A blastoporal organizer in a ctenophore

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The concepts of the embryonic organizer and induction were introduced and developed by Hilde Mangold and Hans Spemann based on their landmark experiments in the 1920s 1 , 6 . Their studies on transplantation of the dorsal blastopore lip of amphibian embryos demonstrated that this tissue has the capacity to induce the formation of a secondary body axis by recruiting neighbouring host cells (Fig. 1a ). The secondary axis is formed through interactions between the transplanted cells and the host embryo tissues, and the data highlighted the critical role of the organizer in directing host tissue differentiation and morphogenesis. This experiment provided clear evidence that specific cell populations in embryos can influence the differentiation of neighbouring cells. Subsequent comparative evolutionary studies revealed the presence of an embryonic organizer in a non-bilaterian animal, the cnidarian N. vectensis 2 , 3 . Transplanting a section of the blastopore lip from an early gastrula of N. vectensis to another embryo at the same stage of development results in the induction of a secondary oral–aboral axis (Fig. 1b ). The central role of WNT–β-catenin signalling in driving the organizing activity of cnidarian and vertebrate blastopore lips suggest the potential homology of these structures. Despite extensive research on the embryonic organizer in bilaterians, particularly chordates (the zebrafish Danio rerio and the frog Xenopus laevis ) 7 , 8 , and their sister group cnidarians ( N. vectensis ) 2 , 3 , the evolutionary history of the embryonic organizer remains unsolved. It is still unclear whether embryonic organizers exist in other non-bilaterian animals predating the cnidaria–bilaterian separation, like sponges (Porifera) and comb jellies (Ctenophora) (Fig. 1c ). Ctenophores are of particular interest because they are considered to occupy a key phylogenetic position as a sister group to all other multicellular animals 4 , 5 . A ctenophore embryonic organizer, if homologous to those in cnidarians and bilaterians, would suggest that an organizer emerged alongside the advent of multicellularity.

Fig. 1: Embryonic organizers in different metazoan groups. The alternative text for this image may have been generated using AI.

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a , b , Schematics of embryonic organizer transplantation in amphibians ( a ) and cnidarians (anthozoans) ( b ). In both cases, transplantation of the blastopore lip fragment from one embryo to another induces a secondary axis involving host tissue. c , Presence of an embryonic organizer in different metazoan groups. The embryonic organizer has so far been described and studied only in bilaterians and their sister group cnidarians. However, it remains unknown whether an embryonic organizer exists in Porifera or Ctenophora; therefore, it is unclear when the embryonic organizer emerged in animal evolution. d , Cydippid stage of M. leidyi (Ctenophora). Scale bar, 2.5 mm. e , M. leidyi embryo at the gastrula stage. Cells surrounding the blastopore are highlighted yellow. Scale bar, 20 μm. Images in d and e are representative images from normal wild-type M. leidyi at the indicated developmental stages. Such normal morphology was consistently observed in all examined specimens. Asterisks ( a , b , e ) indicate the blastopore. A, aboral; cr, comb row; m, mouth; O, oral; PH, pharyngeal axis; t, tentacle; TA, tentacular axis; tb, tentacle bud.

Ctenophore blastopore lip is an organizer

To analyse the inductive capacity of different parts of the M. leidyi gastrula embryo, we transplanted blastopore lip tissue and lateral ectoderm to host embryos of the same stage of development (Fig. 2a and Extended Data Fig. 1 ). In our experiments, 41.8% (28 out of 67) of blastopore lip transplantations resulted in the formation of a complete secondary pharynx with a mouth opening (Fig. 2b ). Moreover, 14.9% (10 out of 67) of embryos formed a mouth-like structure without a developed pharynx (Fig. 2c ), and 43.3% (29 out of 67) developed normally (Fig. 2d ). We did not observe duplication of any other anatomical structures. By contrast, embryos that received lateral ectoderm grafts ( n  = 49) never formed secondary pharynxes or mouth openings. Similarly, after control incisions without grafting ( n  = 63), we did not observe the formation of any additional structures (Fig. 2e–h ). In cases when the ectopic pharynx was fully developed, the primary and secondary induced pharynxes fused together before connecting to the ‘stomach’ (infundibulum) and merging into a single digestive system (Fig. 2i,j ). Both the primary and the ectopically induced mouths were fully functional and capable of capturing food, such as rotifers, and delivering it into the shared gastrovascular system (Fig. 2k ).

Fig. 2: Organizer activity of the blastopore lip of a M. leidyi gastrula. The alternative text for this image may have been generated using AI.

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a , Schematic of the grafting experiment: transplanta…