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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack, Eric (2016) Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins. Proceedings of the National Academy of Sciences of the United States of America, 113 (46). E7202-E7211. ISSN 0027-8424. PMCID PMC5135324. http://resolver.caltech.edu/CaltechAUTHORS:20160419-092626846

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Abstract

Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral–aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirect-developing euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell type–biased alterations.


Item Type:Article
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URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1612820113DOIArticle
http://www.pnas.org/content/113/46/E7202/suppl/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5135324PubMed CentralArticle
http://dx.doi.org/10.1101/044149DOIDiscussion Paper
ORCID:
AuthorORCID
Erkenbrack, Eric0000-0001-9375-3279
Alternate Title:Evolution of gene regulatory network topology and dorsal-ventral axis specification in early development of sea urchins (Echinoidea)
Additional Information:© 2016 National Academy of Sciences. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved October 5, 2016 (received for review August 3, 2016). Published online before print November 3, 2016. I dedicate this paper to my mentor and friend Eric Harris Davidson, who indelibly impacted my life in so many ways and who conceptually influenced the major theme of this paper, as well as provided input on experimental design and assessed portions of the data presented here. I thank Dr. Julius C. Barsi for the Sp onecut engineered BACs; Jennifer Wellman for her insight into statistical analyses; Stefan Materna for the raw data on S. purpuratus mRNA transcript abundance and manuscript critiques; Dr. Matthias Futschik and Cong Liang for mfuzz advice; Drs. Oliver Griffith, David McClay, Tom Stewart, and Jeffrey R. Thompson for their critical commentary on figures and the manuscript; and Prof. Günter P. Wagner for his patience and support. This work was funded by National Science Foundation CREATIV Grant 1240626. Author contributions: E.M.E. designed research, performed research, analyzed data, and wrote the paper. The author declares no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1612820113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NSFIOS-1240626
Subject Keywords:gene regulatory network; echinoderms; sea urchin embryogenesis; embryonic axis specification; echinoids
PubMed Central ID:PMC5135324
Record Number:CaltechAUTHORS:20160419-092626846
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160419-092626846
Official Citation:Eric M. Erkenbrack Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins PNAS 2016 113 (46) E7202-E7211; published ahead of print November 3, 2016, doi:10.1073/pnas.1612820113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:66273
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:19 Apr 2016 21:17
Last Modified:29 Oct 2018 16:28

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