Metazoan evolution of glutamate receptors reveals unreported phylogenetic groups and divergent lineage-specific events

  1. David Ramos-Vicente
  2. Jie Ji
  3. Esther Gratacòs-Batlle
  4. Gemma Gou
  5. Rita Reig-Viader
  6. Javier Luís
  7. Demian Burguera
  8. Enrique Navas-Perez
  9. Jordi García-Fernández
  10. Pablo Fuentes-Prior
  11. Hector Escriva
  12. Nerea Roher
  13. David Soto
  14. Àlex Bayés  Is a corresponding author
  1. Biomedical Research Institute Sant Pau, Spain
  2. Universitat Autònoma de Barcelona, Spain
  3. University of Barcelona, Spain
  4. Sorbonne Université, CNRS, France

Abstract

Glutamate receptors are divided in two unrelated families: ionotropic (iGluR), driving synaptic transmission, and metabotropic (mGluR), which modulate synaptic strength. The present classification of GluRs is based on vertebrate proteins and has remained unchanged for over two decades. Here we report an exhaustive phylogenetic study of GluRs in metazoans. Importantly, we demonstrate that GluRs have followed different evolutionary histories in separated animal lineages. Our analysis reveals that the present organization of iGluRs into six classes does not capture the full complexity of their evolution. Instead, we propose an organization into four subfamilies and ten classes, four of which have never been previously described. Furthermore, we report a sister class to mGluR classes I-III, class IV. We show that many unreported proteins are expressed in the nervous system, and that new Epsilon receptors form functional ligand-gated ion channels. We propose an updated classification of glutamate receptors that includes our findings.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, Figure 1 - figure supplement 1, Figure 1 - figure supplement 3, Figure 1 - figure supplement 4, Figure2, Figure 4, Figure 4 - figure supplement 1 and Figure 4 - figure supplement 3.

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Article and author information

Author details

  1. David Ramos-Vicente

    Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2730-0850
  2. Jie Ji

    Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, Bellaterra (Cerdanyola del Vallès), Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Esther Gratacòs-Batlle

    Department of Biomedicine, Medical School, University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Gemma Gou

    Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Rita Reig-Viader

    Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Javier Luís

    Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Demian Burguera

    Department of Genetics, University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Enrique Navas-Perez

    Department of Genetics, University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Jordi García-Fernández

    Department of Genetics, University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Pablo Fuentes-Prior

    Molecular Bases of Disease, Biomedical Research Institute Sant Pau, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  11. Hector Escriva

    Biologie Intégrative des Organismes Marins, Sorbonne Université, CNRS, Banyuls-sur-Mer, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Nerea Roher

    Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, Bellaterra (Cerdanyola del Vallès), Spain
    Competing interests
    The authors declare that no competing interests exist.
  13. David Soto

    Department of Biomedicine, Medical School, University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7995-3805
  14. Àlex Bayés

    Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain
    For correspondence
    abayesp@santpau.cat
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5265-6306

Funding

Ministerio de Economía y Competitividad (BFU2012-34398)

  • David Ramos-Vicente
  • Gemma Gou
  • Rita Reig-Viader
  • Javier Luís
  • Àlex Bayés

Ministerio de Economía y Competitividad (BFU2014-57562-P)

  • David Soto

Centre National de la Recherche Scientifique (ANR-16-CE12-0008-01)

  • Hector Escriva

Ministerio de Economía y Competitividad (BFU2017-83317-P)

  • David Soto

Ministerio de Economía y Competitividad (RD16/0008/0014)

  • David Soto

Ministerio de Economía y Competitividad (BFU2015-69717-P)

  • David Ramos-Vicente
  • Gemma Gou
  • Rita Reig-Viader
  • Javier Luís
  • Àlex Bayés

Seventh Framework Programme (304111)

  • David Ramos-Vicente
  • Gemma Gou
  • Rita Reig-Viader
  • Javier Luís
  • Àlex Bayés

Ministerio de Economía y Competitividad (RYC-2011-08391)

  • Àlex Bayés

Ministerio de Economía y Competitividad (RYC-2010-06210)

  • Nerea Roher

China Scholarship Council (CSC-2013-06300075)

  • Jie Ji

Ministerio de Economía y Competitividad (SAF2014-57994-R)

  • Pablo Fuentes-Prior

Ministerio de Economía y Competitividad (AGL2015-65129-R)

  • Jie Ji
  • Nerea Roher

Generalitat de Catalunya (SGR-345-2014)

  • David Ramos-Vicente
  • Gemma Gou
  • Rita Reig-Viader
  • Javier Luís
  • Àlex Bayés

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Leon D Islas, Universidad Nacional Autónoma de México, Mexico

Version history

  1. Received: February 9, 2018
  2. Accepted: November 20, 2018
  3. Accepted Manuscript published: November 22, 2018 (version 1)
  4. Version of Record published: December 27, 2018 (version 2)

Copyright

© 2018, Ramos-Vicente et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. David Ramos-Vicente
  2. Jie Ji
  3. Esther Gratacòs-Batlle
  4. Gemma Gou
  5. Rita Reig-Viader
  6. Javier Luís
  7. Demian Burguera
  8. Enrique Navas-Perez
  9. Jordi García-Fernández
  10. Pablo Fuentes-Prior
  11. Hector Escriva
  12. Nerea Roher
  13. David Soto
  14. Àlex Bayés
(2018)
Metazoan evolution of glutamate receptors reveals unreported phylogenetic groups and divergent lineage-specific events
eLife 7:e35774.
https://doi.org/10.7554/eLife.35774

Share this article

https://doi.org/10.7554/eLife.35774

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