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  • Review Article
  • Published:

EvoD/Vo: the origins of BMP signalling in the neuroectoderm

Nature Reviews Genetics volume 9, pages 663–677 (2008)Cite this article

Key Points

  • Signalling by bone morphogenetic proteins (BMPs) acts in a conserved all-or-none fashion to repress the expression of all neural genes in the epidermal ectoderm of bilaterian embryos.

  • The dorsal–ventral (D/V) axis of vertebrate embryos is likely to be inverted with respect to that of invertebrates.

  • BMP signalling represses expression of neural genes in dorsal regions of the central nervous system (CNS) in a threshold-dependent manner in the neural ectoderm of Drosophila melanogaster embryos.

  • BMPs also act in a dose-dependent manner to pattern the CNS of vertebrates and annelid worms.

  • Neural patterning mediated by threshold-dependent BMP repression might be ancestral to all metazoans.

  • D. melanogaster and vertebrates have different ventral patterning systems: flies use a gradient of the Dorsal transcription factor, whereas a gradient of secreted Sonic hedgehog is used in vertebrates.

  • Patterning systems that are present in ventral regions of the CNS act in concert with dorsally produced BMPs to refine and sharpen D/V patterning, and might have evolved independently in vertebrate and invertebrate lineages.

  • Genes, such as Hox genes, that control the initial steps in establishing anterior–posterior (A/P) cell fates might define abstract positional codes that allow for rapid morphological diversification; by contrast, comparable genes acting along the D/V axis might define conserved cell types.

  • To account for the conservation of both A/P and D/V regulators we propose a hypothesis, referred to as regulatory treadmilling, in which gene targets of A/P regulators turn over (or treadmill) more rapidly than those of D/V regulators.

Abstract

The genetic systems controlling body axis formation trace back as far as the ancestor of diploblasts (corals, hydra, and jellyfish) and triploblasts (bilaterians). Comparative molecular studies, often referred to as evo–devo, provide powerful tools for elucidating the origins of mechanisms for establishing the dorsal–ventral and anterior–posterior axes in bilaterians and reveal differences in the evolutionary pressures acting upon tissue patterning. In this Review, we focus on the origins of nervous system patterning and discuss recent comparative genetic studies; these indicate the existence of an ancient molecular mechanism underlying nervous system organization that was probably already present in the bilaterian ancestor.

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Figure 1: Neurulation in flies and vertebrates.
Figure 2: Neural induction in flies and vertebrates.
Figure 3: Patterning the neuroectoderm in flies.
Figure 4: BMP patterning in diverse organisms.
Figure 5: Regulatory treadmilling.

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Acknowledgements

Thanks to E. Ball and D. Hayward of the Australian National University, Canberra, for supplying the image in figure 4b. We would like to thank W. McGinnis, S. Wasserman, R. Bodmer and R. Sousa-Neves, and members of the Bier laboratory for comments on the manuscript.

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  1. Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, 92093-0349, California, USA

    Claudia Mieko Mizutani & Ethan Bier

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Glossary

Hemichordates

From the Greek hemi (half) and from the Latin chorda (cord). Marine worm-like animals that can be slow burrowers (acorn worms, for example) or sessile (pterobranchs, for example). The Hemichordata phylum is closely related to Echinodermata and Chordata phyla; together they constitute the Deuterostomata superphylum.

Echinoderms

From the Greek ekhinos (spiny) and derma (skin). Marine deuterostome animals that include sea stars, sea cucumbers and sea urchins. They possess bilateral symmetry during larval stages, but in adult life they become radially symmetrical.

Imaginal disc

Single layer of epithelial cells that forms a sac-like structure in the larvae and gives rise to adult appendages after metamorphosis (for example, wings, legs, antenna, eyes and genitalia).

Cuticle

A rigid layer of sclerotized chitin and cuticular proteins that covers the insect larval and adult epidermis and constitutes the exoskeleton.

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Mieko Mizutani, C., Bier, E. EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9, 663–677 (2008). https://doi.org/10.1038/nrg2417

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