Like most bilaterian animals, the annelid Platynereis dumerilii generates the majority of its body axis in an anterior to posterior temporal progression with new segments added sequentially. This process relies on a posterior subterminal proliferative body region, known as the "segment addition zone" (SAZ). We explored some of the molecular and cellular aspects of posterior elongation in Platynereis, in particular to test the hypothesis that the SAZ contains a specific set of stem cells dedicated to posterior elongation. We cloned and characterized the developmental expression patterns of orthologs of 17 genes known to be involved in the formation, behavior, or maintenance of stem cells in other metazoan models. These genes encode RNA-binding proteins (e.g., tudor, musashi, pumilio) or transcription factors (e.g., myc, id, runx) widely conserved in eumetazoans. Most of these genes are expressed both in the migrating primordial germ cells and in overlapping ring-like patterns in the SAZ, similar to some previously analyzed genes (piwi, vasa). The SAZ patterns are coincident with the expression of proliferation markers cyclin B and PCNA. EdU pulse and chase experiments suggest that new segments are produced through many rounds of divisions from small populations of teloblast-like posterior stem cells. The shared molecular signature between primordial germ cells and posterior stem cells in Platynereis thus corresponds to an ancestral "stemness" program.
Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/b-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/b-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/b-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.
In animals, body axis patterning is based on the concentration-dependent interpretation of graded morphogen signals, which enables correct positioning of the anatomical structures. The most ancient axis patterning system acting across animal phyla relies on β-catenin signaling, which directs gastrulation, and patterns the main body axis. However, within Bilateria, the patterning logic varies significantly between protostomes and deuterostomes. To deduce the ancestral principles of β-catenin-dependent axial patterning, we investigate the oral–aboral axis patterning in the sea anemone Nematostella—a member of the bilaterian sister group Cnidaria. Here we elucidate the regulatory logic by which more orally expressed β-catenin targets repress more aborally expressed β-catenin targets, and progressively restrict the initially global, maternally provided aboral identity. Similar regulatory logic of β-catenin-dependent patterning in Nematostella and deuterostomes suggests a common evolutionary origin of these processes and the equivalence of the cnidarian oral–aboral and the bilaterian posterior–anterior body axes.
SignificanceEmbryonic 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.
Despite the general uniformity in cellular composition of the adult cerebellum (Cb), the expression of proteins such as ZebrinII/AldolaseC and the small heat shock protein HSP25 reveal striking patterns of parasagittal Purkinje cell (PC) stripes. Based on differences in the stripe configuration within subsets of lobules, the Cb can be further divided into four anterior-posterior transverse zones: anterior zone (AZ) = lobules I-V, central zone (CZ) = lobules VI-VII, posterior zone (PZ) = lobules VIII and anterior IX, and the nodular zone (NZ) = lobules posterior IX-X. Here we used whole-mount and tissue section immunohistochemistry to show that neurofilament heavy chain (NFH) expression alone divides all lobules of the mouse Cb into a complex series of parasagittal stripes of PCs. We revealed that the striped pattern of NFH in the vermis of the AZ and PZ was complementary to ZebrinII and phospholipase C ß3 (PLCß3), and corresponded to phospholipase C ß4 (PLCß4). In the CZ and NZ the stripe pattern of NFH was complementary to HSP25 and corresponded to PLCß3. The boundaries of the NFH stripes were not always sharply delineated. Instead, a gradual decrease in NFH expression was observed toward the edges of particular stripes, resulting in domains comprised of overlapping expression patterns. Furthermore, the terminal field distributions of mossy and climbing fibers had a complex but consistent topographical alignment with NFH stripes. In summary, NFH expression reveals an exquisite level of Cb stripe complexity that respects the transverse zone divisions and delineates an intricately patterned target field for Cb afferents.
Genes of the coe (collier/olfactory/early B-cell factor) family encode Helix-Loop-Helix transcription factors that are widely conserved in metazoans and involved in many developmental processes, neurogenesis in particular. Whereas their functions during vertebrate neural tube formation have been well documented, very little is known about their expression and role during central nervous system (CNS) development in protostomes. Here we characterized the CNS expression of coe genes in the insect Drosophila melanogaster and the polychaete annelid Platynereis dumerilii, which belong to different subgroups of protostomes and show strikingly different modes of development. In the Drosophila ventral nerve cord, we found that the Collier-expressing cells form a subpopulation of interneurons with diverse molecular identities and neurotransmitter phenotypes. We also demonstrate that collier is required for the proper differentiation of some interneurons belonging to the Eve-Lateral cluster. In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells. Using an original technique of in silico 3D registration, we show that Pdu-coe is co-expressed with many different neuronal markers and therefore that, like in Drosophila, its expression defines a heterogeneous population of neurons with diverse molecular identities. Our detailed characterization and comparison of coe gene expression in the CNS of two distantly-related protostomes suggest conserved roles of coe genes in neuronal differentiation in this clade. As similar roles have also been observed in vertebrates, this function was probably already established in the last common ancestor of all bilaterians.
In animals, body axis patterning is based on the concentration-dependent interpretation of graded morphogen signals, which enables correct positioning of the anatomical structures. The most ancient axis patterning system acting across animal phyla relies on β-catenin signaling, which directs gastrulation, and patterns the main body axis. However, within Bilateria, the patterning logic varies significantly between protostomes and deuterostomes. To deduce the ancestral principles of β-catenin dependent axial patterning, we investigated the oral-aboral axis patterning in the sea anemone Nematostella - a member of the bilaterian sister group Cnidaria. Here we elucidate the regulatory logic by which more orally expressed β-catenin targets repress more aborally expressed β- catenin targets, and progressively restrict the initially global, maternally provided aboral identity. Similar regulatory logic of β-catenin-dependent patterning in Nematostella and deuterostomes suggests a common evolutionary origin of these processes.
ancestral molluscs probably possessed a single shell plate as seen extant limpet. In addition, bivalves also acquired a novel structure, adducter muscle to close the separated shell plate. Because the two novel structures, the separated shell plate and the adducter muscle appear early embryonic stage, their evolution should
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