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Caught in the evolutionary act: Precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins

Hinman, Veronica F. and Nguyen, Albert and Davidson, Eric H. (2007) Caught in the evolutionary act: Precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins. Developmental Biology, 312 (2). pp. 584-595. ISSN 0012-1606. doi:10.1016/j.ydbio.2007.09.006. https://resolver.caltech.edu/CaltechAUTHORS:20160122-095050573

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Abstract

The regulatory control of otxβ1/2 in the sea urchin Strongylocentrotus purpuratus and the sea star Asterina miniata provides an exceptional opportunity to determine the genomic basis of evolutionary change in gene regulatory network (GRN) architectures. Network perturbation analyses in both taxa show that Otx regulates the transcription factors gatae and krox/blimp1 and both of these transcription factors also feed back and regulate otx. The otx gene also autoregulates. This three way interaction is an example of a GRN kernel. It has been conserved for 500 million years since these two taxa last shared a common ancestor. Amid this high level of conservation we show here one significant regulatory change. Tbrain is required for correct otxβ1/2 expression in the sea star but not in the sea urchin. In sea urchin, tbrain is not co-expressed with otxβ1/2 and instead has an essential role in specification of the embryonic skeleton. Tbrain in these echinoderms is thus a perfect example of an orthologous gene co-opted for entirely different developmental processes. We isolate and test the sea star otxβ1/2 cis-regulatory module and demonstrate functional binding sites for each of the predicted inputs, including Tbrain. We compare it to the logic processing operating in the sea urchin otxβ1/2 cis-regulatory module and present an evolutionary scenario of the change in Tbrain dependence. Finally, inter-specific gene transfer experiments confirm this scenario and demonstrate evolution occurring at the level of sequence changes to the cis-regulatory module.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.ydbio.2007.09.006DOIArticle
http://www.sciencedirect.com/science/article/pii/S0012160607013425PublisherArticle
Additional Information:© 2007 Elsevier Inc. Received for publication 28 March 2007; revised 2 September 2007; accepted 6 September 2007. Available online 16 September 2007. We are grateful to Julie Hahn for the construction of the otx-BAC-GFP recombinant. Also to Miki Jun for extensive help with sequencing and plasmid DNA preparation. Cathy Yuh provided various sea urchin otx clones and primers and much information and advice. Many thanks are owed to Joel Smith for providing thoughtful comments on the manuscript. This work was supported by a NASA/Ames grant 1587 to EHD.
Funders:
Funding AgencyGrant Number
NASA1587
Subject Keywords:Cis-regulatory evolution; Sea urchin; Asterina miniata; Gene regulatory network
Issue or Number:2
DOI:10.1016/j.ydbio.2007.09.006
Record Number:CaltechAUTHORS:20160122-095050573
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160122-095050573
Official Citation:Veronica F. Hinman, Albert Nguyen, Eric H. Davidson, Caught in the evolutionary act: Precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins, Developmental Biology, Volume 312, Issue 2, 15 December 2007, Pages 584-595, ISSN 0012-1606, http://dx.doi.org/10.1016/j.ydbio.2007.09.006. (http://www.sciencedirect.com/science/article/pii/S0012160607013425)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63877
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:22 Jan 2016 20:35
Last Modified:10 Nov 2021 23:22

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