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Scientific ReportsVolume 9, Issue 1, 1 December 2019, Article number 586

Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula(Article)(Open Access)

  • aCIIMAR – Interdisciplinary Centre of Marine and Environmental Research, Univ. Porto, Porto, Portugal
  • bInstitute of Biomedical Sciences Abel Salazar (ICBAS), Univ. Porto, Porto, Portugal
  • cI3S- Institute for Innovation and Health Research, Univ. Porto, Porto, Portugal
  • dIBMC- Institute for Molecular and Cell Biology, Univ. Porto, Porto, Portugal
  • eDepartment of Comparative Pathobiology, Purdue Univ., Lafayette, United States
  • fPurdue Institute for Integrative Neuroscience, Purdue Univ., Lafayette, United States
  • gPurdue Univ. Center for Cancer, Purdue Univ., Lafayette, United States
  • hPurdue Institute for Inflammation, Immunology and Infectious Diseases, Purdue Univ., Lafayette, United States
  • iCNRS, Sorbonne Universités, UPMC Univ. Paris, Observatoire Océanologique, Banyuls, France
  • jHoward Hughes Medical Institute, UF Genetics Institute, Univ. Florida, FL, United States
  • kDepartment of Biology, UF Genetics Institute, Univ. Florida, FL, United States
  • lDepartment of Molecular Genetics and Microbiology, UF Genetics Institute, Univ. Florida, FL, United States
  • mDepartment of Biology, Faculty of Sciences, Univ. Porto, Porto, Portugal
  • nDepartment of Biology, Wilfrid Laurier Univ., Waterloo, Canada

Abstract

The origin of extracellular digestion in metazoans was accompanied by structural and physiological alterations of the gut. These adaptations culminated in the differentiation of a novel digestive structure in jawed vertebrates, the stomach. Specific endoderm/mesenchyme signalling is required for stomach differentiation, involving the growth and transcription factors: 1) Shh and Bmp4, required for stomach outgrowth; 2) Barx1, Sfrps and Sox2, required for gastric epithelium development and 3) Cdx1 and Cdx2, involved in intestinal versus gastric identity. Thus, modulation of endoderm/mesenchyme signalling emerges as a plausible mechanism linked to the origin of the stomach. In order to gain insight into the ancient mechanisms capable of generating this structure in jawed vertebrates, we characterised the development of the gut in the catshark Scyliorhinus canicula. As chondrichthyans, these animals retained plesiomorphic features of jawed vertebrates, including a well-differentiated stomach. We identified a clear molecular regionalization of their embryonic gut, characterised by the expression of barx1 and sox2 in the prospective stomach region and expression of cdx1 and cdx2 in the prospective intestine. Furthermore, we show that gastric gland development occurs close to hatching, accompanied by the onset of gastric proton pump activity. Our findings favour a scenario in which the developmental mechanisms involved in the origin of the stomach were present in the common ancestor of chondrichthyans and osteichthyans. © 2019, The Author(s).

Funding details

Funding sponsor Funding number Acronym
Fundação Portugal Telecom
Fundação para a Ciência e a Tecnologia
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NORTE 2020
Natural Sciences and Engineering Research Council of Canada
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Fundação para a Ciência e a Tecnologia
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SFRH/ BD/79821/ 2011,IF/00146/2013
Fundação para a Ciência e a Tecnologia
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UID/Multi/04423/2013
Norte-01-0145-FEDER-000036
European Regional Development Fund
POCI-01-0145-FEDER-030562
  • 1

    We acknowledge Fundação para a Ciência e a Tecnologia for the support to OG (SFRH/ BD/79821/ 2011) and RF (IF/00146/2013). JMW was supported by grants from NSERC and the Canadian Foundation for Innovation. This work was funded by Coral—Sustainable Ocean Exploitation (Norte-01-0145-FEDER-000036), a project supported by the North Portugal Regional Operational Program (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF) and by the European Regional Development Fund (ERDF) through the COMPETE - Operational Competitiveness Programme and POPH - Operational Human Potential Programme and national funds through FCT–Foundation for Science and Technology (UID/Multi/04423/2013). The work was also partially funded by FEDER funds through the COMPETE 2020 Programme and National Funds through FCT - Portuguese Foundation for Science and Technology under the project number POCI-01-0145-FEDER-030562. We also would like to thank the technicians of the Facility of Aquatic Organisms at Ciimar and to A. Águas and F. Barroso, who contributed to the execution of the experiments.

  • ISSN: 20452322
  • Source Type: Journal
  • Original language: English
  • DOI: 10.1038/s41598-018-36413-0
  • PubMed ID: 30679499
  • Document Type: Article
  • Publisher: Nature Publishing Group

  Castro, L.F.C.; CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, Univ. Porto, Porto, Portugal;
© Copyright 2019 Elsevier B.V., All rights reserved.

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