Origin of the prechordal plate and patterning of the anteroposterior regional specificity of the involuting and extending archenteron roof of a urodele, Cynops pyrrhogaster

Abstract

We analyzed the notochord formation, formation of the prechordal plate, and patterning of anteroposterior regional specificity of the involuting and extending archenteron roof of a urodele, Cynops pyrrhogaster. The lower (LDMZ) and upper (UDMZ) domains of the dorsal marginal zone (DMZ) of the early gastrula involuted and formed two distinct domains: the anterior fore-notochordal endodermal roof and the posterior domain containing the prospective notochord. Cygsc is expressed in the LDMZ from the onset of gastrulation, and the Cygsc-expressing LDMZ planarly induces the notochord in the UDMZ at the early to mid gastrula stages. At the mid to late gastrula stages, part of the Cygsc-expressing LDMZ is confined to the prechordal plate. On the other hand, Cybra expression only begins at mid gastrula stage, coincident with notochord induction at this stage. Anteroposterior regional specificity of the neural plate was patterned by the posterior domain of the involuting archenteron roof containing the prospective notochord at the mid to late gastrula stages. Cynops gastrulation thus differs significantly from Xenopus gastrulation in that the regions of the DMZ are specified from the onset of gastrulation, while the equivalent state of specification does not occur in Cynops until the middle of gastrulation. Thus we propose that Cynops gastrulation is divided into two phases: a notochord induction phase in the early to mid gastrula, and a neural induction phase in the mid to late gastrula.

EphA4-dependent Brachyury expression is required for dorsal mesoderm involution in the Xenopus gastrula

“…The ring-shaped expression of Brachyury in the blastula marginal zone disappears, to be replaced later by expression in the constricting blastopore; still later, after blastopore closure, Brachyury expression appears in the prospective notochord, suggesting that a tri-phasic Brachyury expression pattern could be ancestral for anurans. In the urodeles Cynops and Ambystoma, Brachyury is expressed late, after the Gscexpressing anterior mesoderm has involuted, but in time for the involution of the Brachyury-expressing posterior mesoderm (Kaneda et al, 2009;Swiers et al, 2010). It remains to be determined, however, whether a role in germ layer internalization is indeed a common feature of the amphibian or even the metazoan Brachyury gene.…”

Gastrulation and pre-gastrulation morphogenesis, inductions, and gene expression: Similarities and dissimilarities between urodelean and anuran embryos

“…At the yolk-plug stage, Cybra expression is restricted to involuted and elongated notochord and surface presumptive tail mesoderm around the blastopore (Sone et al, 1997;Doi et al, 2000;Kaneda et al, 2009). At the neurula stage, Cybra expression is detected in the entire notochord (Figs.…”

“…It has been demonstrated that the vegetal (lower) half of the Cynops early gastrula DMZ (LDMZ) forms the anterior half of the ARF that self-differentiates only into endodermal tissues, such as pharyngeal endoderm (Kaneda et al, 2009). The animal (upper) half of the DMZ (UDMZ) forms the entire notochord after involution.…”

“…In Cynops, goosecoid (Cygsc), noggin (Cynog), chordin (Cychd), Lim-1 (CyLim-1) and VegT (CyVegT) expressions are preferentially restricted to the LDMZ; their expression does not extend to the UDMZ or the sub-blastoporal region (Sone et al, 1997;Yokota et al, 1998;Doi et al, 2000;Kaneda et al, 2009;Motoki et al, unpublished;see Figs. 4B, 5B and Table 1).…”

“…Although the embryonic stage, isolation size, spatial localization and methods of identifying the self-differentiation and organizing capacities vary among studies according to the defining criteria used, the self-differentiation and organizing activities of the early gastrula DMZ have been extensively analyzed in many urodeles (e.g., Spemann and Mangold, 1924;Holtfreter, 1938a;Holtfreter-Ban, 1965;Kaneda and Hama, 1979;Kaneda, 1980Kaneda, , 1981Slack, 1984;Cleine and Slack, 1985;Hama et al, 1985;Delarue et al, 1992;Yamamoto and Suzuki, 1994;Imoh et al, 1998;Kaneda et al, 2002Kaneda et al, , 2009 and in anura species (e.g., Holtfreter, 1938b;Smith and Slack, 1983;Gerhart, 1990, 1991;Shih and Keller, 1992;Domingo and Keller, 1995;Lane and Keller, 1997;Manes and Campos Casal, 1997;Fujii et al, 2002). By inserting the DLP into the blastocoel, earlier experiments revealed that the DLP of the early gastrula has secondary axis organizing activity in which the inserted DLP differentiates into notochord, somites and endoderm, while the secondary neural axis originates from the host embryo (e.g., Spemann and Mangold, 1924).…”