Gut-like ectodermal tissue in a sea anemone challenges germ layer homology

Abstract

Cnidarians (for example, sea anemones and jellyfish) develop from an outer ectodermal and inner endodermal germ layer, whereas bilaterians (for example, vertebrates and flies) additionally have a mesodermal layer as intermediate germ layer. Currently, cnidarian endoderm (that is, ‘mesendoderm’) is considered homologous to both bilaterian endoderm and mesoderm. Here we test this hypothesis by studying the fate of germ layers, the localization of gut cell types, and the expression of numerous ‘endodermal’ and ‘mesodermal’ transcription factor orthologues in the anthozoan sea anemone Nematostella vectensis. Surprisingly, we find that the developing pharyngeal ectoderm and its derivatives display a transcription-factor expression profile (foxA, hhex, islet, soxB1, hlxB9, tbx2/3, nkx6 and nkx2.2) and cell-type combination (exocrine and insulinergic) reminiscent of the developing bilaterian midgut, and, in particular, vertebrate pancreatic tissue. Endodermal derivatives, instead, display cell functions and transcription-factor profiles similar to bilaterian mesoderm derivatives (for example, somatic gonad and heart). Thus, our data supports an alternative model of germ layer homologies, where cnidarian pharyngeal ectoderm corresponds to bilaterian endoderm, and the cnidarian endoderm is homologous to bilaterian mesoderm.

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Fig. 1: An ectodermal origin of the gut-like tissue of N. vectensis supports an alternative homology between cnidarian and bilaterian germ layers.
Fig. 2: Fate mapping reveals an ectodermal origin of the pharynx and septal filaments.
Fig. 3: Expression of exocrine digestive enzymes, and ‘endodermal’ or ‘pancreatic’ transcription-factor orthologues in N. vectensis and A. aurita.
Fig. 4: Storage of lipids, glucose and amino acids, and the expression of ‘mesodermal’ transcription factors in juvenile somatic gonad and muscle tissues.

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Acknowledgements

We thank M. Owusu, J. Steiner, M. Laplante, W. Wang and K. Khalturin for protocols and help with carrying out gene clonings and in situ hybridization experiments; S. I. Q. Kaul-Strehlow for confocal imaging and the Core Facility Cell Imaging of the Faculty of Life Sciences (University of Vienna) for support with confocal imaging; S. Shimeld (foxC) and F. Rentzsch (nkx2.2A, -B and -E genes) for sharing plasmids of Nematostella gene fragments, and the members of the Technau lab for discussion. This work was supported by grants from the Austrian Science Fund FWF to P.R.H.S. (P26538), U.T. (P27353 and P25993) and HFSP to A.A. (LT000809/2012-L).

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P.R.H.S. designed the study, performed most experiments and wrote the paper. A.A. designed and performed the fate mapping and transgene mapping experiments. J.E.M.K. cloned and analysed the A. aurita foxA gene, and developed an A. aurita in situ hybridization protocol. U.T. also designed the study and wrote the paper.

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Correspondence to Patrick R. H. Steinmetz or Ulrich Technau.

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Steinmetz, P.R.H., Aman, A., Kraus, J.E.M. et al. Gut-like ectodermal tissue in a sea anemone challenges germ layer homology. Nat Ecol Evol 1, 1535–1542 (2017). https://doi.org/10.1038/s41559-017-0285-5

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