The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans
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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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Cites
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood
Guindon, S., & Gascuel, O. (2003) · Systematic Biology · doi:10.1080/10635150390235520 · Cited by 16,698 · see citing works
Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · cited 2× · see citing works
“However, basal metazoan relationships remain controversial (see alternative views in [28,29,31]), and the reconstruction may differ under alternative topologies.”
BackgroundSea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
Assessing the root of bilaterian animals with scalable phylogenomic methods
Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., Martinez, P., Baguñà, J., Bailly, X., Jondelius, U., et al. (2009) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2009.0896 · Cited by 747 · cited 2× · see citing works
“However, basal metazoan relationships remain controversial (see alternative views in [28,29,31]), and the reconstruction may differ under alternative topologies.”
BackgroundEarly origins and evolution of microRNAs and Piwi-interacting RNAs in animals
Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B. J., Chiang, H. R., King, N., Degnan, B. M., Rokhsar, D. S., & Bartel, D. P. (2008) · Nature · doi:10.1038/nature07415 · Cited by 725 · see citing works
Phylogenomics Revives Traditional Views on Deep Animal Relationships
Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., et al. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.052 · Cited by 695 · see citing works
Cell adhesion molecules: signalling functions at the synapse
Dalva, M. B., McClelland, A. C., & Kayser, M. S. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2075 · Cited by 620 · see citing works
Animal evolution: interrelationships of the living phyla
(1996) · Choice Reviews Online · doi:10.5860/choice.33-4500 · Cited by 455 · see citing works
Collins, M., Husi, H., Yu, L., Brandon, J. M., Anderson, C. N. G., Blackstock, W., Choudhary, J., & Grant, S. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03507.x · Cited by 448 · see citing works
Medina, M., Collins, A. G., Silberman, J. D., & Sogin, M. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171316998 · Cited by 395 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · cited 1× · see citing works
“[23-27]).”
Shiraishi‐Yamaguchi, Y., & Furuichi, T. (2007) · Genome biology · doi:10.1186/gb-2007-8-2-206 · Cited by 324 · see citing works
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Rokas, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091513 · Cited by 312 · see citing works
A Post-Synaptic Scaffold at the Origin of the Animal Kingdom
Sakarya, O., Armstrong, K. A., Adamska, M., Adamski, M., Wang, I.-F., Tidor, B., Degnan, B. M., Oakley, T. H., & Kosik, K. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000506 · Cited by 291 · see citing works
Genesis and Expansion of Metazoan Transcription Factor Gene Classes
Larroux, C., Luke, G. N., Koopman, P. A., Rokhsar, D. S., Shimeld, S. M., & Degnan, B. M. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn047 · Cited by 275 · see citing works
A Phylogenomic Investigation into the Origin of Metazoa
Ruiz‐Trillo, I., Roger, A. J., Burger, G., Gray, M. W., & Lang, B. F. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn006 · Cited by 269 · see citing works
Schierwater, B., Eitel, M., Jakob, W., Osigus, H.-J., Hadrys, H., Dellaporta, S. L., Kolokotronis, S.-O., & DeSalle, R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000020 · Cited by 260 · see citing works
Dellaporta, S. L., Xu, A., Sagasser, S., Jakob, W., Moreno, M. A., Buss, L. W., & Schierwater, B. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602076103 · Cited by 252 · see citing works
Boeckers, T. M. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0274-5 · Cited by 243 · see citing works
Manning, G., Young, S. L., Miller, W. T., & Zhai, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801314105 · Cited by 211 · see citing works
Choanoflagellates, choanocytes, and animal multicellularity
Maldonado, M. (2004) · Invertebrate Biology · doi:10.1111/j.1744-7410.2004.tb00138.x · Cited by 207 · see citing works
Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit
Richards, G. S., Simionato, E., Perron, M., Adamska, M., Vervoort, M., & Degnan, B. M. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.074 · Cited by 165 · see citing works
Manuel, M., Borchiellini, C., Alivon, E., Parco, Y. L., Vacelet, J., & Boury‐Esnault, N. (2003) · Systematic Biology · doi:10.1080/10635150309322 · Cited by 158 · see citing works
Cell adhesion molecules at the synapse
Gerrow, K. (2006) · Frontiers in bioscience · doi:10.2741/1978 · Cited by 133 · see citing works
Regulation of Presynaptic Calcium Channels by Synaptic Proteins
Zamponi, G. W. (2003) · Journal of Pharmacological Sciences · doi:10.1254/jphs.92.79 · Cited by 111 · see citing works
Microtubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95
Passafaro, M., Sala, C., Niethammer, M., & Sheng, M. (1999) · Nature Neuroscience · doi:10.1038/15990 · Cited by 110 · see citing works
Scaffolding proteins at the postsynaptic density: shank as the architectural framework
Kreienkamp, H. J. (2008) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-72843-6_15 · Cited by 105 · see citing works
Interaction of Synaptic Scaffolding Molecule and β-Catenin
Nishimura, W., Yao, I., Iida, J., Tanaka, N., & Hata, Y. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00757.2002 · Cited by 96 · see citing works
Evolution of sensory structures in basal metazoa
Jacobs, D. K., Nakanishi, N., Yuan, D., Camara, A., Nichols, S., & Hartenstein, V. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm094 · Cited by 87 · see citing works
Molecular morphogens for dendritic spines
Ehlers, M. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02061-1 · Cited by 73 · see citing works
Kir channels in the CNS: emerging new roles and implications for neurological diseases
Neusch, C., Weishaupt, J. H., & Bähr, M. (2003) · Cell and Tissue Research · doi:10.1007/s00441-002-0669-x · Cited by 72 · see citing works
Exposito, J., Larroux, C., Cluzel, C., Valcourt, U., Lethias, C., & Degnan, B. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m804573200 · Cited by 71 · see citing works
Molecular constituents and phosphorylation‐dependent regulation of the post‐synaptic density
Yamauchi, T. (2002) · Mass Spectrometry Reviews · doi:10.1002/mas.10033 · Cited by 63 · see citing works
Hadrys, T., DeSalle, R., Sagasser, S., Fischer, N., & Schierwater, B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi150 · Cited by 60 · see citing works
Placozoa and the evolution of Metazoa and intrasomatic cell differentiation
Schierwater, B., de Jong, D., & DeSalle, R. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.09.023 · Cited by 59 · see citing works
Proteomics analysis of immuno-precipitated synaptic protein complexes
Klemmer, P., Smit, A. B., & Li, K. W. (2008) · Journal of Proteomics · doi:10.1016/j.jprot.2008.10.005 · Cited by 54 · see citing works
The synapse proteome and phosphoproteome: a new paradigm for synapse biology
Grant, S. G. N. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340059 · Cited by 50 · see citing works
Vessey, J. P., & Karra, D. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04662.x · Cited by 44 · see citing works
Organization of brain complexity--synapse proteome form and function
Pocklington, A. J. (2006) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/ell013 · Cited by 36 · see citing works
Exploring the early origins of the synapse by comparative genomics
Kosik, K. S. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0594 · Cited by 28 · see citing works
Animal Evolution: Trichoplax, Trees, and Taxonomic Turmoil
Miller, D. J., & Ball, E. E. (2008) · Current Biology · doi:10.1016/j.cub.2008.09.016 · Cited by 24 · see citing works
Animal Evolution: Once upon a Time
Telford, M. J. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.025 · Cited by 11 · see citing works
Regulation of Presynaptic Calcium Channels by Synaptic Proteins
Zamponi, G. W. (2003) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.1254/s1347-8613(19)32668-4 · Cited by 6 · see citing works
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Arendt, D., Musser, J. M., Baker, C. V. H., Bergman, A., Cepko, C., Erwin, D. H., Pavlicev, M., Schlosser, G., Widder, S., Laubichler, M. D., et al. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.127 · Cited by 764 · see citing works
Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G., & Leys, S. P. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu057 · Cited by 266 · see citing works
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Back to the Basics: Cnidarians Start to Fire
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Hunding, A., & Baumgartner, S. (2017) · Hereditas · doi:10.1186/s41065-017-0029-1 · Cited by 10 · see citing works
Sinkovics, J. (2015) · European Journal of Microbiology and Immunology · doi:10.1556/eujmi-d-14-00034 · Cited by 10 · see citing works
Ali, S., Hoven, A., Dress, R. J., Schaal, H., Alferink, J., & Scheu, S. (2018) · BMC Genomics · doi:10.1186/s12864-018-4573-5 · Cited by 10 · see citing works
Schierwater, B., Osigus, H., Bergmann, T., Blackstone, N. W., Hadrys, H., Hauslage, J., Humbert, P. O., Kamm, K., Kvansakul, M., Wysocki, K., et al. (2021) · BioEssays · doi:10.1002/bies.202100083 · Cited by 9 · see citing works
Evolution of homology: From archetype towards a holistic concept of cell type
Rusin, L. Y. (2023) · Journal of Morphology · doi:10.1002/jmor.21569 · Cited by 8 · see citing works
The Notch ligand E3 ligase, Mind Bomb1, regulates glutamate receptor localization in Drosophila
Sturgeon, M. L., Davis, D., Albers, A., Beatty, D., Austin, R., Ferguson, M., Tounsel, B. L., & Liebl, F. L. W. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.11.004 · Cited by 8 · see citing works
Crystallographic Studies of PDZ Domain–Peptide Interactions of the Scribble Polarity Module
Maddumage, J. C., Stewart, B. Z., Humbert, P. O., & Kvansakul, M. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1166-1_7 · Cited by 7 · see citing works
Back Through Time: How Cnidarians and Basal Metazoans Shed Light on Ancient Nervous Systems
Watanabe, H. (2017) · Diversity and commonality in animals · doi:10.1007/978-4-431-56469-0_3 · Cited by 7 · see citing works
Three explanations for extraterrestrials: sensible, unlikely, mad
Morris, S. C. (2016) · International Journal of Astrobiology · doi:10.1017/s1473550416000379 · Cited by 5 · see citing works
Model Systems for Exploring the Evolutionary Origins of the Nervous System
Whitmer, K. M. H. (2018) · Results and problems in cell differentiation · doi:10.1007/978-3-319-92486-1_10 · Cited by 5 · see citing works
Trafficking of Glutamate Receptors and Associated Proteins in Synaptic Plasticity
Hořák, M., Seabold, G. K., & Petralia, R. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00008-0 · Cited by 4 · see citing works
Hehmeyer, J., Plessier, F., & Marlow, H. Q. (2024) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111822-124041 · Cited by 3 · see citing works
Animal evolution coincides with a novel degree of freedom in exocytic transport processesPreprint
Kollmar, M., Welz, T., Straub, F., Alzahofi, N., Hatje, K., Briggs, D. A., Samol-Wolf, A., Burkhardt, P., Hume, A. N., & Kerkhoff, E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/591974 · Cited by 3 · see citing works
Rise of the Animal Kingdom and Epigenetic Mechanisms of Evolution
Cabej, N. R. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-401667-5.00005-5 · Cited by 2 · see citing works
Leys, S. P., & Farrar, N. R. (2015) · doi:10.1093/acprof:oso/9780199682201.003.0003 · Cited by 1 · see citing works
Conformational dynamics regulate SHANK3 actin and Rap1 bindingPreprint
Salomaa, S. I., Miihkinen, M., Kremneva, E., Paatero, I., Lilja, J., Jacquemet, G., Vuorio, J., Antenucci, L., Nia, F. H., Hollós, P., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.12.379222 · Cited by 1 · see citing works
Insights from Sponge Transcriptomes & Physiology about the Early Evolution of Nervous Systems
Farrar, N. R. (2014) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3183485q
Pre- and Postsynaptic Assembly and Maturation
Sigrist, S. J., & Wichmann, C. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00008-9
Porifera R. E. Grant 1836 [M. Manuel and N. Boury-Esnault], converted clade name
de Queiroz, K., Cantino, P. D., & Gauthier, J. A. (2020) · CRC Press eBooks · doi:10.1201/9780429446276-114
Cell states along oligodendrocyte development and disease
van Bruggen, D. (2020) · Figshare
成光, 原. (2012) · 日本プランクトン学会報 · doi:10.24763/bpsj.59.1_35
Intratumoral and extratumoral synapses are required for glioblastoma progression in DrosophilaPreprint
Losada‐Pérez, M., García-Moreno, M. H., & Casas‐Tintó, S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.14.464400
(2016) · Gallimard eBooks · doi:10.3917/gall.colle.2016.01.0274
Seheon, M. E., Parra, A. S., & Johnston, C. A. (2025) · PLoS ONE · doi:10.1371/journal.pone.0316787
Nervous system evolution : insights from the sea urchin
Formery, L. (2019) · theses.fr (ABES) · doi:10.70675/146c0b8aza71az47ecza2c7zc12baf0f5794
- 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)
- PMC
- PMC2824662
- 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
- gold
- doi.org
- 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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