skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning

Journal Article · · PLoS ONE

Background. The origin of metazoan development and differentiation was contingent upon the evolution of cell adhesion, communication and cooperation mechanisms. While components of many of the major cell signalling pathways have been identified in a range of sponges (phylum Porifera), their roles in development have not been investigated and remain largely unknown. Here, we take the first steps toward reconstructing the developmental signalling systems used in the last common ancestor to living sponges and eumetazoans by studying the expression of genes encoding Wnt and TGF-b signalling ligands during the embryonic development of a sponge. Methodology/Principal Findings. Using resources generated in the recent sponge Amphimedon queenslandica (Demospongiae) genome project, we have recovered genes encoding Wnt and TGFb signalling ligands that are critical in patterning metazoan embryos. Both genes are expressed from the earliest stages of Amphimedon embryonic development in highly dynamic patterns. At the time when the Amphimedon embryos begin to display anterior-posterior polarity, Wnt expression becomes localised to the posterior pole and this expression continues until the swimming larva stage. In contrast, TGF-b expression is highest at the anterior pole. As in complex animals, sponge Wnt and TGF-b expression patterns intersect later in development during the patterning of a sub-community of cells that form a simple tissue-like structure, the pigment ring. Throughout development, Wnt and TGF-b are expressed radially along the anteriorposterior axis. Conclusions/Significance. We infer from the expression of Wnt and TGF-b in Amphimedon that the ancestor that gave rise to sponges, cnidarians and bilaterians had already evolved the capacity to direct the formation of relatively sophisticated body plans, with axes and tissues. The radially symmetrical expression patterns of Wnt and TGF-b along the anterior-posterior axis of sponge embryos and larvae suggest that these signalling pathways contributed to establishing axial polarity in the very first metazoans.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Australian Research Council (ARC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627337
Journal Information:
PLoS ONE, Vol. 2, Issue 10; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (48)

The establishment of spemann's organizer and patterning of the vertebrate embryo journal December 2000
The evolution of metazoan axial properties journal November 2005
Formation of the head organizer in hydra involves the canonical Wnt pathway journal June 2005
Cnidarians and ancestral genetic complexity in the animal kingdom journal October 2005
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. text January 2018
Molecular evidence for deep evolutionary roots of bilaterality in animal development journal July 2006
Precambrian Sponges with Cellular Structures journal February 1998
Localized expression of a dpp/BMP2/4 ortholog in a coral embryo journal June 2002
Genetic interaction between Wnt/ -catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb journal July 2003
Morphogen gradients, positional information, andXenopus: Interplay of theory and experiment journal November 2002
Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: Implications for the evolution of axial patterning journal August 2006
Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. journal December 1995
Requirement for Wnt3 in vertebrate axis formation journal August 1999
Sponge paraphyly and the origin of Metazoa: Sponge paraphyly journal January 2001
HyBMP5-8b , a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra journal March 2004
From The Cover: Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record journal June 2005
Sponge Paleogenomics Reveals an Ancient Role for Carbonic Anhydrase in Skeletogenesis journal June 2007
The NK Homeobox Gene Cluster Predates the Origin of Hox Genes journal April 2007
Interaction between Wnt and TGF-β signalling pathways during formation of Spemann's organizer journal February 2000
Nodal/activin signaling establishes oral-aboral polarity in the early sea urchin embryo journal December 2004
Sponge Development and Antiquity of Animal Pattern Formation journal April 2005
The New View of Animal Phylogeny journal December 2004
Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics journal January 2007
Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes journal September 2002
A Post-Synaptic Scaffold at the Origin of the Animal Kingdom journal June 2007
Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence journal November 1996
Cooperation Between TGF-β and Wnt Pathways During Chondrocyte and Adipocyte Differentiation of Human Marrow Stromal Cells journal December 2003
Developmental expression of AmphiWnt1 , an amphioxus gene in the Wnt1 / wingless subfamily journal September 2000
Isolation and characterization of Wnt pathway-related genes from Porifera☆ journal September 2007
Multiple TGF-β receptor related genes in sponge and ancient gene duplications before the parazoan-eumetazoan split 1 journal June 1999
A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians journal April 2006
Early evolution of animal cell signaling and adhesion genes journal August 2006
From The Cover: Reconstructing early sponge relationships by using the Burgess Shale fossil Eiffelia globosa, Walcott journal January 2005
Phylogeny and Evolution of Calcareous Sponges: Monophyly of Calcinea and Calcaronea, High Level of Morphological Homoplasy, and the Primitive Nature of Axial Symmetry journal June 2003
Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA journal August 2001
Unexpected complexity of the Wnt gene family in a sea anemone journal January 2005
Phylogeny of Choanozoa, Apusozoa, and Other Protozoa and Early Eukaryote Megaevolution journal May 2003
The last common bilaterian ancestor journal July 2002
Allocation of the thoracic imaginal primordia in the Drosophila embryo journal February 1993
A molecular basis for transdetermination in Drosophila imaginal discs: interactions between wingless and decapentaplegic signaling journal January 1998
GDF-3 and GDF-9: two new members of the transforming growth factor-beta superfamily containing a novel pattern of cysteines. journal February 1993
Osteogenic protein-2. A new member of the transforming growth factor-beta superfamily expressed early in embryogenesis. journal December 1992
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. text January 2018
Wnt genes journal June 1992
The evolutionary origin of hedgehog proteins journal October 2007
Polarity factor ‘Frizzled’ in the demosponge Suberites domuncula : identification, expression and localization of the receptor in the epithelium/pinacoderm 1 journal October 2003
One hundred years of positional information journal September 1996
Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity journal March 2006

Cited By (76)

Demosponge EST Sequencing Reveals a Complex Genetic Toolkit of the Simplest Metazoans journal July 2010
Current Perspectives on the Use of Alternative Species in Human Health and Ecological Hazard Assessments journal September 2013
Developmental Drift and the Role of Wnt Signaling in Aging journal August 2016
The significance of sponges for comparative studies of developmental evolution journal July 2019
Evolution of the TGF-β Signaling Pathway and Its Potential Role in the Ctenophore, Mnemiopsis leidyi journal September 2011
Early origin of the bilaterian developmental toolkit journal August 2009
An option space for early neural evolution journal December 2015
Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges: Piwi expression in archeocytes and choanocytes journal May 2010
Differential Responses to Wnt and PCP Disruption Predict Expression and Developmental Function of Conserved and Novel Genes in a Cnidarian journal September 2014
Wnt signaling and polarity in freshwater sponges journal February 2018
Embryonic expression of priapulid Wnt genes journal July 2019
Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity journal April 2017
Co-expression of synaptic genes in the sponge Amphimedon queenslandica uncovers ancient neural submodules journal October 2019
Evidence for Involvement of Wnt Signalling in Body Polarities, Cell Proliferation, and the Neuro-Sensory System in an Adult Ctenophore journal December 2013
Secreted frizzled related protein is a target of PaxB and plays a role in aquiferous system development in the freshwater sponge, Ephydatia muelleri journal February 2019
The Trichoplax genome and the nature of placozoans journal August 2008
Evolution of phototaxis journal October 2009
Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty journal April 2018
Dynamic and Widespread lncRNA Expression in a Sponge and the Origin of Animal Complexity journal May 2015
The Amphimedon queenslandica genome and the evolution of animal complexity text January 2010
Evolutionary origin of gastrulation: insights from sponge development journal January 2014
Early metazoan cell type diversity and the evolution of multicellular gene regulation journal June 2018
Structure, function and disease relevance of Wnt inhibitory factor 1, a secreted protein controlling the Wnt and hedgehog pathways journal March 2019
Phylogenetic evidence for the modular evolution of metazoan signalling pathways journal February 2017
Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans journal May 2014
Genome-wide features of introns are evolutionary decoupled among themselves and from genome size throughout Eukarya posted_content March 2018
The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution journal February 2010
The Analysis of Eight Transcriptomes from All Poriferan Classes Reveals Surprising Genetic Complexity in Sponges journal February 2014
On the evolution of bilaterality journal October 2017
Surprisingly rich repertoire of Wnt genes in the demosponge Halisarca dujardini journal June 2016
Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis journal November 2011
Wound Repair and Regeneration book March 2018
Hox-cluster and evolution of morphogeneses journal September 2010
TCF/Lef regulates the Gsx ParaHox gene in central nervous system development in chordates journal March 2016
Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer: Polarity in sponges journal September 2010
Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics: The disconnect between gene content and body plan evolution journal August 2018
Wound repair and regeneration journal May 2008
Cellular and molecular processes leading to embryo formation in sponges: evidences for high conservation of processes throughout animal evolution journal April 2012
A Phylogenomic Investigation into the Origin of Metazoa journal January 2008
Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis journal January 2012
Insights into the evolution of metazoan regenerative mechanisms: TGF superfamily member roles in tissue regeneration of the marine sponge Chondrosia reniformis Nardo, 1847 journal January 2019
Evo-devo of non-bilaterian animals journal August 2015
The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development journal January 2012
A Comparative Perspective on Wnt/β-Catenin Signalling in Cell Fate Determination book January 2017
Genesis and Expansion of Metazoan Transcription Factor Gene Classes journal February 2008
A novel gene’s role in an ancient mechanism: secreted Frizzled-related protein 1 is a critical component in the anterior–posterior Wnt signaling network that governs the establishment of the anterior neuroectoderm in sea urchin embryos journal January 2018
Distinct interactions between epithelial and mesenchymal cells control cell morphology and collective migration during sponge epithelial to mesenchymal transition journal December 2019
Sponge Long Non-Coding RNAs Are Expressed in Specific Cell Types and Conserved Networks journal March 2018
Structural Biology and Evolution of the TGF-β Family journal September 2016
The origins of developmental gene regulation: ­­­­The origins of developmental gene regulation journal January 2017
Structure, function and disease relevance of Wnt inhibitory factor 1, a secreted protein controlling the Wnt and hedgehog pathways text January 2019
Wnt signal transduction pathways: modules, development and evolution journal August 2016
Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals journal October 2008
Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica: Wnt pathway components in Amphimedon queenslandica journal September 2010
The Amphimedon queenslandica genome and the evolution of animal complexity journal August 2010
Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development journal January 2018
An Option Space for Early Neural Evolution posted_content September 2015
Structure, function and disease relevance of Wnt inhibitory factor 1, a secreted protein controlling the Wnt and hedgehog pathways text January 2019
Lysine Conservation and Context in TGFβ and Wnt Signaling Suggest New Targets and General Themes for Posttranslational Modification journal September 2008
Wnt Signaling and the Polarity of the Primary Body Axis journal December 2009
Phylogenomics Revives Traditional Views on Deep Animal Relationships journal April 2009
Evolution of the NET (NocA, Nlz, Elbow, TLP-1) protein family in metazoans: insights from expression data and phylogenetic analysis journal December 2016
Glycoprotein Hormones and Their Receptors Emerged at the Origin of Metazoans journal June 2014
Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes journal October 2009
Emergence, development and diversification of the TGF-β signalling pathway within the animal kingdom journal January 2009
Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions journal May 2012
Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma journal September 2009
Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla journal January 2007
Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi journal October 2010
Fish connectivity mapping: linking chemical stressors by their mechanisms of action-driven transcriptomic profiles journal January 2016
Integration of Canonical and Noncanonical Wnt Signaling Pathways Patterns the Neuroectoderm Along the Anterior–Posterior Axis of Sea Urchin Embryos journal January 2013
Gene Classification Based on Amino Acid Motifs and Residues: The DLX (distal-less) Test Case journal June 2009
WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella journal June 2009
Origin and Evolution of Dishevelled journal February 2013
Rho Family of Ras-Like GTPases in Early-Branching Animals journal October 2020
The evolution of gene regulation journal May 2017