Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica
Abstract
SUMMARY Wnt‐signalling plays a critical role in animal development, and its misregulation results in serious human diseases, including cancer. While the Wnt pathway is well studied in eumetazoan models, little is known about the evolutionary origin of its components and their functions. Here, we have identified key machinery of the Wnt–β‐catenin (canonical)‐signalling pathway that is encoded in the Amphimedon queenslandica (Demospongiae; Porifera) genome, namely Wnt, Fzd, SFRP, Lrp5/6, Dvl, Axin, APC, GSK3, β‐catenin, Tcf, and Groucho. Most of these genes are not detected in the choanoflagellate and other nonmetazoan eukaryotic genomes. In contrast, orthologues of some of key components of bilaterian Wnt–planar cell polarity and Wnt/Ca 2+ are absent from the Amphimedon genome, suggesting these pathways evolved after demosponge and eumetazoan lineages diverged. Sequence analysis of the identified proteins of the Wnt–β‐catenin pathway has revealed the presence of most of the conserved motifs and domains responsible for protein–protein and protein–DNA interactions in vertebrates and insects. However, several protein–protein interaction domains appear to be absent from the Amphimedon Axin and APC proteins. These are also missing from their orthologues in the cnidarian Nematostella vectensis , suggesting that they are bilaterian novelties. All of the analyzed Wnt pathway genes are expressed in specific patterns during Amphimedon embryogenesis. Most are expressed in especially striking and highly dynamic patterns during formation of a simple organ‐like larval structure, the pigment ring. Overall, our results indicate that the Wnt–β‐catenin pathway was used in embryonic patterning in the last common ancestor of living metazoans. Subsequently, gene duplications and a possible increase in complexity of protein interactions have resulted in the precisely regulated Wnt pathway observed in extant bilaterian animals.
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Previous analysis of gene expression during embryonic development of Amphimedon showed that all key components of the canonical Wnt pathway are expressed throughout the outer layer of embryos and larvae.
“Previous analysis of gene expression during embryonic development of Amphimedon is consistent with this view: all of the key components of the canonical Wnt pathway are expressed throughout the outer layer of embryos and larvae 42 .”
From Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans (2014) · cites this paper as [42]
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Oosterveen, T., Coudreuse, D. Y. M., Yang, P., Fraser, E., Bergsma, J., Dale, T. C., & Korswagen, H. C. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.05.043 · Cited by 28 · see citing works
Wnt Signaling in Stem Cells and Lung Cancer
He, B., & Jablons, D. M. (2007) · Springer eBooks · doi:10.1007/2789_2007_043 · Cited by 26 · see citing works
Whole-Mount In Situ Hybridization in AmphimedonPreprint
Larroux, C., Fahey, B., Adamska, M., Richards, G. S., Gauthier, M., Green, K., Lovas, E. M., & Degnan, B. M. (2008) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5096 · Cited by 21 · see citing works
Self-citationAnalysis of Cell Movement in Amphimedon Embryos by Injection of Fluorescent TracersPreprint
Adamska, M., & Degnan, B. M. (2008) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5097 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
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Sorted by citations
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
Independent evolution of striated muscles in cnidarians and bilaterians
Steinmetz, P. R. H., Kraus, J. E. M., Larroux, C., Hammel, J. U., Amon-Hassenzahl, A., Houliston, E., Wörheide, G., Nickel, M., Degnan, B. M., & Technau, U. (2012) · Nature · doi:10.1038/nature11180 · Cited by 252 · see citing works
Self-citationThe hidden biology of sponges and ctenophores
Dunn, C. W., Leys, S. P., & Haddock, S. H. D. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.03.003 · Cited by 212 · see citing works
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
The Evolutionary History of YAP and the Hippo/YAP Pathway
Hilman, D., & Gat, U. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr065 · Cited by 166 · see citing works
Deep Phylogeny and Evolution of Sponges (Phylum Porifera)
Wörheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C., & Lavrov, D. V. (2012) · Advances in Marine Biology · doi:10.1016/b978-0-12-387787-1.00007-6 · Cited by 166 · see citing works
Self-citationElements of a ‘nervous system’ in sponges
Leys, S. P. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110817 · Cited by 138 · see citing works
Neuroglialpharmacology: Myelination as a shared mechanism of action of psychotropic treatments
Bartzokis, G. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.015 · Cited by 142 · see citing works
Leininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136 · see citing works
Self-citationOrigin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record
Tweedt, S. M., & Erwin, D. H. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_3 · Cited by 27 · see citing works
- Authors
- Adamska, M., Larroux, C., Adamski, M., Green, K., Lovas, E., Koop, D., Richards, G. S., Zwafink, C., & Degnan, B. M.
- Affiliations
- The University of Queensland (AU)
- Corresponding author
- Degnan, Bernard M.
- Venue
- Evolution & Development
- Publisher
- Wiley
- Published
- 2010-09
- Volume
- 12
- Issue
- 5
- Pages
- 494-518
- ISSN
- 1520-541X (ISSN-L)
- 1525-142X
- OpenAlex
- W1605394511
- Cited by
- 139
- References
- 99
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 4 · 2022: 7 · 2021: 13 · 2020: 3 · 2019: 10 · 2018: 11 · 2017: 4 · 2016: 12 · 2015: 12 · 2014: 11 · 2013: 12 · 2012: 18
- FWCI
- 5.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Evolution & Development (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- University of Queensland
- Australian Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- Wnt signaling, canonical Wnt/β-catenin pathway, Amphimedon queenslandica, demosponges, embryonic patterning, Axin, APC, gene duplication, protein-protein interaction domains, Nematostella vectensis, sponges, metazoan origin
- MeSH terms
- Animals, Embryo, Nonmammalian, Biological Evolution, Phylogeny, Porifera, Signal Transduction, Protein Structure, Tertiary, Gene Expression Regulation, Developmental, Body Patterning, Embryonic Development, Wnt Proteins, Frizzled Receptors, beta Catenin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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