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Evolutionary plasticity of developmental gene regulatory network architecture
Open accessAbstract
Sea stars and sea urchins evolved from a last common ancestor that lived at the end of the Cambrian, approximately half a billion years ago. In a previous comparative study of the gene regulatory networks (GRNs) that embody the genomic program for embryogenesis in these animals, we discovered an almost perfectly conserved five-gene network subcircuit required for endoderm specification. We show here that the GRN structure upstream and downstream of the conserved network kernel has, by contrast, diverged extensively. Mesoderm specification is accomplished quite differently; the Delta–Notch signaling system is used in radically distinct ways; and various regulatory genes have been coopted to different functions. The conservation of the conserved kernel is thus the more remarkable. The results indicate types of network linkage subject to evolutionary change. An emergent theme is that subcircuit design may be preserved even while the identity of genes performing given roles changes because of alteration in their cis -regulatory control systems.
Checked 2026-10-06 · 3 references not checked yet
Overview
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Written from the paper’s full text.
TL;DR
Comparing endomesoderm gene regulatory networks (GRNs) in a sea star and a sea urchin, the authors find that a conserved five-gene kernel is surrounded by extensive rewiring of upstream and downstream linkages. Delta-Notch signaling, regulatory gene cooption, and mesoderm/endoderm boundary mechanisms differ radically, even though some subcircuit logic is preserved.
Key findings
- The previously identified five-gene endomesoderm kernel is highly conserved, but outside it “not one of the genes included in Fig. 5 has all of the same regulatory inputs in the two GRNs.”
- Delta-Notch deployment is radically different: in sea urchins Delta-N signaling specifies mesoderm via gcm and pigment cells, whereas sea star gcm is not expressed in the vegetal plate, gcm transcription is unaffected by Delta MASO, and sea stars form no embryonic pigment cells.
- A second Delta-N role is conserved: Delta is required for gatae expression and endoderm specification in both species; in sea stars, blocking Delta expands mesodermal gatac and ets1/2 expression and produces excessive migratory blastocoelar cells.
- tbr is coopted in sea urchins for skeletogenic function, while in sea stars it has the pleisiomorphic endomesodermal role; tbr MASO abolishes from >65% to ≈80% of expression of otxβ1/2, foxa, bra, gatae, tbr itself, and otxα.
Methods
- Comparative GRN analysis between Asterina miniata (sea star) and Strongylocentrotus purpuratus (sea urchin), whose last common ancestor existed ≈500 million years ago in the Late Cambrian.
- A. miniata orthologs of delta, ets1/2, and gatac were cloned by low-stringency hybridization and sequenced; spatial expression was assayed by whole-mount in situ hybridization and alkaline phosphatase staining.
- Gene function was perturbed with morpholino-substituted antisense oligonucleotides (MASOs) targeting Delta, Tbr, Foxa, and Gatae, with quantitative PCR used to measure transcript levels in MASO-treated versus control embryos.
Limitations
- The paper states that many linkages in the sea star GRN are still missing, including what causes initial mesodermal gatac expression, and notes that some Fig. 5 interactions are dashed because evidence suggests they are indirect.
- The paper states that gatae up-regulation in the anterior bulb after Delta-N blockade occurs “for reasons not yet known.”
- Evident from the text: the comparison is limited to two echinoderm species, and several cis-regulatory conclusions are inferred or predicted rather than directly tested in both systems.
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“Brachyury (bra ), which is expressed normally around the blastopore is similarly unaffected (SI Fig. 6).”
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“Nor does gcm expression depend on Delta expression as in sea urchins: in the sea star gcm transcription is unaffected in embryos bearing morpholinosubstituted antisense oligonucleotides (MASOs) targeting Delta, as illustrated in Fig. 1 E and F and supported as well by quantitative PCR (qPCR) measurements of transcript levels (data not shown).”
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“But the Deltaexpressing cells are what become the definitive vegetal plate mesoderm, rather than the cells adjacent to it, as shown in the later stages portrayed in Fig. 1 B and C .”
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“The sea star delta gene is expressed within the mesodermal progenitors of the central vegetal plate and scattered in the cells of the ectoderm at the blastula stage (Fig. 1 A ).”
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“Expression of gatae in the blastopore of late embryos is unaffected.”
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“In direct contrast, when Delta expression is blocked in the sea star, excessive numbers of migratory blastocoelar cells are formed, as can be seen by comparing Fig. 2 A and B .”
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“The loss of expression of the endodermal markers bra , gatae and foxa in Tbr-deficient embryos is confirmed visually by using WMISH (Fig. 4).”
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“The prediction that tbr MASO would elevate ets1 and gatac expression in the endodermal barrel as does delta MASO is confirmed in Fig. 3 E and J .”
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“Sea star gatac expression continues throughout the mesoderm at the top of the archenteron during early gastrulation but has almost disappeared by late gastrula stage (SI Fig. 7 and Fig. 3 A ).”
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“Gatae MASO also causes delamination of excess ets1 / 2 -positive cells later on, which can be seen ectopically collected around the hindgut in Fig. 3 H .”
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In the paper
“Delta was not required for the expression of several early and broadly endomesodermally expressed transcription factors, i.e., tbrain ( tbr ), otx 𝛃 1 / 2 , or otx 𝛂 (SI Fig. 6).”
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“Both whole-mount in situ hybridization (WMISH; Fig. 2 C -F ) and quantitative analyses of transcript levels [supporting information (SI) Fig. 6] revealed that Delta is required for expression of gatae in the gut and for its own expression.”
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“AmGcm is not expressed at all within the vegetal plate (Fig. 1 D and E ), instead displaying a spotty pattern of ectodermal expression.”
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“Foxa , which is restricted to the posterior hindgut and blastopore until late gastrula is also unaffected when measured quantitatively (SI Fig. 6), although possibly the inner-most ring of expression of foxa , fated to the more anterior domain of its hindgut expression, is reduced (Fig. 2 C ).”
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“But foxa expression can be blocked without causing up-regulation of either gatac or ets1 / 2 (Fig. 3 D and I ).”
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In the paper
“In A. miniata , gatac is expressed throughout the central vegetal plate fated to mesoderm (SI Fig. 7), but unlike its orthologue in S. purpuratus its expression is not restricted to the oral quadrant [in the sea urchin embryo the gcmexpressing pigment cell precursors are located in the aboral three-quarters of the mesodermal domain (14)].”
What the sources say
- Not checked yetcites [14] source
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“Normally in sea star embryos gatae is expressed in the archenteron barrel (future hindgut and midgut) and is expressed at very low levels in the mesoderm bulb (Fig. 2 D ), but in the absence of Delta-N signaling its expression is extinguished in the barrel as we have seen, and, for reasons not yet known, is dramatically up-regulated in the anterior bulb (Fig. 2 E and F , regions marked by * ).”
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In the paper
“From > 65% to ≈ 80% of expression of otx 𝛃 1 / 2 , foxa and bra , gatae , tbr itself, and otx 𝛂 is abolished by this treatment, whereas control genes not expressed in endomesoderm at this stage are unaffected.”
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In the paper
“However, in Delta MASO embryos ets1 / 2 expression is also up-regulated, extending throughout the archenteron and at greater than normal intensity (Fig. 3 G ).”
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In the paper
“But in Delta-deficient embryos, gatac expression is up- regulated: it extends throughout the archenteron and persists during gastrulation and is more intense than in normal, similarly staged gastrulae (Fig. 3 A vs. B ).”
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“We note that in echinoderms regulatory genes are generally not 2- or 4-fold paralogous (31), as in mammals, so the process of cis -regulatory changes in input cannot be explained by functional diversification of duplicated genes.”
What the sources say
- Not checked yetcites [31] Sea Urchin Genome Sequencing Consortium (2006) Science 314:941-952. source
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In the paper
“As discussed above, tbr plays totally different roles in the two systems, and we know enough from observations in outgroups that it is clear that the echinoid use of this gene is the cooption and the sea star use the pleisiomorphic state.”
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“This is a surprisingly active evolutionary process, the magnitude of which is partially concealed by its frequently compensatory nature.”
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“The fundamental result of this study, then, is that the genomic regulatory code underlying these similar developmental tasks differs very significantly in the two animals at the cis -regulatory level, but much less so at the circuit design level.”
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In the paper
“In the sea star the boundary depends on Foxa repression of gatae in the mesoderm (6), a function that requires a Foxa-responsive gatae cis -regulatory module.”
What the sources say
- Not checked yetcites [6] source
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In the paper
“Thus, as we show elsewhere (29), the endomesodermal otx 𝛃 1 / 2 cis -regulatory module of the sea urchin indeed lacks a Tbr site and instead another positive regulator interacts with it to drive its early expression; something similar would be predicted for the relevant cis -regulatory module of the delta gene.”
What the sources say
- Not checked yetcites [29] Hinman VF, Nguyen A, Davidson EH (2007) Dev Biol , in press.
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In the paper
“In sea urchins endoderm cells are prevented from expressing mesoderm genes by foxa repression of gcm (22, 23), whereas in sea stars endoderm cells are also prevented from expressing mesoderm genes, but not by foxa : instead it is gatae that executes the exclusion function (possibly indirectly), by blocking expression of gatac and ets1 .”
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In the paper
“in sea stars Delta-N signaling has the effect of preventing mesoderm specification (in the archenteron barrel), whereas in sea urchins it is required to produce mesoderm specification.”
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In the paper
“The conserved five-gene kernel discovered earlier is shown in red in Fig. 5, to which we have now added the equally conserved delta to gatae input demonstrated in this work in the sea star.”
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In the paper
“Not only is Delta-N signaling not used for mesoderm specification in sea stars, but instead it functions oppositely, to limit mesoderm specification.”
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In the paper
“But the foxa gene represses its own transcription in the mesoderm and also represses mesodermal gatae transcription, abolishing expression of both in that territory (6).”
What the sources say
- Not checked yetcites [6] source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“In sea stars Delta-N signaling is used to potentiate gatae expression in the endoderm, where this gene is not subject to foxa repression. It does this in sea urchins, too, in the second phase of Delta-N signaling, and in neither does N input into gatae determine the endoderm/mesoderm boundary.”
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“In the sea urchin gatae runs in both the mesoderm and endoderm almost up to gastrulation. The consequence is that this gene can be used to provide input into mesoderm genes in sea urchin and does so to gatac , a role that would be impossible in the sea star.”
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In the paper
“In other words, the origin of the mesoderm/endoderm boundary in sea stars is ultimately the repression of gatae in the mesoderm by foxa , whereas in sea urchins it is the initial phase of Delta-N signaling.”
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The paper relies on this without support.
Embryonic pigment cells are not formed at all in sea stars as they are in euechinoids.
“Embryonic pigment cells are not formed at all in sea stars as they are in euechinoids.”
The paper relies on this without support.
The sea star embryo lacks micromeres and makes no embryonic skeleton.
“The sea star embryo not only lacks micromeres but also makes no embryonic skeleton.”
The paper relies on this without support.
None of the other five echinoderm classes possesses a skeletogenic micromere lineage.
“Because none of the other five echinoderm classes possesses a skeletogenic micromere lineage, the sea star represents in this respect the pleisiomorphic state, and the sea urchin represents the derived state.”
The paper relies on this without support.
Sea stars produce vegetal plate mesoderm that is topologically central to the surrounding ring of cells which become endoderm.
“Sea stars also produce vegetal plate mesoderm, that just as in sea urchins, is topologically central to the surrounding ring of cells, which become endoderm, but they must use a different mesodermal specification mechanism.”
The paper relies on this without support.
In sea urchins, the cells of the vegetal plate that are exposed to the initial Delta-N signal become mesoderm, and the peripheral cells that are not become endoderm.
“In sea urchins the cells of the vegetal plate that are exposed to the initial Delta-N signal become mesoderm, and the peripheral cells that are not become endoderm.”
The paper relies on this without support.
In S. purpuratus, foxa has no input to gatae, which is expressed in both until just before gut invagination.
“It has no input to gatae , which is expressed in both until just before gut invagination.”
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Sometimes the contrast between the conserved and non-conserved parts of a given GRN is quite dramatic, as in a comparison between sea urchin and sea star endomesodermal GRNs that revealed an extremely conserved, 5-gene subcircuit, surrounded by linkages not one of which had survived the half billion years since divergence without change (Hinman and Davidson, 2007).”
From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Hinman and Davidson, 2007
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Certain remarkably conserved regulatory sub-circuits that are located near the top of developmental GRN hierarchy may serve to lock down developmental process specific to given phyla or classes (GRN kernels)86–91.”
From Emerging properties of animal gene regulatory networks (2010) · cites this paper as [90]
Experimental — accuracy not yet measuredIn the citing paper
“tbr provides an explicit case of cooption, because this gene is expressed in endomesoderm in other echinoderms, including sea stars (20, 21), where it is obligatory for endomesoderm specification (21); in echinoids, tbr is expressed only in the skeletogenic micromere lineage.”
From Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution (2008) · cites this paper as [21]
Citations
Cites
Gene Regulatory Networks and the Evolution of Animal Body Plans
Davidson, E. H., & Erwin, D. H. (2006) · Science · doi:10.1126/science.1113832 · Cited by 1,207
Self-citationThe Genome of the Sea Urchin Strongylocentrotus purpuratus
Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D., et al. (2006) · Science · doi:10.1126/science.1133609 · Cited by 1,132
Self-citationThe Regulatory Genome: Gene Regulatory Networks In Development And Evolution
Davidson, E. H. (2006) · Thammasat University Digital Collections · Cited by 1,048
Self-citationRepetitive and Non-Repetitive DNA Sequences and a Speculation on the Origins of Evolutionary Novelty
Britten, R. J., & Davidson, E. H. (1971) · The Quarterly Review of Biology · doi:10.1086/406830 · Cited by 789
Self-citationGenomic Regulatory Systems: Development and Evolution
Davidson, E. H. (2005) · Thammasat University Digital Collections · Cited by 690
Self-citationEchinoderm phylogeny and evolutionary biology
PAUL, C. R. C., & Smith, A. B. (1988) · Cited by 353
Developmental gene regulatory network architecture across 500 million years of echinoderm evolution
Hinman, V. F., Nguyen, A. T., Cameron, R. A., & Davidson, E. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235868100 · Cited by 272
Self-citationA Regulatory Gene Network That Directs Micromere Specification in the Sea Urchin Embryo
Oliveri, P., Carrick, D. M., & Davidson, E. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0627 · Cited by 251
Self-citationLaubichler, M. D. (2006) · Max Planck Digital Library · Cited by 229
LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo
Sherwood, D. R., & McClay, D. R. (1999) · Development · doi:10.1242/dev.126.8.1703 · Cited by 209
Research works printed but not linked: 2
- YK Maruyama Zool Sci 17, 383–387 (2000).
- VF Hinman, A Nguyen, EH Davidson Dev Biol, in press. (2007).
Cited by
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Metadata
- Authors
- Hinman, V. F., & Davidson, E. H.
- Affiliations
- Carnegie Mellon University (US)
- California Institute of Technology (US)
- Corresponding author
- Davidson, Eric H.
- ORCID
- Hinman, Veronica F.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-12-04
- Volume
- 104
- Issue
- 49
- Pages
- 19404-19409
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2148302
- OpenAlex
- W2167934696
- Cited by
- 154
- References
- 34
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 7 · 2021: 6 · 2020: 6 · 2019: 5 · 2018: 4 · 2017: 14 · 2016: 6 · 2015: 9 · 2014: 11 · 2013: 7 · 2012: 17
- FWCI
- 4.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Science Foundation (0641398)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Keywords
- gene regulatory networks, evolutionary plasticity, sea stars, sea urchins, endoderm specification, mesoderm specification, Delta-Notch signaling, embryonic development, evolutionary developmental biology
- MeSH terms
- Animals, Endoderm, Mesoderm, Sea Urchins, Starfish, Signal Transduction, Evolution, Molecular, T-Box Domain Proteins, Receptors, Notch, Gene Regulatory Networks
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