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Open Access Highly Accessed Research article

Correct anteroposterior patterning of the zebrafish neurectoderm in the absence of the early dorsal organizer

Máté Varga12*, Shingo Maegawa13 and Eric S Weinberg1*

Author Affiliations

1 Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA

2 Current Address: Department of Genetics, Eötvös Loránd University, Pázmány Péter sétány 1/C, Budapest H-1117, Hungary

3 Current Address: Dept. of Intelligence Science and Technology, Graduate School of Informatics, Kyoto University, Yoshidia-Honmachi, Sakyo, Kyoto 606-8501, Japan

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BMC Developmental Biology 2011, 11:26  doi:10.1186/1471-213X-11-26

Published: 16 May 2011

Abstract

Background

The embryonic organizer (i.e., Spemann organizer) has a pivotal role in the establishment of the dorsoventral (DV) axis through the coordination of BMP signaling. However, as impaired organizer function also results in anterior and posterior truncations, it is of interest to determine if proper anteroposterior (AP) pattern can be obtained even in the absence of early organizer signaling.

Results

Using the ventralized, maternal effect ichabod (ich) mutant, and by inhibiting BMP signaling in ich embryos, we provide conclusive evidence that AP patterning is independent of the organizer in zebrafish, and is governed by TGFβ, FGF, and Wnt signals emanating from the germ-ring. The expression patterns of neurectodermal markers in embryos with impaired BMP signaling show that the directionality of such signals is oriented along the animal-vegetal axis, which is essentially concordant with the AP axis. In addition, we find that in embryos inhibited in both Wnt and BMP signaling, the AP pattern of such markers is unchanged from that of the normal untreated embryo. These embryos develop radially organized trunk and head tissues, with an outer neurectodermal layer containing diffusely positioned neuronal precursors. Such organization is reflective of the presumed eumetazoan ancestor and might provide clues for the evolution of centralization in the nervous system.

Conclusions

Using a zebrafish mutant deficient in the induction of the embryonic organizer, we demonstrate that the AP patterning of the neuroectoderm during gastrulation is independent of DV patterning. Our results provide further support for Nieuwkoop's "two step model" of embryonic induction. We also show that the zebrafish embryo can form a radial diffuse neural sheath in the absence of both BMP signaling and the early organizer.