Caught in the evolutionary act: Precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins
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The regulatory control of otxbeta1/2 in the sea urchin Strongylocentrotus purpuratus and the sea star Asterina miniata provides an exceptional opportunity to determine the genomic basis of evolutionary change in gene regulatory network (GRN) architectures. Network perturbation analyses in both taxa show that Otx regulates the transcription factors gatae and krox/blimp1 and both of these transcription factors also feed back and regulate otx. The otx gene also autoregulates. This three way interaction is an example of a GRN kernel. It has been conserved for 500 million years since these two taxa last shared a common ancestor. Amid this high level of conservation we show here one significant regulatory change. Tbrain is required for correct otxbeta1/2 expression in the sea star but not in the sea urchin. In sea urchin, tbrain is not co-expressed with otxbeta1/2 and instead has an essential role in specification of the embryonic skeleton. Tbrain in these echinoderms is thus a perfect example of an orthologous gene co-opted for entirely different developmental processes. We isolate and test the sea star otxbeta1/2 cis-regulatory module and demonstrate functional binding sites for each of the predicted inputs, including Tbrain. We compare it to the logic processing operating in the sea urchin otxbeta1/2 cis-regulatory module and present an evolutionary scenario of the change in Tbrain dependence. Finally, inter-specific gene transfer experiments confirm this scenario and demonstrate evolution occurring at the level of sequence changes to the cis-regulatory module.
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In functional assays inserting known cis-regulatory modules into genomes of different species, only the specific transcription factor target sites are retained, spaced in nonconserved DNA sequence, often in diverse site order and number.
“In such examples, where functional assays carried out by insertion of known cis -regulatory modules into the genomes of different species reveal conserved function, it is found that only the speci fi c transcription factor (TF) target sites are retained, spaced in nonconserved DNA sequence, often in diverse site order and number (9 -11).”
From Transphyletic conservation of developmental regulatory state in animal evolution (2011) · cites this paper as [11]
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Kadri, S. (2012) · KiltHub Repository · doi:10.1184/r1/6720632
Wessel, G. M. (2021) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.739152243.793581573
Reyes, G., Oulhen, N., & Wessel, G. M. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.02.016
- Authors
- Hinman, V. F., Nguyen, A., & Davidson, E. H.
- Affiliations
- Carnegie Mellon University (US)
- California Institute of Technology (US)
- Corresponding author
- Hinman, Veronica F.
- ORCID
- Hinman, Veronica F.
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2007-12
- Volume
- 312
- Issue
- 2
- Pages
- 584-595
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2037112883
- Cited by
- 67
- References
- 46
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 4 · 2019: 2 · 2018: 2 · 2017: 7 · 2016: 7 · 2015: 3 · 2014: 5 · 2013: 3 · 2012: 7
- FWCI
- 1.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2055 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- cis-regulatory modules, gene regulatory networks, Strongylocentrotus purpuratus, echinoderm evolution, autoregulation, cis-regulatory evolution
- MeSH terms
- Animals, Cloning, Molecular, Embryo, Nonmammalian, Genes, Regulator, Sea Urchins, Gene Expression Regulation, Developmental, Evolution, Molecular, Asterina, Otx Transcription Factors, Gene Regulatory Networks
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