Conserved regulatory state expression controlled by divergent developmental gene regulatory networks in echinoids
Abstract
Evolution of the animal body plan is driven by changes in developmental gene regulatory networks (GRNs), but how networks change to control novel developmental phenotypes remains, in most cases, unresolved. Here, we address GRN evolution by comparing the endomesoderm GRN in two echinoid sea urchins, Strongylocentrotus purpuratus and Eucidaris tribuloides, with at least 268 million years of independent evolution. We first analyzed the expression of twelve transcription factors and signaling molecules of the S. purpuratus GRN in E. tribuloides embryos, showing that orthologous regulatory genes are expressed in corresponding endomesodermal cell fates in the two species. However, perturbation of regulatory genes revealed that important regulatory circuits of the S. purpuratus GRN are significantly different in E. tribuloides. For example, mesodermal Delta/Notch signaling controls exclusion of alternative cell fates in E. tribuloides but controls mesoderm induction and activation of a positive feedback circuit in S. purpuratus. These results indicate that the architecture of the sea urchin endomesoderm GRN evolved by extensive gain and loss of regulatory interactions between a conserved set of regulatory factors that control endomesodermal cell fate specification.
Additional Information
© 2018 Published by The Company of Biologists Ltd. Received May 1, 2018; Accepted November 15, 2018; Published 23 November 2018. We thank Deanna Thomas for her contributions to the figures, Jonathan Valencia for contributing an image of S. purpuratus, and Rebekah Kitto for helping with WMISH and imaging embryos. We are grateful to Andy Cameron, Parul Kudtakar and the bioinformatics team at the Center for Computational Regulatory Genomics at the Beckman Institute for their computational support. Competing interests: The authors declare no competing or financial interests. Author contributions: Conceptualization: E.M.E., E.H.D., I.S.P.; Formal analysis: E.M.E., I.S.P.; Investigation: E.M.E.; Writing - original draft: E.M.E., I.S.P.; Writing - review & editing: I.S.P.; Supervision: I.S.P.; Funding acquisition: E.H.D., I.S.P. Funding: This work was supported by the National Institutes of Health (Eunice Kennedy Shriver National Institute of Child Health and Human Development) grant HD037105 and the National Science Foundation (Division of Integrative Organismal Systems) CREATIV grant 1240626. Deposited in PMC for release after 12 months. Data availability: All sequence data have been deposited in GenBank under accession numbers MF990311, MF990312, MF990313, MF990314, MF990315, MF990316, MF990317, MF990318, MF990319, MF990320 and MF990321 (as listed in Table S2). Supplementary information: Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.167288.supplemental.Attached Files
Published - dev167288.full.pdf
Supplemental Material - DEV167288supp.pdf
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Additional details
- PMCID
- PMC6307887
- Eprint ID
- 91415
- DOI
- 10.1242/dev.167288
- Resolver ID
- CaltechAUTHORS:20181204-072548701
- NIH
- HD037105
- NSF
- IOS-1240626
- Created
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2018-12-04Created from EPrint's datestamp field
- Updated
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2021-12-10Created from EPrint's last_modified field