A blastoporal organizer in a ctenophore

In an iconic experiment in 1924, Hilde Mangold and Hans Spemann established that the dorsal blastopore lip of amphibian embryos functions as an organizer and induces a secondary body axis when transplanted into a host embryo1. This discovery demonstrated that specific embryonic regions can regulate embryonic patterning and lead to the establishment of an entire body axis. Subsequent studies have revealed that cnidarians, the sister group to Bilateria, also possess a blastoporal embryonic organizer2,3. However, the evolutionary origin of the organizer remains unclear. Here we report that the blastopore lip of the ctenophore Mnemiopsis leidyi, a member of the evolutionary sister group to all other metazoans4,5, exhibits organizer activity. We show that transplanted fragments of blastopore lip tissue from M. leidyi gastrula induce secondary pharynx and mouth formation. Moreover, transphyletic transplantation experiments show that the blastopore lip of M. leidyi leads to the generation of a secondary body axis in embryos of the cnidarian Nematostella vectensis. Organizer function in M. leidyi requires both β-catenin and TGFβ signalling, and the TGFβ-family ligands probably provide this inductive capacity. These findings reveal the deep homology of the blastoporal organizer in ctenophores, cnidarians and vertebrates, implying the ancestral organizer role of the blastopore lip. We propose that the emergence of the organizer was an essential innovation that facilitated the change from the temporal cell differentiation of unicellular relatives to the spatial cell differentiation of the first multicellular embryo. Experiments using the comb jelly Mnemiopsis leidyi and the sea anemone Nematostella vectensis reveal that the emergence of a core signalling pathway may have been a key innovation enabling the transition to multicellularity in animals.