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Evodevo
2018 Jan 31;9:4. doi: 10.1186/s13227-017-0090-x.
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Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate.
Kremnyov S
,
Henningfeld K
,
Viebahn C
,
Tsikolia N
.
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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]
Alev,
Decoupling of amniote gastrulation and streak formation reveals a morphogenetic unity in vertebrate mesoderm induction.
2013, Pubmed
Alev,
Decoupling of amniote gastrulation and streak formation reveals a morphogenetic unity in vertebrate mesoderm induction.
2013,
Pubmed
Anderson,
Organizers in Development.
2016,
Pubmed
Ang,
HNF-3 beta is essential for node and notochord formation in mouse development.
1994,
Pubmed
Arendt,
Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs.
1999,
Pubmed
,
Xenbase
Bates,
Development of myoplasm-enriched ascidian embryos.
1988,
Pubmed
Bertocchini,
A little winning streak: the reptilian-eye view of gastrulation in birds.
2013,
Pubmed
Catala,
A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls.
1996,
Pubmed
Chamberlain,
Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning.
2008,
Pubmed
Charrier,
Defining subregions of Hensen's node essential for caudalward movement, midline development and cell survival.
1999,
Pubmed
,
Xenbase
Chizhikov,
Roof plate-dependent patterning of the vertebrate dorsal central nervous system.
2005,
Pubmed
Cohen,
Morphogen interpretation: the transcriptional logic of neural tube patterning.
2013,
Pubmed
Cruz,
Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling.
2010,
Pubmed
Cui,
Rotation of organizer tissue contributes to left-right asymmetry.
2009,
Pubmed
Currie,
Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish.
1996,
Pubmed
Dathe,
Morphological left-right asymmetry of Hensen's node precedes the asymmetric expression of Shh and Fgf8 in the chick embryo.
2002,
Pubmed
Echelard,
Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity.
1993,
Pubmed
Ekker,
Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis.
1995,
Pubmed
,
Xenbase
Ekker,
Patterning activities of vertebrate hedgehog proteins in the developing eye and brain.
1995,
Pubmed
Etheridge,
Floor plate develops upon depletion of tiggy-winkle and sonic hedgehog.
2001,
Pubmed
Fernández-Garre,
Fate map of the chicken neural plate at stage 4.
2002,
Pubmed
Fernández-Garre,
A neural plate fate map at stage HH4 in the chick: methodology and preliminary data.
,
Pubmed
Fischer,
FGF8 acts as a right determinant during establishment of the left-right axis in the rabbit.
2002,
Pubmed
Goulding,
The formation of sensorimotor circuits.
2002,
Pubmed
Gros,
Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick.
2009,
Pubmed
,
Xenbase
HAMBURGER,
A series of normal stages in the development of the chick embryo.
1951,
Pubmed
Halpern,
Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation.
1993,
Pubmed
Ishihara,
Reconstitution of a Patterned Neural Tube from Single Mouse Embryonic Stem Cells.
2017,
Pubmed
Johnson,
Sonic hedgehog: a key mediator of anterior-posterior patterning of the limb and dorso-ventral patterning of axial embryonic structures.
1994,
Pubmed
Joubin,
Molecular interactions continuously define the organizer during the cell movements of gastrulation.
1999,
Pubmed
Kinder,
The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm.
2001,
Pubmed
Krauss,
A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos.
1993,
Pubmed
Laland,
The extended evolutionary synthesis: its structure, assumptions and predictions.
2015,
Pubmed
Le Douarin,
Discussion point. Origin and specification of the neural tube floor plate: insights from the chick and zebrafish.
2000,
Pubmed
Lehmann,
[Not Available].
1928,
Pubmed
Levin,
A molecular pathway determining left-right asymmetry in chick embryogenesis.
1995,
Pubmed
Liem,
Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm.
1995,
Pubmed
,
Xenbase
Locascio,
Modularity and reshuffling of Snail and Slug expression during vertebrate evolution.
2002,
Pubmed
Lopez-Sanchez,
Localization of cells of the prospective neural plate, heart and somites within the primitive streak and epiblast of avian embryos at intermediate primitive-streak stages.
2001,
Pubmed
Martí,
Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo.
1995,
Pubmed
Megason,
A mitogen gradient of dorsal midline Wnts organizes growth in the CNS.
2002,
Pubmed
Moczek,
The nature of nurture and the future of evodevo: toward a theory of developmental evolution.
2012,
Pubmed
Nishida,
Developmental potential for tissue differentiation of fully dissociated cells of the ascidian embryo.
1992,
Pubmed
Odenthal,
Two distinct cell populations in the floor plate of the zebrafish are induced by different pathways.
2000,
Pubmed
Otto,
Early left-right asymmetries during axial morphogenesis in the chick embryo.
2014,
Pubmed
Patten,
Distinct modes of floor plate induction in the chick embryo.
2003,
Pubmed
Pearse,
Ptc1 and Ptc2 transcripts provide distinct readouts of Hedgehog signaling activity during chick embryogenesis.
2001,
Pubmed
Pera,
Patterning of the chick forebrain anlage by the prechordal plate.
1997,
Pubmed
Peterson,
Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning.
2012,
Pubmed
Peyrot,
A revised model of Xenopus dorsal midline development: differential and separable requirements for Notch and Shh signaling.
2011,
Pubmed
,
Xenbase
Pigliucci,
Phenotypic plasticity and evolution by genetic assimilation.
2006,
Pubmed
Placzek,
The floor plate: multiple cells, multiple signals.
2005,
Pubmed
,
Xenbase
Placzek,
Mesodermal control of neural cell identity: floor plate induction by the notochord.
1990,
Pubmed
Placzek,
Discussion point. The case for floor plate induction by the notochord.
2000,
Pubmed
Pourquié,
Control of dorsoventral patterning of somitic derivatives by notochord and floor plate.
1993,
Pubmed
Psychoyos,
Restoration of the organizer after radical ablation of Hensen's node and the anterior primitive streak in the chick embryo.
1996,
Pubmed
Puelles,
Correlation of a chicken stage 4 neural plate fate map with early gene expression patterns.
2005,
Pubmed
Ribes,
Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube.
2010,
Pubmed
Ribes,
Establishing and interpreting graded Sonic Hedgehog signaling during vertebrate neural tube patterning: the role of negative feedback.
2009,
Pubmed
Roelink,
Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord.
1994,
Pubmed
,
Xenbase
Ruiz i Altaba,
Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos.
1995,
Pubmed
,
Xenbase
Ruiz i Altaba,
Early stages of notochord and floor plate development in the chick embryo defined by normal and induced expression of HNF-3 beta.
1995,
Pubmed
SPRATT,
Regression and shortening of the primitive streak in the explanted chick blastoderm.
1947,
Pubmed
Schauerte,
Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish.
1998,
Pubmed
Schoenwolf,
Cell movements driving neurulation in avian embryos.
1991,
Pubmed
Schröder,
Paraxial Nodal Expression Reveals a Novel Conserved Structure of the Left-Right Organizer in Four Mammalian Species.
2016,
Pubmed
Selleck,
Fate mapping and cell lineage analysis of Hensen's node in the chick embryo.
1991,
Pubmed
Shih,
Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage.
1996,
Pubmed
Shimeld,
The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog.
1999,
Pubmed
Smith,
Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation.
1989,
Pubmed
Spemann,
Induction of embryonic primordia by implantation of organizers from a different species. 1923.
2001,
Pubmed
Stankova,
Rho kinase activity controls directional cell movements during primitive streak formation in the rabbit embryo.
2015,
Pubmed
Stower,
The evolution of amniote gastrulation: the blastopore-primitive streak transition.
2017,
Pubmed
Streit,
Initiation of neural induction by FGF signalling before gastrulation.
2000,
Pubmed
Swalla,
Mechanisms of gastrulation and tail formation in ascidians.
1993,
Pubmed
Swalla,
Interspecific hybridization between an anural and urodele ascidian: differential expression of urodele features suggests multiple mechanisms control anural development.
1990,
Pubmed
TUNG,
The developmental potencies of the blastomere layers in Amphioxus egg at the 32-cell stage.
1960,
Pubmed
Takatori,
Expression of hedgehog genes in Ciona intestinalis embryos.
2002,
Pubmed
Teillet,
The relationships between notochord and floor plate in vertebrate development revisited.
1998,
Pubmed
Tsikolia,
Paraxial left-sided nodal expression and the start of left-right patterning in the early chick embryo.
2012,
Pubmed
Tung,
Differentiation of the prospective ectodermal and entodermal cells after transplantation to new surroundings in Amphioxus.
1965,
Pubmed
Uygur,
Scaling Pattern to Variations in Size during Development of the Vertebrate Neural Tube.
2016,
Pubmed
Voiculescu,
The amniote primitive streak is defined by epithelial cell intercalation before gastrulation.
2007,
Pubmed
,
Xenbase
Voiculescu,
Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation.
2014,
Pubmed
West-Eberhard,
Developmental plasticity and the origin of species differences.
2005,
Pubmed
Yamanaka,
Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms.
2007,
Pubmed
Zhang,
Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node.
2001,
Pubmed
,
Xenbase
van Straaten,
Effect of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo.
1988,
Pubmed
van Straaten,
Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo.
1991,
Pubmed
