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

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Abstract

Cnidarians (e.g. sea anemones, jellyfish), develop from the outer ectodermal, and the inner endodermal germ layer, while bilaterians (e.g. vertebrates, flies) additionally exhibit mesoderm as intermediate germ layer. Currently, cnidarian endoderm (i.e. ‘mesendoderm’) is considered homologous to both bilaterian endoderm and mesoderm. Here, we test this hypothesis by studying the fate of germ layer, the localisation of gut cell types, and the expression of numerous ‘endodermal’ and ‘mesodermal’ transcription factor orthologs 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, 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 (e.g. somatic gonad, 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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Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

N. H. Putnam, M Srivastava, U Hellsten … (2007)

Sea anemones are seemingly primitive animals that, along with corals, jellyfish, and hydras, constitute the oldest eumetazoan phylum, the Cnidaria. Here, we report a comparative analysis of the draft genome of an emerging cnidarian model, the starlet sea anemone Nematostella vectensis. The sea anemone genome is complex, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes, implying that the genome of the eumetazoan ancestor was similarly complex. Nearly one-fifth of the inferred genes of the ancestor are eumetazoan novelties, which are enriched for animal functions like cell signaling, adhesion, and synaptic transmission. Analysis of diverse pathways suggests that these gene "inventions" along the lineage leading to animals were likely already well integrated with preexisting eukaryotic genes in the eumetazoan progenitor.

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Vertebrate endoderm development and organ formation.

Aaron Zorn, James M. Wells (2009)

The endoderm germ layer contributes to the respiratory and gastrointestinal tracts and to all of their associated organs. Over the past decade, studies in vertebrate model organisms, including frog, fish, chick, and mouse, have greatly enhanced our understanding of the molecular basis of endoderm organ development. We review this progress with a focus on early stages of endoderm organogenesis including endoderm formation, gut tube morphogenesis and patterning, and organ specification. Lastly, we discuss how developmental mechanisms that regulate endoderm organogenesis are used to direct differentiation of embryonic stem cells into specific adult cell types, which function to alleviate disease symptoms in animal models.

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Independent evolution of striated muscles in cnidarians and bilaterians

Patrick R.H. Steinmetz, Johanna E.M. Kraus, Claire Larroux … (2012)

Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin 1, 2 . Here we show that a muscle protein core set, including a Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore, myhc-st and myhc-non-muscle (myhc-nm) orthologues are expressed differentially in two sponges, compatible with the functional diversification of myhc paralogues before the origin of true muscles and the subsequent deployment of MyHC-st in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess myhc-st orthologues but lack crucial components of bilaterian striated muscles, such as troponin complex and titin genes, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.