Abstract
ABSTRACTIn order to gain insight into the impact of yolk increase on endoderm development, we have analyzed the mechanisms of endoderm formation in the catshark S. canicula, a species exhibiting telolecithal eggs and a distinct yolk sac. We show that in this species, endoderm markers are expressed in two distinct tissues, the deep mesenchyme, a mesenchymal population of deep blastomeres lying beneath the epithelial-like superficial layer, already specified at early blastula stages, and the involuting mesendoderm layer, which appears at the blastoderm posterior margin at the onset of gastrulation. Formation of the deep mesenchyme involves cell internalizations from the superficial layer prior to gastrulation, by a movement suggestive of ingressions. These cell movements were observed not only at the posterior margin, where massive internalizations take place prior to the start of involution, but also in the center of the blastoderm, where internalizations of single cells prevail. Like the adjacent involuting mesendoderm, the posterior deep mesenchyme expresses anterior mesendoderm markers under the control of Nodal/activin signaling. Comparisons across vertebrates support the conclusion that endoderm is specified in two distinct temporal phases in the catshark as in all major osteichthyan lineages, in line with an ancient origin of a biphasic mode of endoderm specification in gnathostomes. They also highlight unexpected similarities with amniotes, such as the occurrence of cell ingressions from the superficial layer prior to gastrulation. These similarities may correspond to homoplastic traits fixed separately in amniotes and chondrichthyans and related to the increase in egg yolk mass.
Highlights
Spectacular expansions of the egg yolk mass have taken place several times during vertebrate evolution, extreme examples of this evolutionary trend being observed in amniotes, cartilaginous fishes and myxinoids
The zebrafish yolk syncytial layer (YSL) forms by a collapse of marginal blastomeres with the yolk cell cytoplasmic cortex between the 512- to 1024-cell stage (Carvalho and Heisenberg, 2010). Despite these differences in morphogenesis, the amniote hypoblast/AVE and teleost dorsal YSL share expression of signaling molecules and transcription factors known as components of AME genetic programs, a similarity proposed to be related to independent recruitments in the amniote and actinopterygian lineages (Stern and Downs, 2012)
ScSox17 transcripts accumulated in the involuted mesendoderm along a 60 ̊ crescent of the posterior margin (Fig. 1C,D,D1; supplementary material Fig. S2D)
Summary
Spectacular expansions of the egg yolk mass have taken place several times during vertebrate evolution, extreme examples of this evolutionary trend being observed in amniotes, cartilaginous fishes and myxinoids. In the mouse, the primitive endoderm forms a morphologically distinct polarized epithelium, which arises from the blastocyst inner cell mass by a cell sorting mechanism, shortly after blastocoel formation It later subdivides into two components, the parietal endoderm and visceral endoderm, which contrary to the traditional view of an absolute early segregation between embryonic and extraembryonic tissues, is known to contribute to the gut (Rossant and Tam, 2009; Kwon et al, 2008). The zebrafish YSL forms by a collapse of marginal blastomeres with the yolk cell cytoplasmic cortex between the 512- to 1024-cell stage (Carvalho and Heisenberg, 2010) Despite these differences in morphogenesis, the amniote hypoblast/AVE (anterior visceral endoderm) and teleost dorsal YSL share expression of signaling molecules and transcription factors known as components of AME (anterior mesendoderm) genetic programs, a similarity proposed to be related to independent recruitments in the amniote and actinopterygian lineages (Stern and Downs, 2012)
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