Evolution of the SH3 domain specificity landscape in yeasts

Verschueren, Erik; Spiess, Matthias; Gkourtsa, Areti; Avula, Teja; Landgraf, Christiane; Tapia Mancilla, Victor; Huber, Aline; Volkmer, Rudolf; Winsor, Barbara; Serrano Pubull, Luis, 1982-; Hochstenbach, Frans; Distel, Ben

Evolution of the SH3 domain specificity landscape in yeasts

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dc.contributor.author Verschueren, Erikca
dc.contributor.author Spiess, Matthiasca
dc.contributor.author Gkourtsa, Aretica
dc.contributor.author Avula, Tejaca
dc.contributor.author Landgraf, Christianeca
dc.contributor.author Tapia Mancilla, Victorca
dc.contributor.author Huber, Alineca
dc.contributor.author Volkmer, Rudolfca
dc.contributor.author Winsor, Barbaraca
dc.contributor.author Serrano Pubull, Luis, 1982-ca
dc.contributor.author Hochstenbach, Fransca
dc.contributor.author Distel, Benca
dc.date.accessioned 2015-11-19T14:18:51Z
dc.date.available 2015-11-19T14:18:51Z
dc.date.issued 2015
dc.description.abstract To explore the conservation of Src homology 3 (SH3) domain-mediated networks in evolution, we compared the specificity landscape of these domains among four yeast species, Saccharomyces cerevisiae, Ashbya gossypii, Candida albicans, and Schizosaccharomyces pombe, encompassing 400 million years of evolution. We first aligned and catalogued the families of SH3-containing proteins in these four species to determine the relationships between homologous domains. Then, we tagged and purified all soluble SH3 domains (82 in total) to perform a quantitative peptide assay (SPOT) for each SH3 domain. All SPOT readouts were hierarchically clustered and we observed that the organization of the SH3 specificity landscape in three distinct profile classes remains conserved across these four yeast species. We also produced a specificity profile for each SH3 domain from manually aligned top SPOT hits and compared the within-family binding motif consensus. This analysis revealed a striking example of binding motif divergence in a C. albicans Rvs167 paralog, which cannot be explained by overall SH3 sequence or interface residue divergence, and we validated this specificity change with a yeast two-hybrid (Y2H) assay. In addition, we show that position-weighted matrices (PWM) compiled from SPOT assays can be used for binding motif screening in potential binding partners and present cases where motifs are either conserved or lost among homologous SH3 interacting proteins. Finally, by comparing pairwise SH3 sequence identity to binding profile correlation we show that for 75% of all analyzed families the SH3 specificity profile was remarkably conserved over a large evolutionary distance. Thus, a high sequence identity within an SH3 domain family predicts conserved binding specificity, whereas divergence in sequence identity often coincided with a change in binding specificity within this family. As such, our results are important for future studies aimed at unraveling complex specificity networks of peptide recognition domains in higher eukaryotes, including mammals.ca
dc.description.sponsorship LS, BW, FH and BD received funding from the European Union (Marie Curie Research Training Network Penelope; MRTN-CT-2006-036076).
dc.format.mimetype application/pdfca
dc.identifier.citation Verschueren E, Spiess M, Gkourtsa A, Avula T, Landgraf C, Mancilla VT et al. Evolution of the SH3 domain specificity landscape in yeasts. PLoS ONE. 2015; 10(6): e129229. DOI 10.1371/journal.pone.0129229ca
dc.identifier.doi http://dx.doi.org/10.1371/journal.pone.0129229
dc.identifier.issn 1932-6203
dc.identifier.uri http://hdl.handle.net/10230/25157
dc.language.iso engca
dc.publisher Public Library of Science (PLoS)ca
dc.relation.ispartof PLoS ONE. 2015; 10(6): e129229
dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/036076
dc.rights © 2015 Verschueren et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.ca
dc.rights.accessRights info:eu-repo/semantics/openAccessca
dc.rights.uri http://creativecommons.org/licenses/by/4.0/ca
dc.subject.other Llevats -- Genètica
dc.subject.other Saccharomyces cerevisiae
dc.title Evolution of the SH3 domain specificity landscape in yeastsca
dc.type info:eu-repo/semantics/articleca
dc.type.version info:eu-repo/semantics/publishedVersionca

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