Abstract
Subdivision of the neuroectoderm into three rows of cells along the dorsal-ventral axis by neural identity genes is a highly conserved developmental process. While neural identity genes are expressed in remarkably similar patterns in vertebrates and invertebrates, previous work suggests that these patterns may be regulated by distinct upstream genetic pathways. Here we ask whether a potential conserved source of positional information provided by the BMP signaling contributes to patterning the neuroectoderm. We have addressed this question in two ways: First, we asked whether BMPs can act as bona fide morphogens to pattern the Drosophila neuroectoderm in a dose-dependent fashion, and second, we examined whether BMPs might act in a similar fashion in patterning the vertebrate neuroectoderm. In this study, we show that graded BMP signaling participates in organizing the neural axis in Drosophila by repressing expression of neural identity genes in a threshold-dependent fashion. We also provide evidence for a similar organizing activity of BMP signaling in chick neural plate explants, which may operate by the same double negative mechanism that acts earlier during neural induction. We propose that BMPs played an ancestral role in patterning the metazoan neuroectoderm by threshold-dependent repression of neural identity genes.
Highlights
Morphogen gradients play a central role in creating pattern during embryonic development [1,2]
The bone morphogenetic protein (BMP) antagonist Short gastrulation (Sog) is expressed throughout the neuroectoderm [38] prior to the activation of neural identity gene expression and fades dorsally (Figure 1D and 1E) as the Dorsal gradient collapses [38,39]
The BMP2/4 homolog Dpp is expressed in adjacent dorsal cells (Figure 1B), where it represses the expression of neural genes and acts in a graded fashion to pattern the non-neural ectoderm
Summary
Morphogen gradients play a central role in creating pattern during embryonic development [1,2]. Bone morphogenetic proteins (BMPs) are one of the best studied examples of morphogens and function in a conserved fashion to subdivide the early embryonic ectoderm into neural versus non-neural regions [3] Following this role in establishing the primary ectodermal domains, BMPs and their antagonists, such as Short gastrulation (Sog)/Chordin (Chd), interact in a graded fashion to establish a series of nested gene expression domains in the non-neural ectoderm. The neuroectoderm in Drosophila and vertebrate embryos is subdivided into three conserved dorsal-ventral (DV) domains expressing the homeobox genes ventral nervous system defective (vnd)/Nkx2.2, intermediate nervous system defective (ind)/ Gsh, and muscle specific homeobox (msh)/Drop/Msx1/2 (Figure 1). In Drosophila, both loss-of-function and mis-expression experiments have revealed that neural-identity genes crossregulate each other in a ventral-dominant fashion wherein ventrally expressed genes repress expression of more dorsal ones [9,12,16,18], a mechanism likely to have been conserved in vertebrates [19,20,21]
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