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Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks

Amore, Gabriele and Yavrouian, Robert G. and Peterson, Kevin J. and Ransick, Andrew and McClay, David R. and Davidson, Eric H. (2003) Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks. Developmental Biology, 261 (1). pp. 55-81. ISSN 0012-1606. doi:10.1016/S0012-1606(03)00278-1.

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The Spdeadringer (Spdri) gene encodes an ARID-class transcription factor not previously known in sea urchin embryos. We show that Spdri is a key player in two separate developmental gene regulatory networks (GRNs). Spdri is expressed in a biphasic manner, first, after 12 h and until ingression in the skeletogenic descendants of the large micromeres; second, after about 20 h in the oral ectoderm, where its transcripts remain present at 30–50 mRNA molecules/cell far into development. In both territories, the periods of Spdri expression follow prior territorial specification events. The functional significance of each phase of expression was assessed by determining the effect of an αSpdri morpholino antisense oligonucleotide (MASO) on expression of 17 different mesodermal genes, 8 different oral ectoderm genes, and 18 other genes expressed specifically during endomesoderm specification. These effects were measured by quantitative PCR, supplemented by whole-mount in situ hybridization and morphological observations. Spdri is shown to act in the micromere descendants in the pathways that result in the expression of batteries of terminal skeletogenic genes. But, in the oral ectoderm, the same gene participates in the central GRN controlling oral ectoderm identity. Spdri is linked in the oral ectoderm GRN with several other genes encoding transcriptional regulators that are expressed specifically in various regions of the oral ectoderm. If its expression is blocked by treatment with αSpdri MASO, oral-specific features disappear and expression of the aboral ectoderm marker spec1 encompasses the whole of the ectoderm. In addition to disappearance of the oral ectoderm, morphological consequences of αSpdri MASO treatment include failure of spiculogenesis and of correct primary mesenchyme cell (pmc) patterning in the postgastrular embryo, and also failure of gastrulation. To further analyze these phenotypes, chimeric embryos were constructed consisting of two labeled micromeres combined with micromereless 4th cleavage host embryos; either the micromeres or the hosts contained αSpdri MASO. These experiments showed that, while Spdri expression is required autonomously for expression of skeletogenic genes prior to ingression, complete skeletogenesis also requires the expression of oral ectoderm patterning information. Presentation of this information on the oral side of the blastocoel in turn depends on Spdri expression in the oral ectoderm. Failure of gastrulation is not due to indirect interference with endomesodermal specification per se, since all endomesodermal genes tested function normally in αSpdri MASO embryos. Part of its cause is interference by αSpdri MASO with a late signaling function on the part of the micromere descendants that is needed to complete clearance of the Soxb1 repressor of gastrulation from the prospective endoderm, but in addition there is a nonautonomous oral ectoderm effect.

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Additional Information:© 2003 Elsevier Inc. Received for publication 14 October 2002, revised 30 April 2003, accepted 1 May 2003. Available online 1 July 2003. We thank Dr. R.C. Angerer of Rochester University for the kind gift of aliquots of the Gsc morpholino oligonucleotide and Dr. G. Spinelli of the University of Palermo for providing the sequence of S. purpuratus otp. We acknowledge Dr. William Klein of the MD Anderson Hospital for the kind gift of the ENG-N plasmid used to obtain the Spdri-En construct. We also thank Dr. Takuya Minokawa for providing the krl, gsc, and nk1 WMISH probes, and Dr. Paola Oliveri of Caltech for critical reviews of the manuscript. This work was supported by NIH Grants HD-37105 and RR-06591.
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Subject Keywords:Gene regulatory network; Oral ectoderm; deadringer; Sea urchin embryo
Issue or Number:1
Record Number:CaltechAUTHORS:20160121-075840357
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Official Citation:Gabriele Amore, Robert G Yavrouian, Kevin J Peterson, Andrew Ransick, David R McClay, Eric H Davidson, Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks, Developmental Biology, Volume 261, Issue 1, 1 September 2003, Pages 55-81, ISSN 0012-1606, (
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63826
Deposited By: Ruth Sustaita
Deposited On:21 Jan 2016 18:58
Last Modified:10 Nov 2021 23:21

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