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MBE Advance Access published online on July 10, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn151
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© The Author 2008. 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

SNAREing the basis of multicellularity: Consequences of protein family expansion during evolution

Tobias H. Kloepper1,2, C. Nickias Kienle1 and Dirk Fasshauer1

1 Research Group Structural Biochemistry, Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Göttingen, Germany, e-mail D.F.: dfassha{at}gwdg.de , phone: +49-551-201 1637, Fax: +49-551-201 1499; C.N.K.: nkienle{at}gwdg.de, e-mail T.H.K.: tkloepp{at}gwdg.de
2 Center for Bioinformatics, University of Tübingen, Sand 14, 72076 Tübingen, Germany

Correspondence should be addressed to D.F.

Received for publication April 16, 2008. Revision received June 15, 2008. Accepted for publication July 7, 2008.

Vesicle trafficking between intracellular compartments of eukaryotic cells is mediated by conserved protein machineries. In each trafficking step, fusion of the vesicle with the acceptor membrane is driven by a set of distinctive SNARE proteins that assemble into tight four-helix bundle complexes between the fusing membranes. During evolution about twenty primordial SNARE types were modified independently in different eukaryotic lineages by episodes of duplication and diversification. Here we show that two major changes in the SNARE repertoire occurred in the evolution of animals, each reflecting a main overhaul of the endomembrane system. In addition, we found several lineage-specific losses of distinct SNAREs, particularly in nematodes and platyhelminthes. The first major transformation took place during the transition to multicellularity. The primary event that occurred during this transformation was an increase in the numbers of endosomal SNAREs, but the SNARE-related factor Lgl also emerged. Apparently, enhanced endosomal sorting capabilities were an advantage for early multicellular animals. The second major transformation during the rise of vertebrates resulted in a robust expansion of the secretory set of SNAREs, which may have helped develop a more versatile secretory apparatus.

Key Words: SNARE • membrane fusion • secretion • metazoa • multicellularity • vertebrata


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