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Development Genes and Evolution

, Volume 226, Issue 1, pp 37–45 | Cite as

Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms

  • Eric M. Erkenbrack
  • Kayla Ako-Asare
  • Emily Miller
  • Saira Tekelenburg
  • Jeffrey R. Thompson
  • Laura Romano
Sequence Corner

Abstract

Diverse sampling of organisms across the five major classes in the phylum Echinodermata is beginning to reveal much about the structure and function of gene regulatory networks (GRNs) in development and evolution. Sea urchins are the most studied clade within this phylum, and recent work suggests there has been dramatic rewiring at the top of the skeletogenic GRN along the lineage leading to extant members of the euechinoid sea urchins. Such rewiring likely accounts for some of the observed developmental differences between the two major subclasses of sea urchins—cidaroids and euechinoids. To address effects of topmost rewiring on downstream GRN events, we cloned four downstream regulatory genes within the skeletogenic GRN and surveyed their spatiotemporal expression patterns in the cidaroid Eucidaris tribuloides. We performed phylogenetic analyses with homologs from other non-vertebrate deuterostomes and characterized their spatiotemporal expression by quantitative polymerase chain reaction (qPCR) and whole-mount in situ hybridization (WMISH). Our data suggest the erg–hex–tgif subcircuit, a putative GRN kernel, exhibits a mesoderm-specific expression pattern early in Eucidaris development that is directly downstream of the initial mesodermal GRN circuitry. Comparative analysis of the expression of this subcircuit in four echinoderm taxa allowed robust ancestral state reconstruction, supporting hypotheses that its ancestral function was to stabilize the mesodermal regulatory state and that it has been co-opted and deployed as a unit in mesodermal subdomains in distantly diverged echinoderms. Importantly, our study supports the notion that GRN kernels exhibit structural and functional modularity, locking down and stabilizing clade-specific, embryonic regulatory states.

Keywords

Evolution Embryonic development Gene regulatory networks Echinoderms Cidaroid Co-option 

Notes

Acknowledgments

This work was part of a funding initiative to enhance developmental biology research at undergraduate institutions awarded to LR (National Institutes of Health #1R15HD059927-01). We thank Andy Cameron and his intrepid crew at the Center for Computational Regulatory Genomics at Caltech’s Beckman Institute for their assistance with sequences. EME conducted the spatiotemporal aspect of this research in the Davidson Laboratory and was funded by National Science Foundation CREATIV grant #1240626. The authors wish to dedicate this paper to the memory of Eric Harris Davidson.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Division of Biology and Biological EngineeringCalifornia Institute of TechnologyPasadenaUSA
  2. 2.Department of BiologyDenison UniversityGranvilleUSA
  3. 3.Department of Earth SciencesUniversity of Southern CaliforniaLos AngelesUSA

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