A Post-Synaptic Scaffold at the Origin of the Animal Kingdom

Sakarya, Onur; Armstrong, Kathryn A.; Adamska, Maja; Adamski, Marcin; Wang, I-Fan; Tidor, Bruce; Degnan, Bernard M.; Oakley, Todd H.; Kosik, Kenneth S.

doi:10.1371/journal.pone.0000506

A Post-Synaptic Scaffold at the Origin of the Animal Kingdom

Journal Article · Wed Jun 06 00:00:00 EDT 2007 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0000506· OSTI ID:1627334

Sakarya, Onur ^[1]; Armstrong, Kathryn A. ^[2]; Adamska, Maja ^[3]; Adamski, Marcin ^[3]; Wang, I-Fan ^[4]; Tidor, Bruce ^[2]; Degnan, Bernard M. ^[3]; Oakley, Todd H. ^[4]; Kosik, Kenneth S. ^[4]

Univ. of California, Santa Barbara, CA (United States); DOE/OSTI
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Univ. of Queensland, Brisbane, QLD (Australia)
Univ. of California, Santa Barbara, CA (United States)

Background. The evolution of complex sub-cellular structures such as the synapse requires the assembly of multiple proteins, each conferring added functionality to the integrated structure. Tracking the early evolution of synapses has not been possible without genomic information from the earliest branching animals. As the closest extant relatives to the Eumetazoa, Porifera (sponges) represent a pivotal group for understanding the evolution of nervous systems, because sponges lack neurons with clearly recognizable synapses, in contrast to eumetazoan animals. Methodology/Principal Findings. We show that the genome of the demosponge Amphimedon queenslandica possesses a nearly complete set of post-synaptic protein homologs whose conserved interaction motifs suggest assembly into a complex structure. In the critical synaptic scaffold gene, dlg, residues that make hydrogen bonds and van der Waals interactions with the PDZ ligand are 100% conserved between sponge and human, as is the motif organization of the scaffolds. Expression in Amphimedon of multiple post-synaptic gene homologs in larval flask cells further supports the existence of an assembled structure. Among the few post-synaptic genes absent from Amphimedon, but present in Eumetazoa, are receptor genes including the entire ionotropic glutamate receptor family. Conclusions/Significance. Highly conserved protein interaction motifs and co-expression in sponges of multiple proteins whose homologs interact in eumetazoan synapses indicate that a complex protein scaffold was present at the origin of animals, perhaps predating nervous systems. A relatively small number of crucial innovations to this pre-existing structure may represent the founding changes that led to a post-synaptic element.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Australian Research Council (ARC); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627334

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 6 Vol. 2; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Neurexin–neuroligin signaling in synapse development Craig, Ann Marie; Kang, Yunhee Current Opinion in Neurobiology, Vol. 17, Issue 1 https://doi.org/10.1016/j.conb.2007.01.011	journal	February 2007
Crystal Structures of a Complexed and Peptide-Free Membrane Protein–Binding Domain: Molecular Basis of Peptide Recognition by PDZ Doyle, Declan A.; Lee, Alice; Lewis, John Cell, Vol. 85, Issue 7 https://doi.org/10.1016/s0092-8674(00)81307-0	journal	June 1996
Comparative protein modeling by satisfaction of spatial restraints ⩽ali, Andrej Molecular Medicine Today, Vol. 1, Issue 6 https://doi.org/10.1016/s1357-4310(95)91170-7	journal	September 1995
The Binding of the PDZ Tandem of Syntenin to Target Proteins ^, Grembecka, Jolanta; Cierpicki, Tomasz; Devedjiev, Yancho Biochemistry, Vol. 45, Issue 11 https://doi.org/10.1021/bi052225y	journal	February 2006
Accurate Calculation of Hydration Free Energies Using Macroscopic Solvent Models Sitkoff, Doree; Sharp, Kim A.; Honig, Barry The Journal of Physical Chemistry, Vol. 98, Issue 7 https://doi.org/10.1021/j100058a043	journal	February 1994
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
From The Cover: Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record Peterson, K. J.; Butterfield, N. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 27 https://doi.org/10.1073/pnas.0503660102	journal	June 2005
Early evolution of animal cell signaling and adhesion genes Nichols, S. A.; Dirks, W.; Pearse, J. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 33 https://doi.org/10.1073/pnas.0604065103	journal	August 2006
SMART, a simple modular architecture research tool: Identification of signaling domains Schultz, J.; Milpetz, F.; Bork, P. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.5857	journal	May 1998
Semiquantitative Proteomic Analysis of Rat Forebrain Postsynaptic Density Fractions by Mass Spectrometry Peng, Junmin; Kim, Myung Jong; Cheng, Dongmei Journal of Biological Chemistry, Vol. 279, Issue 20 https://doi.org/10.1074/jbc.m400103200	journal	May 2004
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
A Hybrid Micro–Macroevolutionary Approach to Gene Tree Reconstruction Durand, Dannie; Halldórsson, Bjarni V.; Vernot, Benjamin Journal of Computational Biology, Vol. 13, Issue 2 https://doi.org/10.1089/cmb.2006.13.320	journal	March 2006
Intramolecular interactions regulate SAP97 binding to GKAP Wu, H. The EMBO Journal, Vol. 19, Issue 21 https://doi.org/10.1093/emboj/19.21.5740	journal	November 2000
Mitochondrial Diversity of Early-Branching Metazoa Is Revealed by the Complete mt Genome of a Haplosclerid Demosponge Erpenbeck, D.; Voigt, O.; Adamski, M. Molecular Biology and Evolution, Vol. 24, Issue 1 https://doi.org/10.1093/molbev/msl154	journal	October 2006
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
The Pfam Protein Families Database Bateman, A. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.276	journal	January 2002
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity Larroux, Claire; Fahey, Bryony; Liubicich, Danielle Evolution Development, Vol. 8, Issue 2 https://doi.org/10.1111/j.1525-142x.2006.00086.x	journal	March 2006
Cytological Basis of Photoresponsive Behavior in a Sponge Larva Leys, Sally P.; Degnan, Bernard M. The Biological Bulletin, Vol. 201, Issue 3 https://doi.org/10.2307/1543611	journal	December 2001
CHARMM: A program for macromolecular energy, minimization, and dynamics calculations Brooks, Bernard R.; Bruccoleri, Robert E.; Olafson, Barry D. Journal of Computational Chemistry, Vol. 4, Issue 2 https://doi.org/10.1002/jcc.540040211	journal	July 1983
Polar hydrogen positions in proteins: Empirical energy placement and neutron diffraction comparison Brünger, Axel T.; Karplus, Martin Proteins: Structure, Function, and Genetics, Vol. 4, Issue 2 https://doi.org/10.1002/prot.340040208	journal	January 1988
Prediction of complete gene structures in human genomic DNA Burge, Chris; Karlin, Samuel Journal of Molecular Biology, Vol. 268, Issue 1 https://doi.org/10.1006/jmbi.1997.0951	journal	April 1997
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap Journal of Molecular Biology, Vol. 302, Issue 1 https://doi.org/10.1006/jmbi.2000.4042	journal	September 2000
Aquabacterium terrae sp. nov., isolated from soil Dahal, Ram Hari; Han, Ji Yeon; Lee, Hyosun Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02269-8	journal	April 2021
Crystal Structures of a Complexed and Peptide-Free Membrane Protein–Binding Domain: Molecular Basis of Peptide Recognition by PDZ Doyle, Declan A.; Lee, Alice; Lewis, John Cell, Vol. 85, Issue 7 https://doi.org/10.1016/S0092-8674(00)81307-0	journal	June 1996
Orthology, paralogy and proposed classification for paralog subtypes Sonnhammer, Erik L. L.; Koonin, Eugene V. Trends in Genetics, Vol. 18, Issue 12 https://doi.org/10.1016/S0168-9525(02)02793-2	journal	December 2002
Ion Channels and Synaptic Organization Littleton, J. Troy; Ganetzky, Barry Neuron, Vol. 26, Issue 1 https://doi.org/10.1016/S0896-6273(00)81135-6	journal	April 2000
Comparative protein modeling by satisfaction of spatial restraints ⩽ali, Andrej Molecular Medicine Today, Vol. 1, Issue 6 https://doi.org/10.1016/S1357-4310(95)91170-7	journal	September 1995
Partitioning of genetically distinct cell populations in chimeric juveniles of the sponge Amphimedon queenslandica Gauthier, Marie; Degnan, Bernard M. Developmental & Comparative Immunology, Vol. 32, Issue 11 https://doi.org/10.1016/j.dci.2008.04.002	journal	January 2008
Proteomic analysis of NMDA receptor–adhesion protein signaling complexes Husi, Holger; Ward, Malcolm A.; Choudhary, Jyoti S. Nature Neuroscience, Vol. 3, Issue 7 https://doi.org/10.1038/76615	journal	July 2000
Phylogenomics and the reconstruction of the tree of life Delsuc, Frédéric; Brinkmann, Henner; Philippe, Hervé Nature Reviews Genetics, Vol. 6, Issue 5 https://doi.org/10.1038/nrg1603	journal	May 2005
Mechanism of pore opening in the calcium-activated chloride channel TMEM16A Lam, Andy K. M.; Dutzler, Raimund Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20788-8	journal	February 2021
The synapse proteome and phosphoproteome: a new paradigm for synapse biology Grant, S. G. N. Biochemical Society Transactions, Vol. 34, Issue 1 https://doi.org/10.1042/BST0340059	journal	January 2006
Sponge paraphyly and the origin of Metazoa: Sponge paraphyly Borchiellini, C.; Manuel, M.; Alivon, E. Journal of Evolutionary Biology, Vol. 14, Issue 1 https://doi.org/10.1046/j.1420-9101.2001.00244.x	journal	January 2001
Conflicting phylogenetic signals at the base of the metazoan tree Rokas, Antonis; King, Nicole; Finnerty, John Evolution and Development, Vol. 5, Issue 4 https://doi.org/10.1046/j.1525-142X.2003.03042.x	journal	July 2003
Semiquantitative Proteomic Analysis of Rat Forebrain Postsynaptic Density Fractions by Mass Spectrometry Peng, Junmin; Kim, Myung Jong; Cheng, Dongmei Journal of Biological Chemistry, Vol. 279, Issue 20 https://doi.org/10.1074/jbc.M400103200	journal	May 2004
A Greedy Algorithm for Aligning DNA Sequences Zhang, Zheng; Schwartz, Scott; Wagner, Lukas Journal of Computational Biology, Vol. 7, Issue 1-2 https://doi.org/10.1089/10665270050081478	journal	February 2000
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
ProtTest: selection of best-fit models of protein evolution Abascal, F.; Zardoya, R.; Posada, D. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti263	journal	January 2005
Mitochondrial Genome of the Homoscleromorph Oscarella carmela (Porifera, Demospongiae) Reveals Unexpected Complexity in the Common Ancestor of Sponges and Other Animals Wang, X.; Lavrov, D. V. Molecular Biology and Evolution, Vol. 24, Issue 2 https://doi.org/10.1093/molbev/msl167	journal	November 2006
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
The Pfam Protein Families Database Bateman, A. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.263	journal	January 2000
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
The Pfam protein families database Bateman, Alex; Coin, Lachlan; Durbin, Richard Nucleic Acids Research, Vol. 32, Issue S1, p. D138-D141 https://doi.org/10.1093/nar/gkh121	journal	January 2004
StellaBase: The Nematostella vectensis Genomics Database Sullivan, J. C. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj020	journal	January 2006
PCAP: A Whole-Genome Assembly Program Huang, X. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1390403	journal	September 2003
Computational Inference of Homologous Gene Structures in the Human Genome Yeh, R. -F.; Lim, L. P.; Burge, C. B. Genome Research, Vol. 11, Issue 5 https://doi.org/10.1101/gr.175701	journal	May 2001
Consed: A Graphical Tool for Sequence Finishing Gordon, David; Abajian, Chris; Green, Phil Genome Research, Vol. 8, Issue 3 https://doi.org/10.1101/gr.8.3.195	journal	March 1998
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
Comparative protein modeling by satisfaction of spatial restraints Sali, A. Acta Crystallographica Section A Foundations of Crystallography, Vol. 52, Issue a1 https://doi.org/10.1107/s0108767396095578	journal	August 1996
The Protein Data Bank Berman, Helen M.; Battistuz, Tammy; Bhat, T. N. Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 6 https://doi.org/10.1107/s0907444902003451	journal	May 2002
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity Larroux, Claire; Fahey, Bryony; Liubicich, Danielle Evolution Development, Vol. 8, Issue 2 https://doi.org/10.1111/j.1525-142X.2006.00086.x	journal	March 2006
Conduction system in a sponge Lawn, I.; Mackie, G.; Silver, G. Science, Vol. 211, Issue 4487 https://doi.org/10.1126/science.7466387	journal	March 1981
Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence Cavalier-Smith, T.; Allsopp, M. T. E. P.; Chao, E. E. Canadian Journal of Zoology, Vol. 74, Issue 11 https://doi.org/10.1139/z96-231	journal	November 1996
Orthologs, Paralogs, and Evolutionary Genomics Koonin, Eugene V. Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.114725	journal	December 2005
A hybrid micro-macroevolutionary approach to gene tree reconstruction. Durand, Dannie; Halldórsson, Bjarni V.; Vernot, Benjamin Figshare https://doi.org/10.1184/r1/6097109.v1	text	January 2018
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Larroux, Claire; Fahey, Bryony; Liubicich, Danielle Figshare https://doi.org/10.1184/r1/6097697	text	January 2018
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Larroux, Claire; Fahey, Bryony; Liubicich, Danielle Figshare https://doi.org/10.1184/r1/6097697.v1	text	January 2018
Impulse conduction in a sponge Leys, S. P.; Mackie, G. O.; Meech, R. W. Journal of Experimental Biology, Vol. 202, Issue 9 https://doi.org/10.1242/jeb.202.9.1139	journal	May 1999

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The birth of the synapse Ovsepian, Saak V. Brain Structure and Function, Vol. 222, Issue 8 https://doi.org/10.1007/s00429-017-1459-2	journal	June 2017
The Trichoplax genome and the nature of placozoans Srivastava, Mansi; Begovic, Emina; Chapman, Jarrod Nature, Vol. 454, Issue 7207 https://doi.org/10.1038/nature07191	journal	August 2008
The Amphimedon queenslandica genome and the evolution of animal complexity Srivastava, Mansi; Simakov, Oleg; Chapman, Jarrod Nature, Vol. 466, Issue 7307 https://doi.org/10.1038/nature09201	journal	August 2010
The origin and evolution of cell types Arendt, Detlev; Musser, Jacob M.; Baker, Clare V. H. Nature Reviews Genetics, Vol. 17, Issue 12 https://doi.org/10.1038/nrg.2016.127	journal	November 2016
The origin and evolution of synapses Ryan, Tomás J.; Grant, Seth G. N. Nature Reviews Neuroscience, Vol. 10, Issue 10 https://doi.org/10.1038/nrn2717	journal	September 2009
Exploring phylogeny to find the function of sleep Anafi, Ron C.; Kayser, Matthew S.; Raizen, David M. Nature Reviews Neuroscience, Vol. 20, Issue 2 https://doi.org/10.1038/s41583-018-0098-9	journal	December 2018
Co-expression of synaptic genes in the sponge Amphimedon queenslandica uncovers ancient neural submodules Wong, Eunice; Mölter, Jan; Anggono, Victor Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-51282-x	journal	October 2019
An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge Ueda, Nobuo; Richards, Gemma S.; Degnan, Bernard M. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep37546	journal	November 2016
Convergence of ion channel genome content in early animal evolution Liebeskind, Benjamin J.; Hillis, David M.; Zakon, Harold H. Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1501195112	journal	February 2015
Mutations in Nature Conferred a High Affinity Phosphatidylinositol 4,5-Bisphosphate-binding Site in Vertebrate Inwardly Rectifying Potassium Channels Tang, Qiong-Yao; Larry, Trevor; Hendra, Kalen Journal of Biological Chemistry, Vol. 290, Issue 27 https://doi.org/10.1074/jbc.M115.640409	journal	July 2015
Epithelia and integration in sponges Leys, S. P.; Nichols, S. A.; Adams, E. D. M. Integrative and Comparative Biology, Vol. 49, Issue 2 https://doi.org/10.1093/icb/icp038	journal	June 2009
Sensory Flask Cells in Sponge Larvae Regulate Metamorphosis via Calcium Signaling Nakanishi, Nagayasu; Stoupin, Daniel; Degnan, Sandie M. Integrative and Comparative Biology, Vol. 55, Issue 6 https://doi.org/10.1093/icb/icv014	journal	April 2015
Sponge Behavior and the Chemical Basis of Responses: A Post-Genomic View Leys, Sally P.; Mah, Jasmine L.; McGill, Paul R. Integrative and Comparative Biology, Vol. 59, Issue 4 https://doi.org/10.1093/icb/icz122	journal	July 2019
A "Neural" Enzyme in Nonbilaterian Animals and Algae: Preneural Origins for Peptidylglycine -Amidating Monooxygenase Attenborough, R. M. F.; Hayward, D. C.; Kitahara, M. V. Molecular Biology and Evolution, Vol. 29, Issue 10 https://doi.org/10.1093/molbev/mss114	journal	April 2012
The Analysis of Eight Transcriptomes from All Poriferan Classes Reveals Surprising Genetic Complexity in Sponges Riesgo, Ana; Farrar, Nathan; Windsor, Pamela J. Molecular Biology and Evolution, Vol. 31, Issue 5 https://doi.org/10.1093/molbev/msu057	journal	February 2014
Structural Molecular Components of Septate Junctions in Cnidarians Point to the Origin of Epithelial Junctions in Eukaryotes Ganot, Philippe; Zoccola, Didier; Tambutté, Eric Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu265	journal	September 2014
The Notch pathway in the annelid Platynereis : insights into chaetogenesis and neurogenesis processes Gazave, Eve; Lemaître, Quentin I. B.; Balavoine, Guillaume Open Biology, Vol. 7, Issue 2 https://doi.org/10.1098/rsob.160242	journal	February 2017
Evolution: like any other science it is predictable Conway Morris, Simon Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1537 https://doi.org/10.1098/rstb.2009.0154	journal	January 2010
The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution Degnan, Sandie M.; Degnan, Bernard M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1540 https://doi.org/10.1098/rstb.2009.0248	journal	February 2010
Animal–microbe interactions and the evolution of nervous systems Eisthen, Heather L.; Theis, Kevin R. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1685 https://doi.org/10.1098/rstb.2015.0052	journal	January 2016
Where is my mind? How sponges and placozoans may have lost neural cell types Ryan, Joseph F.; Chiodin, Marta Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1684 https://doi.org/10.1098/rstb.2015.0059	journal	December 2015
Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion Cavalier-Smith, Thomas Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1713 https://doi.org/10.1098/rstb.2015.0476	journal	February 2017
The evolution and function of the Pax/Six regulatory network in sponges: Pax/Six genes in freshwater sponges Rivera, A.; Winters, I.; Rued, A. Evolution & Development, Vol. 15, Issue 3 https://doi.org/10.1111/ede.12032	journal	April 2013
Six major steps in animal evolution: are we derived sponge larvae?: Six major steps in animal evolution Nielsen, Claus Evolution & Development, Vol. 10, Issue 2 https://doi.org/10.1111/j.1525-142X.2008.00231.x	journal	March 2008
Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer: Polarity in sponges Windsor, Pamela J.; Leys, Sally P. Evolution & Development, Vol. 12, Issue 5 https://doi.org/10.1111/j.1525-142x.2010.00434.x	journal	September 2010
The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and interleukin 1 receptor pathways: The origin of Toll-like and IL1 receptor pathways Gauthier, Marie E. A.; Du Pasquier, Louis; Degnan, Bernard M. Evolution & Development, Vol. 12, Issue 5 https://doi.org/10.1111/j.1525-142x.2010.00436.x	journal	September 2010
Origin of animal epithelia: insights from the sponge genome: Evolution of epithelia Fahey, Bryony; Degnan, Bernard M. Evolution & Development, Vol. 12, Issue 6 https://doi.org/10.1111/j.1525-142x.2010.00445.x	journal	October 2010
Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless Porifera? Nickel, Michael Invertebrate Biology, Vol. 129, Issue 1 https://doi.org/10.1111/j.1744-7410.2010.00193.x	journal	February 2010
Origin of the neuro-sensory system: new and expected insights from sponges Renard, Emmanuelle; Vacelet, Jean; Gazave, Eve Integrative Zoology, Vol. 4, Issue 3 https://doi.org/10.1111/j.1749-4877.2009.00167.x	journal	September 2009
The Premetazoan Ancestry of Cadherins Abedin, Monika; King, Nicole Science, Vol. 319, Issue 5865 https://doi.org/10.1126/science.1151084	journal	February 2008
The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution Ryan, J. F.; Pang, K.; Schnitzler, C. E. Science, Vol. 342, Issue 6164 https://doi.org/10.1126/science.1242592	journal	December 2013
What nervous systems do: early evolution, input–output, and the skin brain thesis Keijzer, Fred; van Duijn, Marc; Lyon, Pamela Adaptive Behavior, Vol. 21, Issue 2 https://doi.org/10.1177/1059712312465330	journal	February 2013
MAGUKs, Synaptic Development, and Synaptic Plasticity Zheng, Chan-Ying; Seabold, Gail K.; Horak, Martin The Neuroscientist, Vol. 17, Issue 5 https://doi.org/10.1177/1073858410386384	journal	April 2011
The Porifera Ontology (PORO): enhancing sponge systematics with an anatomy ontology Thacker, Robert W.; Díaz, Maria; Kerner, Adeline Journal of Biomedical Semantics, Vol. 5, Issue 1 https://doi.org/10.1186/2041-1480-5-39	journal	January 2014
Making the connection – shared molecular machinery and evolutionary links underlie the formation and plasticity of occluding junctions and synapses Harden, Nicholas; Wang, Simon Ji Hau; Krieger, Charles Journal of Cell Science, Vol. 129, Issue 16 https://doi.org/10.1242/jcs.186627	journal	August 2016
Modeling spontaneous activity across an excitable epithelium: Support for a coordination scenario of early neural evolution de Wiljes, Oltman O.; van Elburg, Ronald A. J.; Biehl, Michael Frontiers in Computational Neuroscience, Vol. 9 https://doi.org/10.3389/fncom.2015.00110	journal	September 2015
The Amphimedon queenslandica genome and the evolution of animal complexity Srivastava, M.; Simakov, O.; Chapman, J. Nature Publishing Group https://doi.org/10.5167/uzh-42259	text	January 2010
RNA interference in marine and freshwater sponges Rivera, Ajna S.; Hammel, Jörg U.; Haen, Karri M. Universitätsbibliothek der Ludwig-Maximilians-Universität München https://doi.org/10.5282/ubm/epub.13703	text	January 2011

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59 BASIC BIOLOGICAL SCIENCES
Evolutionary genetics
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A Post-Synaptic Scaffold at the Origin of the Animal Kingdom

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