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

Erkenbrack, Eric M. and Ako-Asare, Kayla and Miller, Emily and Tekelenburg, Saira and Thompson, Jeffrey R. and Romano, Laura (2016) Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms. Development Genes and Evolution, 226 (1). pp. 37-45. ISSN 0949-944X. http://resolver.caltech.edu/CaltechAUTHORS:20160121-155216763

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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.


Item Type:Article
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URLURL TypeDescription
http://dx.doi.org/10.1007/s00427-015-0527-yDOIArticle
http://link.springer.com/article/10.1007%2Fs00427-015-0527-yPublisherArticle
http://rdcu.be/ttaxPublisherFree ReadCube access
ORCID:
AuthorORCID
Erkenbrack, Eric M.0000-0001-9375-3279
Additional Information:© 2016 Springer. Received: 15 October 2015; Accepted: 29 December 2015. First online: 19 January 2016. Communicated by Hiroki Nishida. 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.
Funders:
Funding AgencyGrant Number
NIH1R15HD059927-01
NSF1240626
Subject Keywords:Evolution; Embryonic development; Gene regulatory networks; Echinoderms; Cidaroid; Co-option
Record Number:CaltechAUTHORS:20160121-155216763
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160121-155216763
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63857
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:22 Jan 2016 00:07
Last Modified:14 Jun 2017 21:08

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