Cited by 79Marine Invertebrate Physiology and EcologyDevelopmental Biology and Gene RegulationNeuroscience and Neuropharmacology Research

The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans

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Alié, Alexandre, Manuel, Michaël·2010·BMC Evolutionary Biology

Abstract

BACKGROUND: Comparative genomics of the early diverging metazoan lineages and of their unicellular sister-groups opens new window to reconstructing the genetic changes which preceded or accompanied the evolution of multicellular body plans. A recent analysis found that the genome of the nerve-less sponges encodes the homologues of most vertebrate post-synaptic proteins. In vertebrate excitatory synapses, these proteins assemble to form the post-synaptic density, a complex molecular platform linking membrane receptors, components of their signalling pathways, and the cytoskeleton. Newly available genomes from Monosiga brevicollis (a member of Choanoflagellata, the closest unicellular relatives of animals) and Trichoplax adhaerens (a member of Placozoa: besides sponges, the only nerve-less metazoans) offer an opportunity to refine our understanding of post-synaptic protein evolution. RESULTS: Searches for orthologous proteins and reconstruction of gene gains/losses based on the taxon phylogeny indicate that post-synaptic proteins originated in two main steps. The backbone scaffold proteins (Shank, Homer, DLG) and some of their partners were acquired in a unicellular ancestor of choanoflagellates and metazoans. A substantial additional set appeared in an exclusive ancestor of the Metazoa. The placozoan genome contains most post-synaptic genes but lacks some of them. Notably, the master-scaffold protein Shank might have been lost secondarily in the placozoan lineage. CONCLUSIONS: The time of origination of most post-synaptic proteins was not concomitant with the acquisition of synapses or neural-like cells. The backbone of the scaffold emerged in a unicellular context and was probably not involved in cell-cell communication. Based on the reconstructed protein composition and potential interactions, its ancestral function could have been to link calcium signalling and cytoskeleton regulation. The complex later became integrated into the evolving synapse through the addition of novel functionalities.

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  • Cnidarians show an ancestral complexity in synaptic proteins.

    “An “ancestral complexity” of cnidarians in terms of synaptic proteins is therefore apparent [28,32].”

    From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [32]

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Authors
Alié, A., & Manuel, M.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Manuel, Michaël
Venue
BMC Evolutionary Biology
Published
2010
Volume
10
Issue
1
Pages
34
ISSN
1471-2148 (ISSN-L)
OpenAlex
W2155807319
Cited by
79
References
45
Citations by year
2025: 1 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 8 · 2015: 8 · 2014: 7 · 2013: 5 · 2012: 7
FWCI
4.27
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Agence Nationale de la Recherche
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
postsynaptic density, Choanoflagellata, Placozoa, Monosiga brevicollis, Trichoplax adhaerens, sponge genome, shank, Homer, Dlg, gene gain and loss, evolution of multicellularity, calcium signaling, cytoskeleton regulation, neuroevolution
MeSH terms
Animals, Nerve Tissue Proteins, Phylogeny, Sequence Alignment, Evolution, Molecular, Sequence Analysis, Protein, Placozoa, Comparative Genomic Hybridization, Choanoflagellata

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