Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis

J Proteome Res. 2008 Jun;7(6):2458-70. doi: 10.1021/pr8000173. Epub 2008 Apr 24.

Abstract

An estimated one-third of all proteins in higher eukaryotes are regulated by phosphorylation by protein kinases (PKs). Although plant genomes encode more than 1000 PKs, the substrates of only a small fraction of these kinases are known. By mass spectrometry of peptides from cytoplasmic- and nuclear-enriched fractions, we determined 303 in vivo phosphorylation sites in Arabidopsis proteins. Among 21 different PKs, 12 were phosphorylated in their activation loops, suggesting that they were in their active state. Immunoblotting and mutational analysis confirmed a tyrosine phosphorylation site in the activation loop of a GSK3/shaggy-like kinase. Analysis of phosphorylation motifs in the substrates suggested links between several of these PKs and many target sites. To perform quantitative phosphorylation analysis, peptide arrays were generated with peptides corresponding to in vivo phosphorylation sites. These peptide chips were used for kinome profiling of subcellular fractions as well as H 2O 2-treated Arabidopsis cells. Different peptide phosphorylation profiles indicated the presence of overlapping but distinct PK activities in cytosolic and nuclear compartments. Among different H 2O 2-induced PK targets, a peptide of the serine/arginine-rich (SR) splicing factor SCL30 was most strongly affected. SRPK4 (SR protein-specific kinase 4) and MAPKs (mitogen-activated PKs) were found to phosphorylate this peptide, as well as full-length SCL30. However, whereas SRPK4 was constitutively active, MAPKs were activated by H 2O 2. These results suggest that SCL30 is targeted by different PKs. Together, our data demonstrate that a combination of mass spectrometry with peptide chip phosphorylation profiling has a great potential to unravel phosphoproteome dynamics and to identify PK substrates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Arabidopsis / cytology
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / metabolism*
  • Argonaute Proteins
  • Cells, Cultured
  • Cyclin-Dependent Kinases / chemistry
  • Cyclin-Dependent Kinases / metabolism
  • GTPase-Activating Proteins / chemistry
  • GTPase-Activating Proteins / metabolism
  • Glycogen Synthase Kinase 3 / chemistry
  • Glycogen Synthase Kinase 3 / metabolism
  • Hydrogen Peroxide / pharmacology
  • Mass Spectrometry / methods*
  • Mitogen-Activated Protein Kinases / metabolism
  • Molecular Sequence Data
  • Myelin Basic Protein / chemistry
  • Myelin Basic Protein / metabolism
  • Peptides / chemistry
  • Peptides / metabolism
  • Phosphoproteins / metabolism*
  • Phosphorylases / chemistry
  • Phosphorylases / metabolism
  • Phosphorylation / drug effects
  • Protein Array Analysis / methods*
  • Protein Kinases / chemistry
  • Protein Kinases / metabolism
  • Proteomics / methods

Substances

  • AGO1 protein, Arabidopsis
  • Arabidopsis Proteins
  • Argonaute Proteins
  • GTPase-Activating Proteins
  • Myelin Basic Protein
  • Peptides
  • Phosphoproteins
  • topless protein, Arabidopsis
  • Hydrogen Peroxide
  • Phosphorylases
  • Protein Kinases
  • Cyclin-Dependent Kinases
  • Mitogen-Activated Protein Kinases
  • ATSK11 protein, Arabidopsis
  • Glycogen Synthase Kinase 3