title: Spatiotemporal transcriptomics reveals the evolutionary history of the endoderm germ layer.
abstract: The concept of germ layers has been one of the foremost organizing principles in developmental biology, classification, systematics and evolution for 150 years (refs 1 - 3). Of the three germ layers, the mesoderm is found in bilaterian animals but is absent in species in the phyla Cnidaria and Ctenophora, which has been taken as evidence that the mesoderm was the final germ layer to evolve. The origin of the ectoderm and endoderm germ layers, however, remains unclear, with models supporting the antecedence of each as well as a simultaneous origin. Here we determine the temporal and spatial components of gene expression spanning embryonic development for all Caenorhabditis elegans genes and use it to determine the evolutionary ages of the germ layers. The gene expression program of the mesoderm is induced after those of the ectoderm and endoderm, thus making it the last germ layer both to evolve and to develop. Strikingly, the C. elegans endoderm and ectoderm expression programs do not co-induce; rather the endoderm activates earlier, and this is also observed in the expression of endoderm orthologues during the embryology of the frog Xenopus tropicalis, the sea anemone Nematostella vectensis and the sponge Amphimedon queenslandica. Querying the phylogenetic ages of specifically expressed genes reveals that the endoderm comprises older genes. Taken together, we propose that the endoderm program dates back to the origin of multicellularity, whereas the ectoderm originated as a secondary germ layer freed from ancestral feeding functions.
authors.affiliation: Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel.
authors.forename: Tamar
authors.initials: T
authors.lastname: Hashimshony
authors.affiliation: Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel.
authors.forename: Martin
authors.initials: M
authors.lastname: Feder
authors.affiliation: Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel.
authors.forename: Michal
authors.initials: M
authors.lastname: Levin
authors.affiliation: Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4JI, Canada.
authors.forename: Brian K
authors.initials: BK
authors.lastname: Hall
authors.affiliation: Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel.
authors.forename: Itai
authors.initials: I
authors.lastname: Yanai
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology / Q000196:embryology* / Q000235:genetics*; D019070:Cell Lineage; D004435:Eating; D004475:Ectoderm / Q000166:cytology / Q000196:embryology / Q000378:metabolism; D004707:Endoderm / Q000166:cytology / Q000196:embryology / Q000378:metabolism*; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental / Q000235:genetics*; D008648:Mesoderm / Q000166:cytology / Q000196:embryology / Q000378:metabolism; D008954:Models, Biological; D011161:Porifera / Q000166:cytology / Q000196:embryology / Q000235:genetics; D012615:Sea Anemones / Q000166:cytology / Q000196:embryology / Q000235:genetics; D062211:Spatio-Temporal Analysis; D013997:Time Factors; D059467:Transcriptome / Q000235:genetics*; D014981:Xenopus / Q000196:embryology / Q000235:genetics