Abstract
We have assembled a reliable phosphoproteomic data set for budding yeast Saccharomyces cerevisiae and have investigated its properties. Twelve publicly available phosphoproteome data sets were triaged to obtain a subset of high-confidence phosphorylation sites (p-sites), free of “noisy” phosphorylations. Analysis of this combined data set suggests that the inventory of phosphoproteins in yeast is close to completion, but that these proteins may have many undiscovered p-sites. Proteins involved in budding and protein kinase activity have high numbers of p-sites and are highly over-represented in the vast majority of the yeast phosphoproteome data sets. The yeast phosphoproteome is characterized by a few proteins with many p-sites and many proteins with a few p-sites. We confirm a tendency for p-sites to cluster together and find evidence that kinases may phosphorylate off-target amino acids that are within one or two residues of their cognate target. This suggests that the precise position of the phosphorylated amino acid is not a stringent requirement for regulatory fidelity. Compared with nonphosphorylated proteins, phosphoproteins are more ancient, more abundant, have longer unstructured regions, have more genetic interactions, more protein interactions, and are under tighter post-translational regulation. It appears that phosphoproteins constitute the raw material for pathway rewiring and adaptation at various evolutionary rates.
Highlights
The overlap observed between any two experiments is always statistically significant, whether it is for p-sites or the phosphoproteins identified
By using a published data set of yeast orthologous groups [45] that was based on phylogenetic analysis and chromosomal synteny from YGOB [46], we identified orthologs in the genomes of nine other fungi and observed that a higher fraction of S. cerevisiae phosphoproteins have orthologs in other fungal genomes than do nonphosphorylated proteins
We have provided a high quality data set of p-sites, which may be employed to study the general properties of the yeast phosphoproteome
Summary
Twelve high-throughput experiments between the years 2005 and 2009 were merged in the 12HQ data set (where HQ stands for high quality). These experiments were performed with yeast cells in a variety of physiological and developmental states, including mating, exponential growth, different phases of the cell cycle and challenged by DNA-damaging agents, osmotic stress, rapamycin, or cycloheximide. To ensure the high quality of the combined phosphoproteome data set, we required that phosphopeptides were correctly identified with a probability of Ն99%, and that p-sites were correctly localized with dium of the 12 data sets; 12HQ_3X, high-quality compendium of the 12 data sets with p-sites found in at least 3 or more experiments; ID, intrinsic disorder; GO, Gene ontology
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