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Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics
Open accessAbstract
Background: Molecular and genetic analyses conducted in model organisms such as Drosophila and vertebrates, have provided a wealth of information about how networks of transcription factors control the proper development of these species. Much less is known, however, about the evolutionary origin of these elaborated networks and their large-scale evolution. Here we report the first evolutionary analysis of a whole superfamily of transcription factors, the basic helix-loop-helix (bHLH) proteins, at the scale of the whole metazoan kingdom. Results: We identified in silico the putative full complement of bHLH genes in the sequenced genomes of 12 different species representative of the main metazoan lineages, including three non-bilaterian metazoans, the cnidarians Nematostella vectensis and Hydra magnipapillata and the demosponge Amphimedon queenslandica. We have performed extensive phylogenetic analyses of the 695 identified bHLHs, which has allowed us to allocate most of these bHLHs to defined evolutionary conserved groups of orthology. Conclusion: Three main features in the history of the bHLH gene superfamily can be inferred from these analyses: (i) an initial diversification of the bHLHs has occurred in the pre-Cambrian, prior to metazoan cladogenesis; (ii) a second expansion of the bHLH superfamily occurred early in metazoan evolution before bilaterians and cnidarians diverged; and (iii) the bHLH complement during the evolution of the bilaterians has been remarkably stable. We suggest that these features may be extended to other developmental gene families and reflect a general trend in the evolution of the developmental gene repertoires of metazoans.
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Citations
Cites
CAP3: A DNA Sequence Assembly Program
Huang, X., & Madan, A. (1999) · Genome Research · doi:10.1101/gr.9.9.868 · Cited by 5,261
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638 · cited 1×
“Since this ancestor which is estimated to have lived some 600–700 millions years ago [24,25], the bHLH complement in bilaterians is remarkably stable.”
BackgroundUnexpected complexity of the Wnt gene family in a sea anemone
Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q., et al. (2005) · Nature · doi:10.1038/nature03158 · Cited by 599
The new animal phylogeny: Reliability and implications
Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B., & de Rosa, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4453 · Cited by 512 · cited 1×
“The tree is based on the current view of the phylogeny of the metazoans [73,74].”
BackgroundEstimating metazoan divergence times with a molecular clock
Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J., & McPeek, M. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401670101 · Cited by 461
Evolution of Key Cell Signaling and Adhesion Protein Families Predates Animal Origins
King, N., Hittinger, C. T., & Carroll, S. B. (2003) · Science · doi:10.1126/science.1083853 · Cited by 424
Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004) · Development · doi:10.1242/dev.01119 · Cited by 396
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
Sponge 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
Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements
Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R. B., Rentzsch, F., Renfer, E., Jensen, M. F., Zhu, B., de Jong, P., Steele, R. E., et al. (2006) · Nature · doi:10.1038/nature04863 · Cited by 197
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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
Self-citationThe deep evolution of metazoan microRNAs
Wheeler, B. M., Heimberg, A. M., Moy, V. N., Sperling, E. A., Holstein, T. W., Heber, S., & Peterson, K. J. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00302.x · Cited by 534
Goding, C. R., & Arnheiter, H. (2019) · Genes & Development · doi:10.1101/gad.324657.119 · Cited by 430
Adamska, M., Degnan, S. M., Green, K. M., Adamski, M., Craigie, A., Larroux, C., & Degnan, B. M. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001031 · Cited by 257
Self-citationOsborne, T. F., & Espenshade, P. J. (2009) · Genes & Development · doi:10.1101/gad.1854309 · Cited by 238
On the Independent Origins of Complex Brains and Neurons
Moroz, L. L. (2009) · Brain, Behavior and Evolution · doi:10.1159/000258665 · Cited by 209
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
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
Sebe-Pedros, A., de Mendoza, A., Lang, B. F., Degnan, B. M., & Ruiz-Trillo, I. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msq309 · Cited by 195
Self-citationThe phylogenetic position of ctenophores and the origin(s) of nervous systems
Jákely, G., Paps, J., & Nielsen, C. (2015) · EvoDevo · doi:10.1186/2041-9139-6-1 · Cited by 189
Deep conservation of the enhancer regulatory code in animals
Wong, E. S., Zheng, D., Tan, S. Z., Bower, N. I., Garside, V., Vanwalleghem, G., Gaiti, F., Scott, E., Hogan, B. M., Kikuchi, K., et al. (2020) · Science · doi:10.1126/science.aax8137 · Cited by 176
Self-citationThe 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
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
Sperling, E. A., Peterson, K. J., & Pisani, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp148 · Cited by 172
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
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
Self-citationDiversity as opportunity: Insights from 600 million years of AHR evolution
Hahn, M. E., Karchner, S. I., & Merson, R. R. (2017) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2017.02.003 · Cited by 134
The Physiology and Molecular Biology of Sponge Tissues
Leys, S. P., & Hill, A. (2012) · Advances in Marine Biology · doi:10.1016/b978-0-12-394283-8.00001-1 · Cited by 128
The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments
Mills, D. B., Francis, W. R., Vargas, S., Larsen, M., Elemans, C. P., Canfield, D. E., & Wörheide, G. (2018) · eLife · doi:10.7554/elife.31176 · Cited by 114
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112
Layden, M. J., Boekhout, M., & Martindale, M. Q. (2012) · Development · doi:10.1242/dev.073221 · Cited by 98
Evolution of eumetazoan nervous systems: insights from cnidarians
Kelava, I., Rentzsch, F., & Technau, U. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0065 · Cited by 84
PETERSON, K. J., SUMMONS, R. E., & DONOGHUE, P. C. J. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2007.00692.x · Cited by 93
A two‐step process in the emergence of neurogenesis
Galliot, B., & Quiquand, M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07829.x · Cited by 77
Evolution: Ctenophore Genomes and the Origin of Neurons
Marlow, H., & Arendt, D. (2014) · Current Biology · doi:10.1016/j.cub.2014.06.057 · Cited by 71
Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi
Pang, K., & Martindale, M. Q. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0222-3 · Cited by 70
Degnan, S. M., & Degnan, B. M. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0248 · Cited by 71
Self-citationEmbryonic expression of zebrafish MiT family genes tfe3b, tfeb, and tfec
Lister, J. A., Lane, B. M., Nguyen, A., & Lunney, K. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22743 · Cited by 61
Markov, G. V., Paris, M., Bertrand, S., & Laudet, V. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.06.011 · Cited by 48
Metadata
- Authors
- Simionato, E., Ledent, V., Richards, G., Thomas-Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M.
- Venue
- BMC Evolutionary Biology
- Published
- 2007-03-02
- Volume
- 7
- Issue
- 1
- Pages
- 33-33
- ISSN
- 1471-2148 (ISSN-L)
- OpenAlex
- W1988011675
- Cited by
- 288
- References
- 12
- FWCI
- 9.22
- Type
- journal article
- Language
- en
- Open access
- gold
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