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Background: The notochord has organizer properties and is required for floor plate induction and dorsoventral patterning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the floor plate. However, reported data are inconsistent and the spatiotemporal development of the relevant shh expression domains has not been studied in detail. We therefore studied the expression dynamics of shh in rabbit, chicken and Xenopus laevis embryos (as well as indian hedgehog and desert hedgehog as possible alternative functional candidates in the chicken).
Results: Our analysis reveals a markedly divergent pattern within these vertebrates: whereas in the rabbit shh is first expressed in the notochord and its floor plate domain is then induced during subsequent somitogenesis stages, in the chick embryoshh is expressed in the prospective neuroectoderm prior to the notochord formation and, interestingly, prior to mesoderm immigration. Neither indian hedgehog nor desert hedgehog are expressed in these midline structures although mRNA of both genes was detected in other structures of the early chick embryo. In X. laevis, shh is expressed at the beginning of gastrulation in a distinct area dorsal to the dorsal blastopore lip and adjacent to the prospective neuroectoderm, whereas the floor plate expresses shh at the end of gastrulation.
Conclusions: While shh expression patterns in rabbit and X. laevis embryos are roughly compatible with the classical view of "ventral to dorsal induction" of the floor plate, the early shh expression in the chick floor plate challenges this model. Intriguingly, this alternative sequence of domain induction is related to the asymmetrical morphogenesis of the primitive node and other axial organs in the chick. Our results indicate that the floor plate in X. laevis and chick embryos may be initially induced by planar interaction within the ectoderm or epiblast. Furthermore, we propose that the mode of the floor plate induction adapts to the variant topography of interacting tissues during gastrulation and notochord formation and thereby reveals evolutionary plasticity of early embryonic induction.
Fig. 1. Temporal dynamics of shh expression in the chick. a–c whole-mount views of embryos at HH stage 5 (a), 7 (b) and 8 (c); median sagittal technovit sections of stage 5 (d) and stage 7 (e); f–j transversal sections of HH stage 8 embryos at the levels shown in c. i median sagittal section of stage 8 embryo. Labeling: fp floor plate, am axial mesoderm, ec ectoderm, en endoderm, n node, pm prechordal mesoderm, sp preoral gut (prospective area of Seessel’s pouch), se superficialectoderm, arrow—position of the node. Intersecting arrows indicate anatomical axes: A anterior, P posterior, L left, R right, D dorsal, V ventral. Scale bar 400 µm (a–c), 75 μm (e) and 50 µm (d, f–i)
Fig. 2. Early shh expression in the chick stage 2 +/3 − embryo. Arrow: position of the tip of the primitive streak
Fig. 3. Expression of Indian hedgehog (ihh) and desert hedgehog (dhh) in the chick. a, b whole-mount views of ihh expression at HH stage 4 (a) and 7 (b). c transversal technovit section of embryo shown in b; d
ihh expression in the gutendoderm (HH stage 17); whole-mount view (e) and section (f) of dhh expression in the dorsal part of intermediate mesoderm (HH stage 11); f
dhh expression in the mesonephric tubules (HH stage 17). N notochord, fp floor plate, im intermediate mesoderm, s somite, vv vitelline vein, md mesonephric duct, mt mesonephric tubule, arrowhead—position of the node
Fig. 4. Temporal dynamics of shh expression in the rabbit embryo. a–c whole-mount views of stage 5 − (a), 5 + (b) and 8 (c) embryos. d–j transversal technovit sections of a–c. Levels of sections are shown in a–c. Labeling: f floor plate, am axial mesoderm, nm node mesoderm. Intersecting arrows in a indicate anatomical axes: A anterior, P posterior, L left, R right, D dorsal, V ventral. Scale bar 250 (a, b), 400 (c) and 50 µm (d–j)
Fig. 5. a–f temporal dynamics of shh expression in Xenopus laevis embryos between early gastrula and tadpole stages. g–h expression of patched 2 at middle (g) and late (h) gastrula stage. bl Blastopore. Scale bar 200 µm
Fig. 6. Technovit sections of Xenopus laevis embryos at early gastrula (a), mid-gastrula (b), late gastrula (c, d), early neurula (e–g) and tailbud stage (h) at levels shown in Fig. 3. Labeling: ec midline neuroectoderm, am axial mesoderm, se superficialectoderm, pam preaxial mesoderm (leading edge), s somites, nt neural tube. Intersecting arrows in indicate anatomical axes: A animal, Veg vegetal, L left, R right, D dorsal, V ventral
Fig. 7. Axial morphogenesis during initial stages of primitive streak regression in the schematic dorsal view of chick embryo between stages 4 + (a), 5 − (b) and 5 + (c). Labeling: aqua blue—shh domain in the epiblast/ectoderm, red—notochord and its proposed progenitor domain, pink—primitive streak. Dotted arrows indicate directions of tissue displacement
Fig. 8. Expansion of prospective neural plate and growth of notochord from the node in the schematic dorsal view of rabbit embryo. a prior to the notochord formation (stage 4), b early notochord stage (stage 5). Labeling: arrows—growth of the blastoderm, dotted arrow—direction of notochord growth, red—notochord, pink—primitive streak, black—primitive groove
Fig. 9. Schematic view of Xenopus laevis embryo during early and mid-gastrula: a dorsal view, b and c midline sagittal view. Labeling: red axial mesoderm, aqua blue—midline neuroectoderm, dark blue—shh expression domain, gray—bottle cells; blc—blastocoel, bl—blastopore, dotted arrows—direction of proposed induction, blue arrows—directions of morphogenetic movements, dotted curve in a—dorsal blastopore lip
Fig. 10. Initial shh expression in context of phylogeny of chordate. MNE midline neuroectoderm, AM axial mesoderm. References: 1—this report, 2—[10], 3—[34], 4—[84], 5—[72]
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