Developmental gene regulatory network architecture across 500 million years of echinoderm evolution.
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.
Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.
Veronica F
VF
Hinman
Albert T
AT
Nguyen
R Andrew
RA
Cameron
Eric H
EH
Davidson
D000818:Animals; D005075:Biological Evolution; D003001:Cloning, Molecular; D004305:Dose-Response Relationship, Drug; D004447:Echinodermata / Q000235:genetics* / Q000378:metabolism; D025461:Feedback, Physiological; D018507:Gene Expression Regulation, Developmental; D008648:Mesoderm / Q000378:metabolism; D010802:Phylogeny; D012333:RNA, Messenger / Q000378:metabolism; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012617:Sea Urchins; D013215:Starfish; D013997:Time Factors; D014157:Transcription Factors
D012333:RNA, Messenger; D014157:Transcription Factors