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

Hinman, Veronica F. and Nguyen, Albert T. and Cameron, R. Andrew and Davidson, Eric H. (2003) Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proceedings of the National Academy of Sciences of the United States of America, 100 (23). pp. 13356-13361. ISSN 0027-8424. PMCID PMC263818. doi:10.1073/pnas.2235868100.

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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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Cameron, R. Andrew0000-0003-3947-6041
Additional Information:Copyright © 2003 by the National Academy of Sciences Contributed by Eric H. Davidson, September 12, 2003. Published online before print October 31, 2003, 10.1073/pnas.2235868100 We thank members of the Davidson laboratory, whose extraordinary efforts in constructing the GRN for endomesoderm specification in sea urchins have provided the foundations for this comparative study; Drs. Andy Ransick and Takuya Minokawa, who provided their unpublished data on tbr expression in SpOtx-Eng-injected S. purpuratus embryos; Pei Yun Lee for allowing us to use unpublished data regarding the effect of Gatae on tbr expression in S. purpuratus; Pat Leahy and the staff at the Kerckhoff Marine Laboratory (Corona del Mar, CA) for maintaining starfish; the staff at the California Institute of Technology Beckman Institute Arraying Facility for preparing cDNA library filters; Miki Yun, who helped with sequencing and plasmid DNA preparation; and Dr. Paola Oliveri of the Davidson laboratory and Professor Ellen Rothenberg for very helpful comments on the manuscript. This work was supported by National Aeronautics and Space Administration/Ames Grant NAG2-1587 and National Center for Research Resources Grant RR-15044 and by the California Institute of Technology Beckman Institute Genomics Technology Facility (to E.H.D.).
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Caltech Beckman InstituteUNSPECIFIED
Subject Keywords:gene regulatory networks;quantitative PCR; morpholino-substituted antisense oligonucleotide; Engrailed
Issue or Number:23
PubMed Central ID:PMC263818
Record Number:CaltechAUTHORS:HINpnas03
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:1189
Deposited By: Archive Administrator
Deposited On:04 Jan 2006
Last Modified:01 Jun 2023 23:12

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