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Biol Open. 2014 Oct 31;3(11):1098-107. doi: 10.1242/bio.20148037.

Mechanisms of endoderm formation in a cartilaginous fish reveal ancestral and homoplastic traits in jawed vertebrates.

Author information

1
Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France.
2
Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France Present address: CNRS UPR 3294, Institute of Neurobiology Alfred Fessard, 91198 Gif-sur-Yvette, France.
3
Plateforme d'Imagerie, Sorbonne Universités, UPMC Univ Paris 06, CNRS, FR 2424, Station Biologique, 29688 Roscoff, France.
4
Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France Present address: UMR 7355, Université d'Orleans-CNRS, 45071 Orléans, France.
5
Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France Present address: Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas y Universidad Miguel Hernández, Campus San Juan de Alicante, 03550 Alicante, Spain.
6
CEA-Institut de Génomique-Genoscope, 2 rue Gaston-Crémieux, 91057 Evry, France.
7
Genome Resource and Analysis Unit (GRAS), Center for Developmental Biology, RIKEN.2-2-3 Minatojima-minami, Chuo-KU, Kobe 650-0047, Japan.
8
ABiMS, Sorbonne Universités, UPMC Univ Paris 06, CNRS, FR 2424, 29688 Roscoff, France.
9
Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France smazan@sb-roscoff.fr.

Abstract

In 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.

KEYWORDS:

Nodal signalling; chondrichthyan; endoderm; telolecithal egg

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