Abstract
BackgroundCell-to-cell communication is a key process in multicellular organisms. In multicellular animals, scaffolding proteins belonging to the family of membrane-associated guanylate kinases (MAGUK) are involved in the regulation and formation of cell junctions. These MAGUK proteins were believed to be exclusive to Metazoa. However, a MAGUK gene was recently identified in an EST survey of Capsaspora owczarzaki, an unicellular organism that branches off near the metazoan clade. To further investigate the evolutionary history of MAGUK, we have undertook a broader search for this gene family using available genomic sequences of different opisthokont taxa.ResultsOur survey and phylogenetic analyses show that MAGUK proteins are present not only in Metazoa, but also in the choanoflagellate Monosiga brevicollis and in the protist Capsaspora owczarzaki. However, MAGUKs are absent from fungi, amoebozoans or any other eukaryote. The repertoire of MAGUKs in Placozoa and eumetazoan taxa (Cnidaria + Bilateria) is quite similar, except for one class that is missing in Trichoplax, while Porifera have a simpler MAGUK repertoire. However, Vertebrata have undergone several independent duplications and exhibit two exclusive MAGUK classes. Three different MAGUK types are found in both M. brevicollis and C. owczarzaki: DLG, MPP and MAGI. Furthermore, M. brevicollis has suffered a lineage-specific diversification.ConclusionsThe diversification of the MAGUK protein gene family occurred, most probably, prior to the divergence between Metazoa+choanoflagellates and the Capsaspora+Ministeria clade. A MAGI-like, a DLG-like, and a MPP-like ancestral genes were already present in the unicellular ancestor of Metazoa, and new gene members have been incorporated through metazoan evolution within two major periods, one before the sponge-eumetazoan split and another within the vertebrate lineage. Moreover, choanoflagellates have suffered an independent MAGUK diversification. This study highlights the importance of generating enough genome data from the broadest possible taxonomic sampling, in order to fully understand the evolutionary history of major protein gene families.
Highlights
Cell-to-cell communication is a key process in multicellular organisms
A membrane-associated guanylate kinase with an inverted repeat (MAGI)-like, a Disc Large Homolog (DLG)-like, and a MPP-like ancestral genes were already present in the unicellular ancestor of Metazoa, and new gene members have been incorporated through metazoan evolution within two major periods, one before the spongeeumetazoan split and another within the vertebrate lineage
The analysis clearly shows that the homologs of C. owczarzaki and M. brevicollis do not come from lateral gene transfer (LGT) from metazoans since they clearly group outside the major metazoan membrane-associated guanylate kinases (MAGUK) types, as we would expect if LGT between metazoans and those protists had taken place (Additional file 4)
Summary
In multicellular animals, scaffolding proteins belonging to the family of membrane-associated guanylate kinases (MAGUK) are involved in the regulation and formation of cell junctions. These MAGUK proteins were believed to be exclusive to Metazoa. The MAGUK family have been divided into different classes or groups, according to phylogenetic position and protein domain architecture (see for example [2] and [10], and Figure 1 for our own MAGUK classification) These MAGUKs classes are known as calcium/calmodulin-dependent proteins kinase (CASK), palmitoylated de Mendoza et al BMC Evolutionary Biology 2010, 10:93 http://www.biomedcentral.com/1471-2148/10/93. All of these modular motifs in MAGUK mediate protein-protein interactions
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