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Early gastrula stage. (A) Several epithelial sheet fragments (esf) are colored artificially in green, magenta, and cyan. Outer cell with constricted apex is colored in yellow (red arrow). Non‐epithelized cells are colored in red. The white line shows the flat region of the embryonic surface, magenta lines—curved regions. (B) Nuclei (in blue) are shifted to the apical domain of esf cells. Cells are highlighted in magenta. (C) Outer cell with constricted apex is in yellow. (D) Septate junction (red arrow, sj) in the sub‐apical region of outer cells. (E) The apical domain of the esf cell. cg, cortical granule; yg, yolk granule. (F) esf forming a “rosette” (magenta). Yellow arrowhead points to the border between magenta and green esfs. Arrow shows the bending of the forming esf. (G) Yellow arrowhead points to the border between merged esfs (magenta). Non‐epithelized cells are in red. (H) Adjacent surfaces of inner cells. flpd, filopodia. (I, i′) Several esf are colored artificially. Yellow arrowhead points to the border between merging esfs. Arrow points to cell protrusion. (J‐L) Stages of the formation of cell protrusions (arrows). le, leading edge. CLM: (A, F). Transmission electron microscopy: (B‐E, G, H). Scanning electron microscopy: (I‐L)
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Background
In almost all metazoans examined to this respect, the axial patterning system based on canonical Wnt (cWnt) signaling operates throughout the course of development. In most metazoans, gastrulation is polar, and embryos develop morphological landmarks of axial polarity, such as blastopore under control/regulation from cWnt signaling. Howe...
Citations
... This mode of development has been observed in Parerythropodium fulvum fulvum (Benayahu and Loya, 1983), Xenia macrospiculata (Benayahu and Loya, 1984), X. umbellulata (Benayahu et al., 1988), Anthelia glauca (Kruger et al., 1998), and P. guerneyi (Chia and Crawford, 1977). Representatives of the class Hydrozoa gastrulate in the same way, when developing under the protection of the mother colony (Hydractinia echinata, Kraus et al., 2014) or inside a reduced medusa attached to the colony (Fig. 12b) (Gonothyraea loveni, Burmistrova et al., 2021;Dynamena pumila, Kraus, 2006;Vetrova et al., 2022). These hydrozoan embryos acquire cilia and begin to move at a later stage than embryos developing in the water column (e.g. ...
... The planula body can be divided into oral and aboral regions, which differ in structure and cellular composition. The endoderm consists of columnar cells in the oral region and highly vacuolated cells in the aboral region (Wulfert, 1902;Burmistrova et al., 2018;Vetrova et al., 2022). The aboral ectoderm contains a large number of glandular cells, including mucus secreting cells (Martin and Thomas, 1980;Sommer, 1990;Piraino et al., 2011). ...
... The pattern of i-cell localization is another feature that reflects the regionalization of the planula body. It has been shown that i-cells are located in the endoderm of the central part of the planula body (Martin, Archer, 1997;Vetrova et al., 2022). This is the region where the most active proliferation of endodermal cells takes place (Kroiher et al., 1990;Vetrova et al., 2022). ...
The review highlights the enormous diversity of cnidarian larvae, which is still underestimated, and infers the relationship between the evolution of life cycles, reproductive patterns, and larval forms in various phylogenetic groups of cnidarians.
... The molecular players underlying axis specification and symmetry breaking, as well as directional asymmetry of the cormidia in some species, have yet to be investigated in siphonophores. Recent work on other hydrozoan species, notably Clytia hemisphaerica (Momose and Houliston 2007;Momose et al. 2008), Dynamena pumila (Vetrova et al. 2022), Hydractinia echinata (Duffy et al. 2010;Kraus et al. 2014), or on the anthozoan sea anemone Nematostella vectensis (e.g., Lebedeva et al. 2021), all showed that the Wnt-βcatenin signaling pathway plays a major and evolutionarily conserved role in setting up the oral-aboral axis during embryogenesis. Activation of this pathway at the animal pole of early cleaving Clytia embryos through deposition of Wnt ligand and receptors on the animal and vegetal sides of the egg leads to the activation of a set of transcription factors and signaling molecules setting up the oral pole (Momose and Houliston 2007;Momose et al. 2008). ...
Synopsis
Siphonophores are colonial hydrozoans, characterized by complex colony organization and unparalleled zooid functional specialization. Recent genomic studies have offered an evolutionary perspective on how this morphological complexity arose, but a molecular characterization of symmetry breaking in siphonophore embryonic development is still largely missing. Here, bringing together historical data on early development with new immunohistochemical data, we review the diversity of developmental trajectories that lead to the formation of bilaterally symmetric planula larvae in siphonophores. Embryonic development, up to the planula stage, is remarkably similar across siphonophore phylogeny. Then, with the appearance of the lateral endodermal thickening (= ventral endoderm), larval development diverges between taxa, differing in the location and patterning of the primary buds, chronology of budding, establishment of growth zones, and retention of larval zooids. Our work also uncovers a number of open questions in siphonophore development, including homology of different zooids, mechanisms underlying formation and maintenance of spatially restricted growth zone(s), and molecular factors establishing a secondary dorsal-ventral axis in planulae. By discussing siphonophore development and body axes within the broader cnidarian context, we then set the framework for future work on siphonophores, which is finally achievable with the advent of culturing methods.
... The last indentation tends to be located in the oral domain of the embryo. However, this last indentation is not homologous to a blastopore 39 . At the end of gastrulation, in situ hybridization revealed expression of DpBra1 in a unitary broad domain (Fig. 3a) which did not overlap with any specific region within the gastrula stage embryo. ...
... Azakenpaullone (Azk) activates cWnt signaling and iCRT14 inhibits it [42][43][44] . It was shown in a previous study that hyper-activation of cWnt signaling results in the enlargement of larval oral domain, while its inhibition leads to reduction of oral domain in D. pumila 39 . ...
... 3a, 4a, 5a). In contrast to the cnidarian species with polar gastrulation 12 , it is unlikely, that Brachyury genes provide demarcation of ecto-endoderm boundary in D. pumila, since germ layers specification is not associated with axial polarity and oral region in particular during gastrulation in this species 39 . ...
Brachyury, a member of T-box gene family, is widely known for its major role in mesoderm specification in bilaterians. It is also present in non-bilaterian metazoans, such as cnidarians, where it acts as a component of an axial patterning system. In this study, we present a phylogenetic analysis of Brachyury genes within phylum Cnidaria, investigate differential expression and address a functional framework of Brachyury paralogs in hydrozoan Dynamena pumila. Our analysis indicates two duplication events of Brachyury within the cnidarian lineage. The first duplication likely appeared in the medusozoan ancestor, resulting in two copies in medusozoans, while the second duplication arose in the hydrozoan ancestor, resulting in three copies in hydrozoans. Brachyury1 and 2 display a conservative expression pattern marking the oral pole of the body axis in D. pumila. On the contrary, Brachyury3 expression was detected in scattered presumably nerve cells of the D. pumila larva. Pharmacological modulations indicated that Brachyury3 is not under regulation of cWnt signaling in contrast to the other two Brachyury genes. Divergence in expression patterns and regulation suggest neofunctionalization of Brachyury3 in hydrozoans.
... The in situ hybridization protocol was adapted from Vetrova et al. (2022). Samples were fixed with 4% paraformaldehyde in FSW overnight at +4°C, rinsed with PBS, and stored at -20°C in 100% methanol until hybridization. ...
Hydrozoan cnidarians are widely known for a diversity of life cycles. While some hydrozoan polyps produce medusae, in most species the gonophore remains attached to the polyp. Little is known about the mechanisms behind the loss of the medusal stage in hydrozoans. Hydrozoan Sarsia lovenii is a promising model for studying this issue. It is a polymorphic species with several haplogroups. One haplogroup produces attached eumedusoids and the other one buds free-swimming medusae. Here, we compared patterns of cell proliferation and distribution of nematocytes in medusoids, medusa buds and medusae of S. lovenii .
Cell proliferation is absent from exumbrella of late medusa buds and medusae, but presumably i-cells proliferate in exumbrella of medusoids. In exumbrella of medusoids, we also observed evenly distributed nematocytes with capsules and expression of late nematogenesis-associated gene, Nowa . Nematocyte capsules and Nowa expression were also observed in exumbrella of medusa bud, but we did not detect prominent Nowa signal in the bell of developed medusa. It is also known that abundance of exumbrellar nematocysts signs immaturity in medusae of Sarsia genus. Our data demonstrate that nematocyte distribution and associated gene expression in medusoids resemble medusa buds rather than developed medusae. Thus, sexually mature medusoids exhibit juvenile somatic characters, demonstrating signs of neoteny.
Research highlights
Hydrozoan Sarsia lovenii has attached eumedusoids and free-swimming medusae. The distribution of nematocytes in eumedusoids resembles that in medusa buds. This may indicate neoteny of eumedusoids.
... Some species gastrulate by invagination, unipolar ingression or epiboly, while others have multipolar modes of gastrulation such as cellular, morular or mixed delamination or multipolar ingression (33). In case of multipolar gastrulation, germ layer specification and gastrulation movements are spatially uncoupled from the universally cWnt-dependent O-A patterning (21,(34)(35)(36)(37). Importantly, in cnidarians with a unipolar . ...
Endomesoderm specification based on a maternal β-catenin signal and axial patterning by interpreting a gradient of zygotic Wnt/β-catenin signalling was suggested to predate the split between Bilateria and their evolutionary sister Cnidaria. However, in Cnidaria, the roles of β-catenin signalling in both these processes have not been proven directly. Here, by tagging the endogenous β-catenin protein in the sea anemone Nematostella vectensis , we show that the oral-aboral axis in a cnidarian is indeed patterned by a gradient of β-catenin signalling. Unexpectedly, in a striking contrast to Bilateria, Nematostella endoderm specification takes place opposite to the part of the embryo, where β-catenin is translocated into the nuclei. This suggests that β-catenin-dependent endomesoderm specification is a Bilateria-specific co-option, which may have linked endomesoderm specification with the subsequent posterior-anterior patterning.
... Hydrozoans can have different modes of gastrula tion; however, even in the case of apolar mode character ized by the absence of morphological polarity of embryos [70], the pattern of the oral-aboral axis is formed in the gastrula due to the Wnt signaling gradient [46]. At the same time, morphogenic processes during gastrulation and cell specialization in some hydrozoans are independent of the molecular axis mediated by Wnt signaling [76,77]. An elongated shape of the planula of hydroid jellyfish Clytia is formed during gastrulation and is determined by the Wnt/PCP cascade [78]. ...
A unique set of features and characteristics of species of the Cnidaria phylum is the one reason that makes them a model for a various studies. The plasticity of a life cycle and the processes of cell differentiation and development of an integral multicellular organism associated with it are of a specific scientific interest. A new stage of development of molecular genetic methods, including methods for high-throughput genome, transcriptome, and epigenome sequencing, both at the level of the whole organism and at the level of individual cells, makes it possible to obtain a detailed picture of the development of these animals. This review examines some modern approaches and advances in the reconstruction of the processes of ontogenesis of cnidarians by studying the regulatory signal transduction pathways and their interactions.
Background
The avian node is the equivalent of the amphibian Spemann's organizer, as indicated by its ability to induce a secondary axis, cellular contribution, and gene expression, whereas the node of the mouse, which displays limited inductive capacities, was suggested to be a part of spatially distributed signaling. Furthermore, the structural identity of the mouse node is subject of controversy, while little is known about equivalent structures in other mammals.
Results
We analyzed the node and emerging organizer in the pig using morphology and the expression of selected organizer genes prior to and during gastrulation. The node was defined according to the “four‐quarter model” based on comparative consideration. The node of the pig displays a multilayered, dense structure that includes columnar epithelium, bottle‐like cells in the dorsal part, and mesenchymal cells ventrally. Expression of goosecoid (gsc), chordin, and brachyury, together with morphology, reveal the consecutive emergence of three distinct domains: the gastrulation precursor domain, the presumptive node, and the mature node. Additionally, gsc displays a ventral expression domain prior to epiblast epithelialization.
Conclusion
Our study defines the morphological and molecular context of the emerging organizer equivalent in the pig and suggests a sequential development of its function.
Epithelia are the first organized tissues that appear during development. In many animal embryos, early divisions give rise to a polarized monolayer, the primary epithelium, rather than a random aggregate of cells. Here, we review the mechanisms by which cells organize into primary epithelia in various developmental contexts. We discuss how cells acquire polarity while undergoing early divisions. We describe cases where oriented divisions constrain cell arrangement to monolayers including organization on top of yolk surfaces. We finally discuss how epithelia emerge in embryos from animals that branched early during evolution and provide examples of epithelia‐like arrangements encountered in single‐celled eukaryotes. Although divergent and context‐dependent mechanisms give rise to primary epithelia, here we trace the unifying principles underlying their formation.
Brachyury, a member of T-box gene family, is widely known for its major role in mesoderm specification in bilaterians. It is also present in non-bilaterian metazoans, such as cnidarians, where it acts as a component of an axial patterning system. In this study, we present a phylogenetic analysis of Brachyury genes within phylum Cnidaria, investigate differential expression and address a functional framework of Brachyury paralogs in hydrozoan Dynamena pumila. Our analysis indicates two duplication events of Brachyury in the cnidarian lineage: in the common ancestor of the Medusozoa clade and at the base of the class Hydrozoa. We designate result of the first step as Brachyury2 and of the second as Brachyury3.
Brachyury1 and 2 display a conservative expression pattern marking the oral pole of the body axis in D. pumila. On the contrary, Brachyury3 expression was detected in scattered presumably nerve cells of the D. pumila larva. Pharmacological modulations indicated that Brachyury3 is not under regulation of cWnt signalling in contrast to the other two Brachyury genes. Divergence in expression patterns and regulation suggest neofunctionalization of Brachyury3 in hydrozoans.
