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Research Article
Mechanisms of endoderm formation in a cartilaginous fish reveal ancestral and homoplastic traits in jawed vertebrates
Benoit G. Godard, Marion Coolen, Sophie Le Panse, Aurélie Gombault, Susana Ferreiro-Galve, Laurent Laguerre, Ronan Lagadec, Patrick Wincker, Julie Poulain, Corinne Da Silva, Shigehiro Kuraku, Wilfrid Carre, Agnès Boutet, Sylvie Mazan
Biology Open 2014 3: 1098-1107; doi: 10.1242/bio.20148037
Benoit G. Godard
1Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France
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Marion Coolen
2Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France
7Present address: CNRS UPR 3294, Institute of Neurobiology Alfred Fessard, 91198 Gif-sur-Yvette, France.
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Sophie Le Panse
3Plateforme d'Imagerie, Sorbonne Universités, UPMC Univ Paris 06, CNRS, FR 2424, Station Biologique, 29688 Roscoff, France
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Aurélie Gombault
2Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France
9Present address: UMR 7355, Université d'Orleans-CNRS, 45071 Orléans, France.
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Susana Ferreiro-Galve
2Université d'Orléans-CNRS, UMR 6218, 45070 Orléans, France
8Present address: Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas y Universidad Miguel Hernández, Campus San Juan de Alicante, 03550 Alicante, Spain.
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Laurent Laguerre
1Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France
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Ronan Lagadec
1Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France
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Patrick Wincker
4CEA-Institut de Génomique-Genoscope, 2 rue Gaston-Crémieux, 91057 Evry, France
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Julie Poulain
4CEA-Institut de Génomique-Genoscope, 2 rue Gaston-Crémieux, 91057 Evry, France
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Corinne Da Silva
4CEA-Institut de Génomique-Genoscope, 2 rue Gaston-Crémieux, 91057 Evry, France
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Shigehiro Kuraku
5Genome Resource and Analysis Unit (GRAS), Center for Developmental Biology, RIKEN.2-2-3 Minatojima-minami, Chuo-KU, Kobe 650-0047, Japan
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Wilfrid Carre
6ABiMS, Sorbonne Universités, UPMC Univ Paris 06, CNRS, FR 2424, 29688 Roscoff, France
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Agnès Boutet
1Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France
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Sylvie Mazan
1Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR 7150, 29688 Roscoff, France
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  • For correspondence: smazan@sb-roscoff.fr
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Data supplements

  • bio.20148037 Supplementary Material

    Files in this Data Supplement:

    • Supplementary Material - Benoit G. Godard et al. doi: 10.1242/bio.20148037
    • Movie 1 - Movie 1. Time lapse imaging of a developing catshark embryo (stages 6 to 10). The movie shows a dorsal view of a catshark embryo from stages 6 to 10, anterior (referring to the orientation of the future embryonic axis) to the left. At early blastula stages (stages 6–7), the blastoderm is round-shaped, less than 1.5 mm diameter and surrounded by a characteristic white area. The blastocoel appears as a crescent located to the posterior side of the blastoderm at stage 6 and disappears at stage 7. Stages 8 to 9 (midblastula) are characterized by a size expansion and the partial (stage 8) to complete (stage 9) disappearance of the white area surrounding the blastoderm. Stage 10 is marked by the appearance of a thickening of the posterior side of the blastoderm. For the movie, a window was opened in the eggshell at the embryo level and photographs were taken every 15 minutes using an Olympus SZX12 stereomicroscope and a Qimaging colour 12-bit digital camera for the duration indicated in the movie.
    • Movie 2 - Movie 2. Time lapse imaging of a developing catshark embryo (stages 11 to 15). The movie shows a dorsal view of a catshark embryon from stages 11 to 15, anterior to the left. The embryonic axis proper forms in the posterior part of the blastoderm, while anterior and lateral blastoderm territories spread over the yolk to form the yolk sac. Stage 11 is characterized by the morphological appearance of the involuting mesendoderm layer, which extends over the yolk at the posterior margin. At stage 12, the ScT positive (Sauka-Spengler et al., 2003), bilaterally symmetrical extensions which form on each side of the midline at the posterior margin are referred to as the posterior arms and the midline, ScChordin positive groove visible at this level (this study) is referred to as the notochordal triangle, following the nomenclature of Ballard et al. (Ballard et al., 1993). The anterior-most part of the embryonic axis, positive for ScGsc and ScOtx1/2, forms at this stage (Coolen et al., 2007). At this stage, trunk markers are restricted to the posterior arms (Coolen et al., 2007). The neural groove becomes visible in the anterior part of the forming embryonic axis at stage 13 while mesendoderm internalization progresses at the trunk level, as assessed by ScT and trunk markers expression (Sauka-Spengler et al., 2003; Coolen et al., 2007). At subsequent stages, the embryonic axis elongates from anterior to posterior with a sharp temporal regulation (Coolen et al., 2007). At stage 14, the neural plate exhibits an enlargement in the cephalic region, and the neural folds lying between the prospective epidermis and the neural plate become clearly delineated. At stage 15, the neural groove hollows and the neural folds get closer together (Coolen et al., 2007). We refer to the mesenchymal cell population in contact with the yolk as deep mesenchyme (dm) and to the involuting lower cell layer observed starting from stage 11 (onset of gastrulation) as involuting mesendoderm (ime). For the movie, a window was opened in the eggshell at the embryo level and photographs were taken every 15 minutes using an Olympus SZX12 stereomicroscope and a Qimaging colour 12-bit digital camera for the duration indicated in the movie.
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Keywords

  • Endoderm
  • telolecithal egg
  • chondrichthyan
  • Nodal signalling

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Research Article
Mechanisms of endoderm formation in a cartilaginous fish reveal ancestral and homoplastic traits in jawed vertebrates
Benoit G. Godard, Marion Coolen, Sophie Le Panse, Aurélie Gombault, Susana Ferreiro-Galve, Laurent Laguerre, Ronan Lagadec, Patrick Wincker, Julie Poulain, Corinne Da Silva, Shigehiro Kuraku, Wilfrid Carre, Agnès Boutet, Sylvie Mazan
Biology Open 2014 3: 1098-1107; doi: 10.1242/bio.20148037
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Research Article
Mechanisms of endoderm formation in a cartilaginous fish reveal ancestral and homoplastic traits in jawed vertebrates
Benoit G. Godard, Marion Coolen, Sophie Le Panse, Aurélie Gombault, Susana Ferreiro-Galve, Laurent Laguerre, Ronan Lagadec, Patrick Wincker, Julie Poulain, Corinne Da Silva, Shigehiro Kuraku, Wilfrid Carre, Agnès Boutet, Sylvie Mazan
Biology Open 2014 3: 1098-1107; doi: 10.1242/bio.20148037

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