Sea urchin goosecoid function links fate specification along the animal-vegetal and oral-aboral embryonic axes

Author:

Angerer Lynne M.1,Oleksyn David W.1,Levine Amy M.1,Li Xiaotao2,Klein William H.2,Angerer Robert C.1

Affiliation:

1. Department of Biology, University of Rochester, Rochester, NY 14627, USA

2. Department of Biochemistry and Molecular Biology, The University of Texas M.D. Anderson Cancer Center, and Graduate Program in Genes and Development, Houston, TX 77030, USA

Abstract

We have identified a single homolog of goosecoid, SpGsc, that regulates cell fates along both the animal-vegetal and oral-aboral axes of sea urchin embryos. SpGsc mRNA is expressed briefly in presumptive mesenchyme cells of the ∼200-cell blastula and, beginning at about the same time, accumulates in the presumptive oral ectoderm through pluteus stage. Loss-of-function assays with morpholine-substituted antisense oligonucleotides show that SpGsc is required for endoderm and pigment cell differentiation and for gastrulation. These experiments and gain-of-function tests by mRNA injection show that SpGsc is a repressor that antagonizes aboral ectoderm fate specification and promotes oral ectoderm differentiation. We show that SpGsc competes for binding to specific cis elements with SpOtx, a ubiquitous transcription activator that promotes aboral ectoderm differentiation. Moreover, SpGsc represses transcription in vivo from an artificial promoter driven by SpOtx. As SpOtx appears long before SpGsc transcription is activated, we propose that SpGsc diverts ectoderm towards oral fate by repressing SpOtx target genes. Based on the SpGsc-SpOtx example and other available data, we propose that ectoderm is first specified as aboral by broadly expressed activators, including SpOtx, and that the oral region is subsequently respecified by the action of negative regulators, including SpGsc. Accumulation of SpGsc in oral ectoderm depends on cell-cell interactions initiated by nuclear β-catenin function, which is known to be required for specification of vegetal tissues, because transcripts are undetectable in dissociated or in cadherin mRNA-injected embryos. This is the first identified molecular mechanism underlying the known dependence of oral-aboral ectoderm polarity on intercellular signaling.

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

Reference41 articles.

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2. Angerer, L. M. and Angerer, R. C. (2000). Animal-vegetal axis patterning mechanisms in the early sea urchin embryo. Dev. Biol.218, 1-12.

3. Angerer, L. M., Cox, K. H. and Angerer, R. C. (1987). Demonstration of tissue-specific gene expression by in situ hybridization. Methods Enzymol.152, 649-661.

4. Angerer, L. M., Oleksyn, D. W., Logan, C. Y., McClay, D. R., Dale, L. and Angerer, R. C. (2000). A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development127, 1105-1114.

5. Cameron, R. A., Fraser, S. E., Britten, R. J. and Davidson, E. H. (1989). The oral-aboral axis of a sea urchin embryo is specified by first cleavage. Development106, 641-647.

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