Embryonic development of the moon jellyfish Aurelia aurita (Cnidaria, Scyphozoa): another variant on the theme of invagination

Abstract

Background Aurelia aurita (Scyphozoa, Cnidaria) is an emblematic species of the jellyfish. Currently, it is an emerging model of Evo-Devo for studying evolution and molecular regulation of metazoans’ complex life cycle, early development, and cell differentiation. For Aurelia, the genome was sequenced, the molecular cascades involved in the life cycle transitions were characterized, and embryogenesis was studied on the level of gross morphology. As a reliable representative of the class Scyphozoa, Aurelia can be used for comparative analysis of embryonic development within Cnidaria and between Cnidaria and Bilateria. One of the intriguing questions that can be posed is whether the invagination occurring during gastrulation of different cnidarians relies on the same cellular mechanisms. To answer this question, a detailed study of the cellular mechanisms underlying the early development of Aurelia is required. Methods We studied the embryogenesis of A. aurita using the modern methods of light microscopy, immunocytochemistry, confocal laser microscopy, scanning and transmission electron microscopy. Results In this article, we report a comprehensive study of the early development of A. aurita from the White Sea population. We described in detail the embryonic development of A. aurita from early cleavage up to the planula larva. We focused mainly on the cell morphogenetic movements underlying gastrulation. The dynamics of cell shape changes and cell behavior during invagination of the archenteron (future endoderm) were characterized. That allowed comparing the gastrulation by invagination in two cnidarian species—scyphozoan A. aurita and anthozoan Nematostella vectensis. We described the successive stages of blastopore closure and found that segregation of the germ layers in A. aurita is linked to the ’healing’ of the blastopore lip. We followed the developmental origin of the planula body parts and characterized the planula cells’ ultrastructure. We also found that the planula endoderm consists of three morphologically distinct compartments along the oral-aboral axis. Conclusions Epithelial invagination is a fundamental morphogenetic movement that is believed as highly conserved across metazoans. Our data on the cell shaping and behaviours driving invagination in A. aurita contribute to understanding of morphologically similar morphogenesis in different animals. By comparative analysis, we clearly show that invagination may differ at the cellular level between cnidarian species belonging to different classes (Anthozoa and Scyphozoa). The number of cells involved in invagination, the dynamics of the shape of the archenteron cells, the stage of epithelial-mesenchymal transition that these cells can reach, and the fate of blastopore lip cells may vary greatly between species. These results help to gain insight into the evolution of morphogenesis within the Cnidaria and within Metazoa in general.