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Sci. Signal., 1 May 2012
Vol. 5, Issue 222, p. ra35
[DOI: 10.1126/scisignal.2002733]

RESEARCH ARTICLES

Genomic Survey of Premetazoans Shows Deep Conservation of Cytoplasmic Tyrosine Kinases and Multiple Radiations of Receptor Tyrosine Kinases

Hiroshi Suga1,2*, Michael Dacre3, Alex de Mendoza1,2, Kamran Shalchian-Tabrizi4, Gerard Manning3*, and Iñaki Ruiz-Trillo1,2,5*

1 Institut de Biologia Evolutiva (UPF-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
2 Departament de Genètica, Universitat de Barcelona, 08024 Barcelona, Spain.
3 Razavi Newman Center for Bioinformatics, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
4 Microbial Evolution Research Group, Department of Biology, University of Oslo, 0316 Oslo, Norway.
5 Institució Catalana per a la Recerca i Estudis Avançats, 08010 Barcelona, Spain.

Abstract: The evolution of multicellular metazoans from a unicellular ancestor is one of the most important advances in the history of life. Protein tyrosine kinases play important roles in cell-to-cell communication, cell adhesion, and differentiation in metazoans; thus, elucidating their origins and early evolution is crucial for understanding the origin of metazoans. Although tyrosine kinases exist in choanoflagellates, few data are available about their existence in other premetazoan lineages. To unravel the origin of tyrosine kinases, we performed a genomic and polymerase chain reaction (PCR)–based survey of the genes that encode tyrosine kinases in the two described filasterean species, Capsaspora owczarzaki and Ministeria vibrans, the closest relatives to the Metazoa and Choanoflagellata clades. We present 103 tyrosine kinase–encoding genes identified in the whole genome sequence of C. owczarzaki and 15 tyrosine kinase–encoding genes cloned by PCR from M. vibrans. Through detailed phylogenetic analysis, comparison of the organizations of the protein domains, and resequencing and revision of tyrosine kinase sequences previously found in some whole genome sequences, we demonstrate that the basic repertoire of metazoan cytoplasmic tyrosine kinases was established before the divergence of filastereans from the Metazoa and Choanoflagellata clades. In contrast, the receptor tyrosine kinases diversified extensively in each of the filasterean, choanoflagellate, and metazoan clades. This difference in the divergence patterns between cytoplasmic tyrosine kinases and receptor tyrosine kinases suggests that receptor tyrosine kinases that had been used for receiving environmental cues were subsequently recruited as a communication tool between cells at the onset of metazoan multicellularity.

* To whom correspondence should be addressed. E-mail: hiroshi.suga{at}ibe.upf-csic.es (H.S.); manning{at}manninglab.org (G.M.); inaki.ruiz{at}icrea.es (I.R.-T.)

Citation: H. Suga, M. Dacre, A. de Mendoza, K. Shalchian-Tabrizi, G. Manning, I. Ruiz-Trillo, Genomic Survey of Premetazoans Shows Deep Conservation of Cytoplasmic Tyrosine Kinases and Multiple Radiations of Receptor Tyrosine Kinases. Sci. Signal. 5, ra35 (2012).

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