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The evolutionary landscape of the Rab family in chordates

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Abstract

Intracellular traffic amongst organelles represents a key feature for eukaryotes and is orchestrated principally by members of Rab family, the largest within Ras superfamily. Given that variations in Rab repertoire have been fundamental in animal diversification, we provided the most exhaustive survey regarding the Rab toolkit of chordates. Our findings reveal the existence of 42 metazoan conserved subfamilies exhibiting a univocal intron/exon structure preserved from cnidarians to vertebrates. Since the current view does not capture the Rab complexity, we propose a new Rab family classification in three distinct monophyletic clades. The Rab complement of chordates shows a dramatic diversification due to genome duplications and independent gene duplications and losses with sharp differences amongst cephalochordates, tunicates and gnathostome vertebrates. Strikingly, the analysis of the domain architecture of this family highlighted the existence of chimeric calcium-binding Rabs, which are animal novelties characterized by a complex evolutionary history in gnathostomes and whose role in cellular metabolism is obscure. This work provides novel insights in the knowledge of Rab family: our hypothesis is that chordates represent a hotspot of Rab variability, with many events of gene gains and losses impacting intracellular traffic capabilities. Our results help to elucidate the role of Rab members in the transport amongst endomembranes and shed light on intracellular traffic routes in vertebrates. Then, since the predominant role of Rabs in the molecular communication between different cellular districts, this study paves to way to comprehend inherited or acquired human disorders provoked by dysfunctions in Rab genes.

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Acknowledgements

The authors are grateful to the Branchiostoma lanceolatum Genome Consortium that provided access to the European amphioxus genome [76]. We would like to thank Dr. Eva Jimenez-Guri for her critical reading of the manuscript, and three anonymous reviewers for their comments that helped to improve the manuscript. R.A. was supported by BIO2015-67358-C2-1-P grant from Ministerio de Economía y Competitividad (Spain) and by Grant SGR2017-1665 from Generalitat de Catalunya. U.C. was supported by a OU-SZN PhD fellowship.

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  1. Ugo Coppola

    Present address: Molecular Cardiovascular Biology Division, Cincinnati Children’s Hospital Medical Center, Cincinnati, USA

Authors and Affiliations

  1. Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn Napoli, Villa Comunale 1, 80121, Naples, Italy

    Ugo Coppola, Filomena Ristoratore & Salvatore D’Aniello

  2. Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

    Ricard Albalat

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– Raw phylogenetic trees (A, B) including Rab names. (PDF 5642 kb)

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Coppola, U., Ristoratore, F., Albalat, R. et al. The evolutionary landscape of the Rab family in chordates. Cell. Mol. Life Sci. 76, 4117–4130 (2019). https://doi.org/10.1007/s00018-019-03103-7

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