Mittag, and G. Kreimer (2008)
Plant Physiology 146, 772-788
   Abstract »    Full Text »    PDF »
PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor.
J. L. Heazlewood, P. Durek, J. Hummel, J. Selbig, W. Weckwerth, D. Walther, and W. X. Schulze (2008)
Nucleic Acids Res. 36, D1015-D1021
   Abstract »    Full Text »    PDF »
Highly Efficient Phosphopeptide Enrichment by Calcium Phosphate Precipitation Combined with Subsequent IMAC Enrichment.
X. Zhang, J. Ye, O. N. Jensen, and P. Roepstorff (2007)
Mol. Cell. Proteomics 6, 2032-2042
   Abstract »    Full Text »    PDF »
Temporal Analysis of Sucrose-induced Phosphorylation Changes in Plasma Membrane Proteins of Arabidopsis.
T. Niittyla, A. T. Fuglsang, M. G. Palmgren, W. B. Frommer, and W. X. Schulze (2007)
Mol. Cell. Proteomics 6, 1711-1726
   Abstract »    Full Text »    PDF »
The FERONIA Receptor-like Kinase Mediates Male-Female Interactions During Pollen Tube Reception.
J.-M. Escobar-Restrepo, N. Huck, S. Kessler, V. Gagliardini, J. Gheyselinck, W.-C. Yang, and U. Grossniklaus (2007)
Science 317, 656-660
   Abstract »    Full Text »    PDF »
Regulation of Phototropic Signaling in Arabidopsis via Phosphorylation State Changes in the Phototropin 1-interacting Protein NPH3.
U. V. Pedmale and E. Liscum (2007)
J. Biol. Chem. 282, 19992-20001
   Abstract »    Full Text »    PDF »
Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis.
J. J. Benschop, S. Mohammed, M. O'Flaherty, A. J. R. Heck, M. Slijper, and F. L. H. Menke (2007)
Mol. Cell. Proteomics 6, 1198-1214
   Abstract »    Full Text »    PDF »
Arabidopsis Protein Kinase PKS5 Inhibits the Plasma Membrane H+-ATPase by Preventing Interaction with 14-3-3 Protein.
A. T. Fuglsang, Y. Guo, T. A. Cuin, Q. Qiu, C. Song, K. A. Kristiansen, K. Bych, A. Schulz, S. Shabala, K. S. Schumaker, et al. (2007)
PLANT CELL 19, 1617-1634
   Abstract »    Full Text »    PDF »
Receptor-like protein kinase HvLysMR1 of barley (Hordeum vulgare L.) is induced during leaf senescence and heavy metal stress.
A. Ouelhadj, M. Kaminski, M. Mittag, and K. Humbeck (2007)
J. Exp. Bot. 58, 1381-1396
   Abstract »    Full Text »    PDF »
Regulation of NH4+ Transport by Essential Cross Talk between AMT Monomers through the Carboxyl Tails.
B. Neuhauser, M. Dynowski, M. Mayer, and U. Ludewig (2007)
Plant Physiology 143, 1651-1659
   Abstract »    Full Text »    PDF »
Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry.
A. Chi, C. Huttenhower, L. Y. Geer, J. J. Coon, J. E. P. Syka, D. L. Bai, J. Shabanowitz, D. J. Burke, O. G. Troyanskaya, and D. F. Hunt (2007)
PNAS 104, 2193-2198
   Abstract »    Full Text »    PDF »
Interactions among PIN-FORMED and P-Glycoprotein Auxin Transporters in Arabidopsis.
J. J. Blakeslee, A. Bandyopadhyay, O. R. Lee, J. Mravec, B. Titapiwatanakun, M. Sauer, S. N. Makam, Y. Cheng, R. Bouchard, J. Adamec, et al. (2007)
PLANT CELL 19, 131-147
   Abstract »    Full Text »    PDF »
Large Scale Identification and Quantitative Profiling of Phosphoproteins Expressed during Seed Filling in Oilseed Rape.
G. K. Agrawal and J. J. Thelen (2006)
Mol. Cell. Proteomics 5, 2044-2059
   Abstract »    Full Text »    PDF »
Immunophilin-like TWISTED DWARF1 Modulates Auxin Efflux Activities of Arabidopsis P-glycoproteins.
R. Bouchard, A. Bailly, J. J. Blakeslee, S. C. Oehring, V. Vincenzetti, O. R. Lee, I. Paponov, K. Palme, S. Mancuso, A. S. Murphy, et al. (2006)
J. Biol. Chem. 281, 30603-30612
   Abstract »    Full Text »    PDF »
Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism.
S. de la Fuente van Bentem, D. Anrather, E. Roitinger, A. Djamei, T. Hufnagl, A. Barta, E. Csaszar, I. Dohnal, D. Lecourieux, and H. Hirt (2006)
Nucleic Acids Res. 34, 3267-3278
   Abstract »    Full Text »    PDF »
Phosphoproteomics in Arabidopsis: moving from empirical to predictive science.
S. C Peck (2006)
J. Exp. Bot. 57, 1523-1527
   Abstract »    Full Text »    PDF »
Arabidopsis thaliana proteomics: from proteome to genome.
S. Baginsky and W. Gruissem (2006)
J. Exp. Bot. 57, 1485-1491
   Abstract »    Full Text »    PDF »
Proteomics studies of post-translational modifications in plants.
S. J. Kwon, E. Y. Choi, Y. J. Choi, J. H. Ahn, and O. K Park (2006)
J. Exp. Bot. 57, 1547-1551
   Abstract »    Full Text »    PDF »
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis..
S. Robatzek, D. Chinchilla, and T. Boller (2006)
Genes & Dev. 20, 537-542
   Abstract »    Full Text »    PDF »
Arabidopsis PEN3/PDR8, an ATP Binding Cassette Transporter, Contributes to Nonhost Resistance to Inappropriate Pathogens That Enter by Direct Penetration.
M. Stein, J. Dittgen, C. Sanchez-Rodriguez, B.-H. Hou, A. Molina, P. Schulze-Lefert, V. Lipka, and S. Somerville (2006)
PLANT CELL 18, 731-746
   Abstract »    Full Text »    PDF »
Proteomics of Rac GTPase Signaling Reveals Its Predominant Role in Elicitor-Induced Defense Response of Cultured Rice Cells.
M. Fujiwara, K. Umemura, T. Kawasaki, and K. Shimamoto (2006)
Plant Physiology 140, 734-745
   Abstract »    Full Text »    PDF »
Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics.
W. Majeran, Y. Cai, Q. Sun, and K. J. van Wijk (2005)
PLANT CELL 17, 3111-3140
   Abstract »    Full Text »    PDF »
Rapid Phosphorylation of a Syntaxin during the Avr9/Cf-9-Race-Specific Signaling Pathway.
A. Heese, A. A. Ludwig, and J. D.G. Jones (2005)
Plant Physiology 138, 2406-2416
   Abstract »    Full Text »    PDF »
Prospects and Challenges in Proteomics.
P. Bertone and M. Snyder (2005)
Plant Physiology 138, 560-562
   Full Text »    PDF »
Update on Proteomics in Arabidopsis. Where Do We Go From Here?.
S. C. Peck (2005)
Plant Physiology 138, 591-599
   Full Text »    PDF »
Identification and Functional Analysis of in Vivo Phosphorylation Sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 Receptor Kinase.
X. Wang, M. B. Goshe, E. J. Soderblom, B. S. Phinney, J. A. Kuchar, J. Li, T. Asami, S. Yoshida, S. C. Huber, and S. D. Clouse (2005)
PLANT CELL 17, 1685-1703
   Abstract »    Full Text »    PDF »
Regulation of Plant Symbiosis Receptor Kinase through Serine and Threonine Phosphorylation.
S. Yoshida and M. Parniske (2005)
J. Biol. Chem. 280, 9203-9209
   Abstract »    Full Text »    PDF »
Quantitative Phosphoproteomics Applied to the Yeast Pheromone Signaling Pathway.
A. Gruhler, J. V. Olsen, S. Mohammed, P. Mortensen, N. J. Faergeman, M. Mann, and O. N. Jensen (2005)
Mol. Cell. Proteomics 4, 310-327
   Abstract »    Full Text »    PDF »

ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (pre-2008: Science's STKE. ISSN 1525-8882)