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Open Access Highly Accessed Research article

The reduced kinome of Ostreococcus tauri: core eukaryotic signalling components in a tractable model species

Matthew M Hindle14, Sarah F Martin12, Zeenat B Noordally12, Gerben van Ooijen12, Martin E Barrios-Llerena12, T Ian Simpson34, Thierry Le Bihan12 and Andrew J Millar12*

Author Affiliations

1 SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JD, UK

2 Institute of Structural and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JR, UK

3 Biomathematics & Statistics Scotland, University of Edinburgh, Edinburgh EH9 3JZ, UK

4 Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh EH8 9AB, UK

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BMC Genomics 2014, 15:640  doi:10.1186/1471-2164-15-640

Published: 2 August 2014

Abstract

Background

The current knowledge of eukaryote signalling originates from phenotypically diverse organisms. There is a pressing need to identify conserved signalling components among eukaryotes, which will lead to the transfer of knowledge across kingdoms. Two useful properties of a eukaryote model for signalling are (1) reduced signalling complexity, and (2) conservation of signalling components. The alga Ostreococcus tauri is described as the smallest free-living eukaryote. With less than 8,000 genes, it represents a highly constrained genomic palette.

Results

Our survey revealed 133 protein kinases and 34 protein phosphatases (1.7% and 0.4% of the proteome). We conducted phosphoproteomic experiments and constructed domain structures and phylogenies for the catalytic protein-kinases. For each of the major kinases families we review the completeness and divergence of O. tauri representatives in comparison to the well-studied kinomes of the laboratory models Arabidopsis thaliana and Saccharomyces cerevisiae, and of Homo sapiens. Many kinase clades in O. tauri were reduced to a single member, in preference to the loss of family diversity, whereas TKL and ABC1 clades were expanded. We also identified kinases that have been lost in A. thaliana but retained in O. tauri. For three, contrasting eukaryotic pathways – TOR, MAPK, and the circadian clock – we established the subset of conserved components and demonstrate conserved sites of substrate phosphorylation and kinase motifs.

Conclusions

We conclude that O. tauri satisfies our two central requirements. Several of its kinases are more closely related to H. sapiens orthologs than S. cerevisiae is to H. sapiens. The greatly reduced kinome of O. tauri is therefore a suitable model for signalling in free-living eukaryotes.

Keywords:
Conserved eukaryote signalling; Protein kinase phylogeny; Ostreococcus tauri; Model kinome; Phosphorylation; TOR signalling; MAPK cascade; Circadian clock