Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals
Abstract
Developmental transcription factors (DTFs) control development of animals by affecting expression of target genes, some of which are transcription factors themselves. In bilaterians and cnidarians, conserved DTFs are involved in homologous processes such as gastrulation or specification of neurons. The genome of Amphimedon queenslandica, the first sponge to be sequenced, revealed that only a fraction of these conserved DTF families are present in demosponges. This finding was in line with the view that morphological complexity in the animal lineage correlates with developmental toolkit complexity. However, as the phylum Porifera is very diverse, Amphimedon's genome may not be representative of all sponges. The recently sequenced genomes of calcareous sponges Sycon ciliatum and Leucosolenia complicata allowed investigations of DTFs in a sponge lineage evolutionarily distant from demosponges. Surprisingly, the phylogenetic analyses of identified DTFs revealed striking differences between the calcareous sponges and Amphimedon. As these differences appear to be a result of independent gene loss events in the two sponge lineages, the last common ancestor of sponges had to possess a much more diverse repertoire of DTFs than extant sponges. Developmental expression of sponge homologs of genes involved in specification of the Bilaterian endomesoderm and the neurosensory cells suggests that roles of many DTFs date back to the last common ancestor of all animals. Strikingly, even DTFs displaying apparent pan-metazoan conservation of sequence and function are not immune to being lost from individual species genomes. The quest for a comprehensive picture of the developmental toolkit in the last common metazoan ancestor is thus greatly benefitting from the increasing accessibility of sequencing, allowing comparisons of multiple genomes within each phylum.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Genomic and transcriptomic databases are becoming available for several sponge species and for the placozoan Trichoplax adhaerens.
“an extensive set of genomic and transcriptomic databases is becoming available for several sponge species -Amphimedon queenslandica, Oscarella carmela and Sycon ciliatum, as well as for a placozoan Trichoplax adhaerens [22–25]”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [24]
Cites
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 · see citing works
A census of human transcription factors: function, expression and evolution
Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A., & Luscombe, N. M. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2538 · Cited by 1,573 · see citing works
Sea 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
The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
Self-citationAssessing 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 · see citing works
The ctenophore genome and the evolutionary origins of neural systems
Moroz, L. L., Kocot, K. M., Citarella, M. R., Dosung, S., Norekian, T. P., Povolotskaya, I. S., Grigorenko, A. P., Dailey, C., Berezikov, E., Buckley, K. M., et al. (2014) · Nature · doi:10.1038/nature13400 · Cited by 716 · see citing works
The Genome of the Ctenophore <i>Mnemiopsis leidyi</i> and Its Implications for Cell Type Evolution
Ryan, J. F., Pang, K., Schnitzler, C. E., Nguyen, A.-D., Moreland, R. T., Simmons, D. K., Koch, B. J., Francis, W. R., Havlak, P., Program, N. C. S., et al. (2013) · Science · doi:10.1126/science.1242592 · Cited by 702 · see citing works
Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396 · 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 · see citing works
Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians
Technau, U., Rudd, S., Maxwell, P., Gordon, P. M. K., Saina, M., Grasso, L. C., Hayward, D. C., Sensen, C. W., Saint, R., Holstein, T. W., et al. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.09.007 · Cited by 337 · see citing works
The Capsaspora genome reveals a complex unicellular prehistory of animals
Suga, H., Chen, Z., de Mendoza, A., Sebé-Pedrós, A., Brown, M. W., Kramer, E., Carr, M., Kerner, P., Vervoort, M., Sánchez-Pons, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3325 · Cited by 317 · 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
Self-citationSponge paraphyly and the origin of Metazoa
Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N., Vacelet, J., & Le Parco, Y. (2001) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2001.00244.x · Cited by 275 · 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
Cnidarians and the evolutionary origin of the nervous system
Watanabe, H., Fujisawa, T., & Holstein, T. W. (2009) · Development, Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01103.x · Cited by 206 · see citing works
The NK homeobox gene cluster predates the origin of Hox genes.
Larroux, C., Fahey, B., Degnan, S. M., Adamski, M., Rokhsar, D. S., & Degnan, B. M. (2007) · Current Biology · doi:10.1016/j.cub.2007.03.008 · Cited by 173 · see citing works
Sperling, E. A., Peterson, K. J., & Pisani, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp148 · Cited by 172 · see citing works
Origins of neurogenesis, a cnidarian view
Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., & Chera, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.563 · Cited by 168 · see citing works
Ryan, J. F., Pang, K., Program, N. C. S., Mullikin, J. C., Martindale, M. Q., & Baxevanis, A. D. (2010) · EvoDevo · doi:10.1186/2041-9139-1-9 · Cited by 160 · see citing works
Röttinger, E., Dahlin, P., & Martindale, M. Q. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003164 · Cited by 140 · 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-citationNo longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera
Gazave, E., Lapébie, P., Ereskovsky, A. V., Vacelet, J., Renard, E., Cárdenas, P., & Borchiellini, C. (2012) · Hydrobiologia · doi:10.1007/s10750-011-0842-x · Cited by 126 · see citing works
Evolution of the TGF-β Signaling Pathway and Its Potential Role in the Ctenophore, Mnemiopsis leidyi
Pang, K., Ryan, J. F., Baxevanis, A. D., & Martindale, M. Q. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024152 · Cited by 93 · see citing works
Novel scenarios of early animal evolution--is it time to rewrite textbooks?
Dohrmann, M., & Worheide, G. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict008 · Cited by 71 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Back to the Basics: Cnidarians Start to Fire
Bosch, T. C. G., Klimovich, A., Domazet-Lošo, T., Gründer, S., Holstein, T. W., Jékely, G., Miller, D. J., Murillo-Rincon, A. P., Rentzsch, F., Richards, G. S., et al. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2016.11.005 · Cited by 144 · see citing works
Ferrier, D. E. K. (2016) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv056 · Cited by 28 · see citing works
- Authors
- Fortunato, S. A. V., Adamski, M., & Adamska, M.
- Affiliations
- University of Bergen (NO)
- Corresponding author
- Adamska, Maja
- Venue
- Marine Genomics
- Publisher
- Elsevier BV
- Published
- 2015-12
- Volume
- 24
- Pages
- 121-129
- ISSN
- 1874-7787 (ISSN-L)
- OpenAlex
- W1115029164
- Cited by
- 31
- References
- 25
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 1 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 4 · 2017: 4 · 2016: 8 · 2015: 3
- FWCI
- 0.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Marine Genomics (publishedVersion)
- PubMed (publishedVersion)
- ResearchOnline - JCU (James Cook University) (submittedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- Funders
- Sars International Centre for Marine Molecular Biology, Bergen, Norway
- 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 › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Keywords
- developmental transcription factors, sponges, Amphimedon queenslandica, Sycon ciliatum, Leucosolenia complicata, calcareous sponges, demosponges, gene loss, endomesoderm specification, sponge evolution, gene family evolution
- MeSH terms
- Animals, Biological Evolution, Porifera, Transcription Factors, Gene Expression Regulation, Developmental
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
