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. However, in many cnidarian species, gastrulation is morphologically apolar. The question remains whether сWnt signaling providing the establishment of a body axis controls morphogenetic processes involved in apolar gastrulation. Results In this study, we focused on the embryonic development of Dynamena pumila, a cnidarian species with apolar gastrulation. We thoroughly described cell behavior, proliferation, and ultrastructure and examined axial patterning in the embryos of this species. We revealed that the first signs of morphological polarity appear only after the end of gastrulation, while molecular prepatterning of the embryo does exist during gastrulation. We have shown experimentally that in D. pumila, the direction of the oral‐aboral axis is highly robust against perturbations in cWnt activity. Conclusions Our results suggest that morphogenetic processes are uncoupled from molecular axial patterning during gastrulation in D. pumila. Investigation of D. pumila might significantly expand our understanding of the ways in which morphological polarization and axial molecular patterning are linked in Metazoa.
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 Wnt signaling. However, in many cnidarian species, gastrulation is morphologically apolar. The question remains whether cWnt signaling providing the establishment of a body axis controls morphogenetic processes involved in apolar gastrulation. Results: In this study, we focused on the embryonic development of Dynamena pumila, a cnidarian species with apolar gastrulation. We thoroughly described cell behavior, proliferation, and ultrastructure and examined axial patterning in the embryos of this species. We revealed that the first signs of morphological polarity appear only after the end of gastrulation, while molecular prepatterning of the embryo does exist during gastrulation. We have shown experimentally that in D. pumila, the morphological axis is highly robust against perturbations in cWnt activity. Conclusion: Our results suggest that morphogenetic processes are uncoupled from molecular axial patterning during gastrulation in D. pumila. Investigation of D. pumila might significantly expand our understanding of the ways in which morphological polarization and axial molecular patterning are linked in Metazoa.
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.
Hydrozoans are widely known for their complex life cycles. The life cycle usually includes an asexual benthic polyp, which produces a sexual zooid (gonophore). Here, we performed an extensive analysis of 183 specimens of hydrozoan genus Sarsia from the White Sea and identified four types of gonophores. We also compared the type of gonophore with haplotypes of molecular markers COI and ITS. Analysis of COI sequences recovered that the studied specimens relate to the species S. tubulosa, S. princeps and S. lovenii, and that S. lovenii specimens divide into two COI-haplogroups. More intraspecies genetic diversity was revealed in the analysis of ITS sequences. Sarsia tubulosa specimens divide into two ITS-haplotypes, and presumably, hybrid forms between these lineages were found. For S. lovenii, we identified 14 ITS-haplotypes as a result of alleles separation. Intra-individual genetic polymorphism of ITS-region is most likely associated with intraspecific hybridization between different haplotypes. The diversity of morphotypes is associated with the genetic diversity of the specimens. Thus, we demonstrated that the morphologically variable species S. lovenii is represented in the White Sea by a network of intensively hybridizing haplotypes. Hybridization affects the morphology and maturation period of gonophores and presumably affects the processes of speciation.
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.
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.
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