Yulia Kraus

Pre-bilaterian origin of the blastoporal axial organizer

The startling capacity of the amphibian Spemann organizer to induce naïve cells to form a Siamese twin embryo with a second set of body axes is one of the hallmarks of developmental biology. However, the axis-inducing potential of the blastopore-associated tissue is commonly regarded as a chordate feature. Here we show that the blastopore lip of a non-bilaterian metazoan, the anthozoan cnidarian Nematostella vectensis, possesses the same capacity and uses the same molecular mechanism for inducing extra axes as chordates: Wnt/β-catenin signaling. We also demonstrate that the establishment of the secondary, directive axis in Nematostella by BMP signaling is sensitive to an initial Wnt signal, but once established the directive axis becomes Wnt-independent. By combining molecular analysis with experimental embryology, we provide evidence that the emergence of the Wnt/β-catenin driven blastopore-associated axial organizer predated the cnidarian-bilaterian split over 600 million years ago.

A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development

Functional and morphological planar cell polarity (PCP) oriented along the oral-aboral body axis is clearly evident in the ectoderm of torpedo-shaped planula larvae of hydrozoan cnidarians such as Clytia hemisphaerica. Ectodermal epithelial cells bear a single motile cilium the beating of which is coordinated between cells, causing directional swimming towards the blunt, aboral pole. We have characterised PCP during Clytia larval development and addressed its molecular basis. PCP is first detectable in ectodermal cells during gastrulation as coordinated basal body positioning, the ciliary root becoming consistently positioned on the oral side of the apical surface of the cell. At later stages, more pronounced structural polarity develops around the base of each cilium in relation to the cilia beating direction, including a characteristic asymmetric cortical actin organisation. Morpholino antisense oligonucleotide and mRNA injection studies showed that PCP development requires the Clytia orthologues of the core Fz-PCP pathway components Strabismus (CheStbm), Frizzled (CheFz1) and Dishevelled (CheDsh). Morpholinos targeting any of these components prevented ectodermal PCP, disrupted ciliogenesis and inhibited embryo elongation during gastrulation, which involves cell intercalation. We show that YFP-tagged CheStbm adopts a polarised intracellular distribution, localising preferentially to the aboral boundary of each cell, as has been demonstrated in Drosophila and some vertebrate PCP studies. Our findings in a cnidarian strongly suggest that the Fz-PCP pathway is a highly conserved and evolutionary ancient metazoan feature that is probably widely responsible for oriented swimming and/or feeding in relation to body axis in the many ciliated larval types found throughout the animal kingdom.

Organizer regions in marine colonial hydrozoans

Organizers are specific tissue regions of developing organisms that provide accuracy and robustness to the body plan formation. Hydrozoan cnidarians (both solitary and colonial) require organizer regions for maintaining the regular body patterning during continuous tissue dynamics during asexual reproduction and growth. While the hypostomal organizer of the solitary Hydra has been studied relatively well, our knowledge of organizers in colonial hydrozoans remains fragmentary and incomplete. As colonial hydrozoans demonstrate an amazing diversity of morphological and life history traits, it is of special interest to investigate the organizers specific for particular ontogenetic stages and particular types of colonies. In the present study we aimed to assess the inductive capacities of several candidate organizer regions in hydroids with different colony organization. We carried out grafting experiments on colonial hydrozoans belonging to Leptothecata and Anthoathecata. We confirmed that the hypostome tip is an organizer in the colonial Anthoathecata as it is in the solitary polyp Hydra. We also found that the posterior tip of the larva is an organizer in hydroids regardless of the peculiarities of their metamorphosis mode and colony structure. We show for the first time that the shoot growing tip, which can be considered a key evolutionary novelty of Leptothecata, is an organizer region. Taken together, our data demonstrate that organizers function throughout the larval and polypoid stages in colonial hydroids.

The embryonic development of the cnidarian Hydractinia echinata

With the rapid increase of the quantity of molecular data, many animals joined the ranks of the so‐called ‘emerging models’ of Evo‐Devo. One of the necessary steps in converting an emerging model into an established one is gaining comprehensive knowledge of its normal embryonic development. The marine colonial hydrozoan Hydractinia echinata – an excellent model for research on stem cells, metamorphosis, and allorecognition – has been studied for decades. Yet knowledge of its embryonic development remains fragmentary and incomplete. Here we provide a detailed account of H. echinata embryonic development using in vivo observations, histology, immunohistochemistry, and electron microscopy. Furthermore, we propose a model describing the cellular basis of the morphogenetic movements occurring during development and also reveal a functional link between canonical Wnt signaling and regional differences in the morphology of the embryo. Hydractinia embryogenesis is an example of the diversity and plasticity of hydrozoan development where multiple routes lead to the same result – the formation of a normal planula larva.

Germ-layer commitment and axis formation in sea anemone embryonic cell aggregates

Significance Embryonic development of any animal species is a robust series of morphogenetic events tightly controlled by molecular signals. However, the variety of developmental trajectories undertaken by different members of the same phylum suggests that normal development in each particular species might involve only a subset of morphogenetic capacities available to the highly developmentally plastic embryonic cells. Here we show that, faced by a new developmental context, the aggregates of dissociated gastrula cells of the sea anemone Nematostella vectensis use an alternative developmental trajectory typical for other, distantly related members of the cnidarian phylum. We conclude that new modes of development may evolve relatively easily due to the versatility and developmental plasticity of embryonic cells. Robust morphogenetic events are pivotal for animal embryogenesis. However, comparison of the modes of development of different members of a phylum suggests that the spectrum of developmental trajectories accessible for a species might be far broader than can be concluded from the observation of normal development. Here, by using a combination of microsurgery and transgenic reporter gene expression, we show that, facing a new developmental context, the aggregates of dissociated embryonic cells of the sea anemone Nematostella vectensis take an alternative developmental trajectory. The self-organizing aggregates rely on Wnt signals produced by the cells of the original blastopore lip organizer to form body axes but employ morphogenetic events typical for normal development of distantly related cnidarians to re-establish the germ layers. The reaggregated cells show enormous plasticity including the capacity of the ectodermal cells to convert into endoderm. Our results suggest that new developmental trajectories may evolve relatively easily when highly plastic embryonic cells face new constraints.

Embryonic development of thecate hydrozoan Gonothyraea loveni (Allman, 1859)

Progress of Evo‐Devo requires broad phylogenetic sampling providing the data for comparative analysis as well as new objects suitable for experimental investigation. Representatives of the early‐branching animal phylum Cnidaria and particularly hydrozoans draw great attention due to the high diversity of embryonic and post‐embryonic development and life‐cycles in general. Most detailed studies on embryonic development in hydrozoans were performed on the species shedding their gametes with subsequent embryo development in the water column. Widely distributed thecate hydrozoan Gonothyraea loveni broods its embryos within reduced medusae attached to the colony until development of a free‐swimming metamorphosis competent planula‐larva. In the current essay we present a detailed description of G. loveni embryonic development based on in vivo observations, histology, immuno‐cytochemistry, and electron microscopy. Starting from early cleavage, the embryo becomes a morula without any sign of blastocoele. Gastrulation proceeds as mixed delamination and ends with parenchymula formation. The first morphological sign of primary body axis appears only in the beginning of parenchymula‐preplanula transition. In mature metamorphosis competent planula only the cells of the oral two‐thirds of endoderm retain proliferative activity resulting in accumulation of great number of i‐cells and nematoblasts, which can be used during metamorphosis accompanied with essential reorganization of larval tissues. G. loveni demonstrates the diversity as well as evolutionary plasticity of hydrozoans development: in brooding hydrozoans embryonic and larval development is highly embryonized in comparison with the spawning species with free‐swimming embryos.