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Dev Biol
2012 Sep 01;3691:1-18. doi: 10.1016/j.ydbio.2012.05.019.
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Gastrulation and pre-gastrulation morphogenesis, inductions, and gene expression: similarities and dissimilarities between urodelean and anuran embryos.
Kaneda T
,
Motoki JY
.
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Studies of meso-endoderm and neural induction and subsequent body plan formation have been analyzed using mainly amphibians as the experimental model. Xenopus is currently the predominant model, because it best enables molecular analysis of these induction processes. However, much of the embryological information on these inductions (e.g., those of the Spemann-Mangold organizer), and on the morphogenetic movements of inductively interacting tissues, derives from research on non-model amphibians, especially urodeles. Although the final body pattern is strongly conserved in vertebrates, and although many of the same developmental genes are expressed, it has become evident that there are individually diverse modes of morphogenesis and timing of developmental events. Whether or not this diversity represents essential differences in the early induction processes remains unclear. The aim of this review is to compare the gastrulation process, induction processes, and gene expressions between a urodele, mainly Cynops pyrrhogaster, and an anura, Xenopus laevis, thereby to clarify conserved and diversified aspects. Cynops gastrulation differs significantly from that of Xenopus in that specification of the regions of the Xenopus dorsal marginal zone (DMZ) are specified before the onset of gastrulation, as marked by blastopore formation, whereas the equivalent state of specification does not occur in Cynops until the middle of gastrulation. Detailed comparison of the germ layer structure and morphogenetic movements during the pre-gastrula and gastrula stages shows that the entire gastrulation process should be divided into two phases of notochord induction and neural induction. Cynops undergoes these processes sequentially after the onset of gastrulation, whereas Xenopus undergoes notochord induction during a series of pre-gastrulation movements, and its traditionally defined period of gastrulation only includes the neural induction phase. Comparing the structure, fate, function and state of commitment of each domain of the DMZ of Xenopus and Cynops has revealed that the true form of the Spemann-Mangold organizer is suprablastoporal gsc-expressing endoderm that has notochord-inducing activity. Gsc-expressing deependoderm and/or superficialendoderm in Xenopus is involved in inducing notochord during pre-gastrulation morphogenesis, rather than both gsc- and bra-expressing tissues being induced at the same time.
Fig. 3. Fine structure of Cynops early gastrula dorsal marginal zone (DMZ) and the structure of the involuted archenteron roof. (A) At the late blastula/early gastrula stage, the animal cap and DMZ are single-cell-layered structures, except for the most vegetal (future anterior) part of the LDMZ region. The Cynops embryo is approximately 2.2.4 mm in diameter. (Reproduced with permission from Suzuki et al., 1994, Dev. Growth Differ. 39, 13541); (B) External form of a stage 11 beginning gastrula. The crescent-shaped pigment line (PL) is formed by the accumulation of bottle cells at the dorso-vegetally restricted blastopore (Blp) site. (C) Fine structure of the blastopore (Blp) with bottle cells (red dotted circle) at stage 11. (D) Involution of the DMZ about 6 h after the onset of gastrulation (approximately stage 12a). Bottle cells are seen in the red dotted circle. (Figs. C and D reproduced with permission from Sakaguchi et al., 2002, Int. J. Dev. Biol., 79300); (E) Spemann and Mangold (1924) inserted the DLP into the blastocoel of the host embryo and analyzed the organizing activity of the DLP. Imoh et al. (1998) transplanted the LDMZ into the surface layer of the host embryo. The LDMZ is isolated with bottle cells and part of the sub-blastoporal endoderm from a FDA-labeled embryo, transplanted into the surface layer of the ventral part of a stage 11 gastrula and then the FDADMZ transplanted embryo develops to the late gastrula stage. Transplanted LDMZ induces a complete secondary archenteron roof (ARF) in which the notochord of the secondary axis is entirely derived from host cells, while the transplanted LDMZ forms the fore-notochordal endodermal roof (FNE) of the secondary ARF. (Reproduced with permission from Imoh et al., 1998, Dev. Growth Differ. 40, 43948). (F) Single-cell-layered structure of the late gastrula ARF. It is divided into notochord (Nt) and FNE. Dotted line is the approximate position of the boundary between the notochord and FNE. Neu, neuroectoderm. (G) Cross-section of the early neurula ARF. Notochordal plate (Nt) occupies the median line of the ARF. Lateralmesoderm (LM) is covered with lateral endodermal crest (LEC). During neurulation, LEC progressively covers the Nt, and the ARF is finally covered with endoderm at the mid- to late neurula stage. Blue dotted line represents the boundary between neuroectoderm and LM. Red dotted line represents the boundary between LM and LEC. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 4. Fate map and gene expression domains of Cynops early gastrula. (A) Fate map of Cynops late blastula/early gastrulaembryo (right-lateral view, redrawn from Nakamura, 1942). Like other urodeles ( [Vogt, 1929] and [Pasteels, 1942]), Cynops has a large surface prospective mesoderm. Presumptive pharyngeal endoderm (PhE), prechordal plate (PrC), notochord (NT) and tailsomites (Pre-Sm) are planarly located on the embryo's surface. Presumptive anterior and trunksomites (Pre-Sm) are located lateral to the presumptive notochord. (B) Gene expression map of early Cynops gastrula (dorso-vegetal view). At the early gastrula stage, expressions of Cygsc, Cychd, Cylim-1, Cynog and CyVegT are preferentially restricted to the LDMZ (light green), and their expressions do not extend below the blastopore. CyNodal (Ito et al., 2006) is expressed around the marginal zone, except for the LDMZ region. Cynops Wnt-8 is expressed in the ventro-vegetal part of the embryo (gray) around the vegetal pole (Vp), but Wnt-8 expression does not extend beyond the blastopore (Blp). Cybra is not expressed in any part of the embryo at this stage. The presumptive notochord (UDMZ) has epidermal self-differentiation capacity at this stage and no inducing activity. (Gene expression patterns are from Motoki et al., unpublished). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 6. Gene expression patterns at the neurula stage of Cynops. (A) Cygsc, (B) Cychd and (C) Cybra expression at the neurula stage (stage 18) of Cynops. Cygsc expression is restricted to the fore-notochordal endodermal roof (FNE), just anterior to the notochord. Cychd and Cybra expressions are restricted to the entire notochord. Arrowhead indicates the anterior end of the notochord. (A and C from Kaneda et al., 2009; B is from Motoki et al., unpublished.).
Fig. 8. Gene expression, self-differentiation and notochord-inducing activity of the dorsal marginal zone (DMZ) of the early gastrula of Cynops. (A) The early gastrula (stage 11) DMZ of Cynops is divided into two domains of UDMZ (future trunkail notochord) and LDMZ (future pharyngeal endoderm/prechordal plate). (B) The UDMZ and LDMZ are separately isolated and Cygsc and Cybra expressions analyzed. The UDMZ express neither Cygsc nor Cybra at stage 11 (B, C). The expression is unchanged when isolated UDMZ is cultured in vitro for 24 h. LDMZ expresses Cygsc but not Cybra (D, E). When the LDMZ is isolated and cultured in vitro for 24 h, Cygsc expression is maintained. (F) Keller sandwich of early gastrulaDMZ. The early gastrulaDMZ was isolated and cultured in the Keller sandwiches for 24 h at 20 until the control embryo developed to the late gastrula (stage 13b/c). Cybra expression was planarly induced in the UDMZ part of the explants. Approximate position of the UDMZ is marked by asterisks (B reproduced from Kaneda et al., 2009.); (G, I, J) Self-differentiation of the LDMZ in the isolation culture. LDMZ differentiates to an endodermal cell mass. Any mesodermal or ectodermal tissues are differentiated. (I and J reproduced with permission from Sakaguchi et al., 2002, Int. J. Dev. Biol., 46, 79300). (H) UDMZ self-differentiates to epidermis. (K) When the LDMZ is combined with a small piece of animal cap ectoderm, the animal cap ectoderm is induced to notochord (Nt) and muscle cells (Mus), while LDMZ itself differentiates into a mass of endodermal cells.
Fig. 9. Planar notochord induction in the upper dorsal marginal zone during the early phase of Cynops gastrulation. (A, B) Spatial and temporal process of anteroposterior regional patterning of the involuting and extending ARF. At the early gastrula stage, the Cygsc-expressing LDMZ is identified as the rechordal regionand the notochord is not yet induced in the UDMZ. During early to mid-gastrulation, the LDMZ planarly induces Cybra-expressing notochord in the UDMZ. As involution proceeds, the LDMZ loses its notochord-inducing activity and forms the fore-notochordal endodermal roof (FNE). Cygsc expression of the LDMZ is progressively restricted to the FNE just anterior to the induced notochord, and finally confined to the prechordal plate. (C) Spatial and temporal expression patterns of Cybra and Cygsc during gastrulation. At stage 11, Cygsc expression is restricted to the surface region of the suprablastoporal endodermal prechordal region (LDMZ); however, Cybra expression is not identified in any part of the embryo. Cybra expression is first induced in the surface presumptive notochord at the mid-gastrula stage (stage 12b). At this stage, Cygsc-expressing cells involute and underlie the surface Cybra-expressing region. Despite the Cygsc expression, the anterior two-thirds of the ARF at this stage show no inducing activity. At the late gastrula stage (stage 13c), Cygsc expression is progressively restricted to the FNE anterior to the induced notochord. At this stage, Cybra is expressed in the posterior one-third of the ARF and the surface region around the blastopore. In neurulae, Cybra expression is restricted to notochord, and the Cygsc-expressing region is confined to the prechordal plate beneath the anterior neural plate. Arrows indicate the anterior margin of the involuting ARF. In B and C, left and right represent the anterior and posterior directions, respectively. blp: blastopore; yp: yolk plug. (B and C reproduced from Kaneda et al., 2009.).
