Abstract
We have compared the dorsoventral development of hemichordates and chordates to deduce the organization of their common ancestor, and hence to identify the evolutionary modifications of the chordate body axis after the lineages split. In the hemichordate embryo, genes encoding bone morphogenetic proteins (Bmp) 2/4 and 5/8, as well as several genes for modulators of Bmp activity, are expressed in a thin stripe of ectoderm on one midline, historically called “dorsal.” On the opposite midline, the genes encoding Chordin and Anti-dorsalizing morphogenetic protein (Admp) are expressed. Thus, we find a Bmp-Chordin developmental axis preceding and underlying the anatomical dorsoventral axis of hemichordates, adding to the evidence from Drosophila and chordates that this axis may be at least as ancient as the first bilateral animals. Numerous genes encoding transcription factors and signaling ligands are expressed in the three germ layers of hemichordate embryos in distinct dorsoventral domains, such as pox neuro, pituitary homeobox, distalless, and tbx2/3 on the Bmp side and netrin, mnx, mox, and single-minded on the Chordin-Admp side. When we expose the embryo to excess Bmp protein, or when we deplete endogenous Bmp by small interfering RNA injections, these expression domains expand or contract, reflecting their activation or repression by Bmp, and the embryos develop as dorsalized or ventralized limit forms. Dorsoventral patterning is independent of anterior/posterior patterning, as in Drosophila but not chordates. Unlike both chordates and Drosophila, neural gene expression in hemichordates is not repressed by high Bmp levels, consistent with their development of a diffuse rather than centralized nervous system. We suggest that the common ancestor of hemichordates and chordates did not use its Bmp-Chordin axis to segregate epidermal and neural ectoderm but to pattern many other dorsoventral aspects of the germ layers, including neural cell fates within a diffuse nervous system. Accordingly, centralization was added in the chordate line by neural-epidermal segregation, mediated by the pre-existing Bmp-Chordin axis. Finally, since hemichordates develop the mouth on the non-Bmp side, like arthropods but opposite to chordates, the mouth and Bmp-Chordin axis may have rearranged in the chordate line, one relative to the other.
Highlights
Arthropods and chordates and presumably all bilaterians are fundamentally similar in the development of their body plans [1,2]
We have examined the topology of expression of a range of orthologs of genes in S. kowalevskii embryos that are known in vertebrates to depend on the bone morphogenetic proteins (Bmp)-Chordin axis for their domain location and to have roles in dorsoventral development
Bmp Signaling and the bmp Synexpression Group The site of Bmp signaling in the embryos of chordates and arthropods defines one pole of the Bmp-Chordin developmental axis
Summary
Arthropods (especially Drosophila) and chordates (especially mouse, fish, frogs, and birds) and presumably all bilaterians are fundamentally similar in the development of their body plans [1,2]. Suites of genes are arranged in conserved domain maps in both the anteroposterior and dorsoventral dimensions of developing embryos. This conservation of axial patterning provides the developmental platform for astonishing anatomical and physiological diversification both within and between phyla. At least back to the Cambrian, have numerous anatomical and physiological specializations located along this axis, in all three germ layers. The mesodermal tissues such as the heart, blood forming elements (and the direction of blood flow), gonads, visceral muscle, and striated muscle are arranged in dorsoventral patterns. The gill slits (in chordates and hemichordates) and other endodermal organs
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