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Dev Biol
2010 Aug 01;3441:138-49. doi: 10.1016/j.ydbio.2010.04.028.
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The ascidian mouth opening is derived from the anterior neuropore: reassessing the mouth/neural tube relationship in chordate evolution.
Veeman MT
,
Newman-Smith E
,
El-Nachef D
,
Smith WC
.
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The relative positions of the brain and mouth are of central importance for models of chordate evolution. The dorsal hollow neural tube and the mouth have often been thought of as developmentally distinct structures that may have followed independent evolutionary paths. In most chordates however, including vertebrates and ascidians, the mouthprimordia have been shown to fate to the anterior neural boundary. In ascidians such as Ciona there is a particularly intimate relationship between brain and mouth development, with a thin canal connecting the neural tube lumen to the mouthprimordium at larval stages. This so-called neurohypophyseal canal was previously thought to be a secondary connection that formed relatively late, after the independent formation of the mouthprimordium and the neural tube. Here we show that the Ciona neurohypophyseal canal is present from the end of neurulation and represents the anteriormost neural tube, and that the future mouth opening is actually derived from the anterior neuropore. The mouth thus forms at the anterior midline transition between neural tube and surface ectoderm. In the vertebrate Xenopus, we find that although the mouthprimordium is not topologically continuous with the neural tube lumen, it nonetheless forms at this same transition point. This close association between the mouthprimordium and the anterior neural tube in both ascidians and amphibians suggests that the evolution of these two structures may be more closely linked than previously appreciated.
Fig. 8. Early fate mapping of the Xenopus mouth. (A) Selected timepoints from a timelapse of Xenopus neural tube closure. The embryo is oriented in a modeling clay well with anterior facing the camera and dorsal to the top. Time and approximate Nieuwkoop and Faber stages are indicated. Scale bar: 300 μM. In (E), the blue arrowhead indicates the anterior neuropore and the white arrowhead the dorsal border of the forming cement gland. (I) Small groups of cells were labeled with DiI as the neuropore was closing, either (I) just ventral to the neuropore (neuropore indicated with blue arrowhead) or (J) just dorsal to the cement gland (boundary indicated with white arrowhead). The neural tube is outlined with a blue dashed line and the cement gland with a yellow dashed line. (I′, J′) The same embryos imaged again at stage 28. The white circle indicates where the mouth will form. (K, L) Wholemount confocal imaging of fixed, cleared Xenopus embryos stained for laminin (green) and nuclei (magenta). (K) Stage 18/19. (L) Stage 27/28. The blue arrowhead marks the anterior neuropore. The white arrowhead marks the dorsal boundary of the cement gland. The yellow bracket marks the cement gland. The blue bracket marks the neural tube. The white bracket marks the site of mouth formation. (K′, L′) Schematic cartoons of K and L showing the neural tube (bright green), mouthprimordium (pale green, also marked with a white asterisk), epidermis (blue), endoderm (magenta) and mesoderm (brown).
Fig. 9. Model of the mouth/neural tube relationship for a generic chordate and chordate ancestor. (A, B) Schematic representation based on our observations in Ciona and Xenopus of a generic chordate both before (A, A′) and after (B, B′) neurulation. The neural plate is marked in green and the presumptive site of mouth formation is shown in magenta. Anterior is to the left. (A, B) Dorsal views. (A′ ,B′) Lateral views. Note that the mouthprimordium arises at the precise topological transition between the definitive neural tube (internalized by neurulation) and the anterior adhesive organ (cement gland/palps), which remains on the surface. (C) Schematic view of the ventral side of a hypothetical pre-inversion chordate ancestor. The mouth (left) and anus (right) are shown in magenta. The ventral neurogenic region (green) is partly folded to form an accessory pocket of the mouth.
