The molecular nature of zebrafish <i>swirl</i>: BMP2 function is essential during early dorsoventral patterning

TLDR

Early dorsoventral patterning in vertebrate embryos is governed by opposing BMP signaling and its antagonists, and zebrafish mutants such as swirl exhibit ventralized or dorsalized phenotypes that highlight defects in this regulatory network. We show that mutations in zebrafish bmp2 cause the swirl phenotype, which can be fully rescued by wild‑type bmp2 mRNA, and that bmp2 is required only for early dorsoventral patterning, with no maternal or post‑gastrulation role.

Abstract

Early dorsoventral pattern formation in vertebrate embryos is regulated by opposing activities of ventralizing bone morphogenetic proteins (BMPs) and dorsal-specific BMP antagonists such as Chordin, Noggin and Follistatin. Specific defects in early dorsoventral patterning have been recently found in a number of zebrafish mutants, which exhibit either a ventralized or dorsalized phenotype. One of these, the ventralized mutant chordino (originally called dino) is caused by a mutation in the zebrafish chordin homologue and interacts genetically with the dorsalized mutant swirl. In swirl mutant embryos, dorsal structures such as notochord and somites are expanded while ventral structures such as blood and nephros are missing. Here we demonstrate that the swirl phenotype is caused by mutations in the zebrafish bmp2 gene (zbmp2). While injection of mRNAs encoded by the mutant alleles has no ventralizing effect, injection of wild-type zbmp2 mRNA leads to a complete rescue of the swirl mutant phenotype. Fertile adult mutant fish were obtained, showing that development after gastrulation is not dependent on zbmp2 function. In addition zBMP2 has no maternal role in mesoderm induction. Our analysis shows that swirl/BMP2, unlike mouse BMP2 but like mouse BMP4, is required for early dorsoventral patterning of the zebrafish embryo.