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Cited by 272Developmental Biology and Gene RegulationMarine Invertebrate Physiology and EcologyGene Regulatory Network Analysis

Developmental gene regulatory network architecture across 500 million years of echinoderm evolution

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Hinman, Veronica F., Nguyen, Albert T., Cameron, R. Andrew, Davidson, Eric H.·2003·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.2235868100PMC PMC263818
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Abstract

Evolutionary change in morphological features must depend on architectural reorganization of developmental gene regulatory networks (GRNs), just as true conservation of morphological features must imply retention of ancestral developmental GRN features. Key elements of the provisional GRN for embryonic endomesoderm development in the sea urchin are here compared with those operating in embryos of a distantly related echinoderm, a starfish. These animals diverged from their common ancestor 520-480 million years ago. Their endomesodermal fate maps are similar, except that sea urchins generate a skeletogenic cell lineage that produces a prominent skeleton lacking entirely in starfish larvae. A relevant set of regulatory genes was isolated from the starfish Asterina miniata, their expression patterns determined, and effects on the other genes of perturbing the expression of each were demonstrated. A three-gene feedback loop that is a fundamental feature of the sea urchin GRN for endoderm specification is found in almost identical form in the starfish: a detailed element of GRN architecture has been retained since the Cambrian Period in both echinoderm lineages. The significance of this retention is highlighted by the observation of numerous specific differences in the GRN connections as well. A regulatory gene used to drive skeletogenesis in the sea urchin is used entirely differently in the starfish, where it responds to endomesodermal inputs that do not affect it in the sea urchin embryo. Evolutionary changes in the GRNs since divergence are limited sharply to certain cis-regulatory elements, whereas others have persisted unaltered.

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  • As in sea urchins, gatae expression is essential for the correct specification of endoderm in A. miniata embryos.

    “As in sea urchins, gatae expression is essential for the correct specification of endoderm in A. miniata embryos (6).”

    From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [6]

  • In the sea star, foxa represses its own transcription in the mesoderm and represses mesodermal gatae transcription, abolishing expression of both in that territory.

    “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).”

    From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [6]

  • The positive input of tbr to bra and foxa can be accounted for as an indirect consequence of Tbr inputs into delta plus its direct inputs into otxβ1/2.

    “Because bra and foxa are downstream of both gatae and otx 𝛃 1 / 2 (6), the positive input of tbr to these endodermal genes can easily be accounted for as an indirect consequence of Tbr inputs into delta (direct or indirect) plus its direct inputs into otx 𝛃 1 / 2 .”

    From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [6]

  • In the sea star the mesoderm/endoderm boundary depends on Foxa repression of gatae in the mesoderm, requiring a Foxa-responsive gatae cis-regulatory module.

    “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.”

    From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [6]

  • The Delta-N to gatae linkage is likely a pleisomorphic feature of endoderm specification in echinoderms.

    “It is likely a pleisomorphic feature of endoderm specification in echinoderms, like the endomesodermal specification kernel (6) into which it feeds, and unlike the Delta-N function in initial mesoderm specification seen in sea urchins.”

    From Evolutionary plasticity of developmental gene regulatory network architecture (2007) · cites this paper as [6]

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Authors
Hinman, V. F., Nguyen, A. T., Cameron, R. A., & Davidson, E. H.
Affiliations
California Institute of Technology (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2003-10-31
Volume
100
Issue
23
Pages
13356-13361
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.2235868100
PMC
PMC263818
OpenAlex
W2165937624
Cited by
272
References
31
Citations by year
2026: 7 · 2025: 9 · 2024: 5 · 2023: 6 · 2022: 13 · 2021: 8 · 2020: 5 · 2019: 12 · 2018: 6 · 2017: 13 · 2016: 16 · 2015: 13 · 2014: 16 · 2013: 10 · 2012: 19
FWCI
5.29
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • KiltHub Repository
Funders
  • National Institute on Aging (K07AG021587)
  • National Center for Research Resources (P40RR015044, RR15044)
Topics
  • 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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
gene regulatory networks, echinoderm evolution, sea urchins, sea stars, endoderm specification, skeletogenesis, feedback loops, cis-regulatory elements, developmental gene expression, morphological evolution, embryonic development
MeSH terms
Animals, Cloning, Molecular, Dose-Response Relationship, Drug, Echinodermata, Biological Evolution, Mesoderm, Phylogeny, RNA, Messenger, Sea Urchins, Starfish, Time Factors, Transcription Factors, Gene Expression Regulation, Developmental, Reverse Transcriptase Polymerase Chain Reaction, Feedback, Physiological

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