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MBE Advance Access published online on December 14, 2006

Molecular Biology and Evolution, doi:10.1093/molbev/msl197
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Evidence of Interaction Network Evolution by Whole Genome Duplications: a Case-study in MADS-box Proteins

Amelie Veron{ddagger},*, Kerstin Kaufmann{dagger} and Erich Bornberg-Bauer{ddagger}

{ddagger} Division of Bioinformatics, Institute for Evolution and Biodiversity, The Westphalian Wilhelms University of Münster, Germany
{dagger} Business Unit Bioscience, Plant Research International, Wageningen, The Netherlands

* Corresponding Author Address: Division of Bioinformatics, The Westfalian Wilhelms University of Münster, Institute for Evolution and Biodiversity, Schlossplatz 4, D48149 Münster / Germany, Telephone: +49-(0)251-83-21635, Fax: +49-(0)251-83-21631, e-mail address: averon{at}uni-muenster.de

Accepted for publication December 5, 2006.

Recent investigations on metazoan transcription factors (TF) indicate that single gene duplication events and the gain and loss of protein domains are two crucial factors in shaping their protein-protein interaction networks. Plant genomes, on the other hand, have a history of polyploidy and whole genome duplications, thus their study helps to understand whether whole genome duplications have also had a significant influence on protein network evolution. Here we investigate the evolution of the interaction network in the well studied MADS-domain MIKC-type proteins, a TF family which plays an important role in both the vegetative and the reproductive phases of plant life. We combine phylogenetic reconstruction, protein domain analysis and interaction data from different species. We show that, unlike previously analysed interaction networks, the MIKC-type protein network displays a characteristic topology, with overall high inter-subfamily connectivity, shared interactors between paralogs, and conservation of interaction patterns across species. The evaluation of the number of MIKC-type proteins at key time points throughout the evolution of land plants in the lineage leading to Arabidopsis suggested that most duplicates were retained after each round of whole genome duplication. We provide evidence that an initial network, formed by nine to eleven homodimerizing proteins interacting with each other, existed in the common ancestor of all seed plants. This basic structure has been conserved after each round of whole genome duplication, adding layers of paralogs with similar interaction patterns. We thus present the first model where we can show that a network of eukaryotic TFs has evolved via rounds of whole genome duplication. Furthermore, we found that subfamilies in which the K domain is most diverged, the interactions with other subfamilies have been largely lost. We discuss the possibility that such a high proportion of genes were retained after each whole genome duplication because of their capacity to form higher order complexes involving proteins from different subfamilies. The simulteaneous duplications allowed for the conservation of the quantitative balance between the constituents, and facilitated sub- and neo-functionalization through differential expression of whole units.

Key Words: genome duplication • protein network • MADS • transcription factor


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