Larval development in Cnidaria: A connection to bilateria?

Gröger, Hans; Schmid, Volker

doi:10.1002/gene.1013

Cited by 65 publications

(42 citation statements)

References 25 publications

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“…BMP2͞4-Am may perform such roles in Acropora, and not be involved in axis formation. In summary, it is possible that dpp͞BMP ligands were already playing a role in axis formation in a putative common ancestor of Acropora and the Bilateria, consistent with the proposal that cnidarians either are, or were at one stage in their evolution, biradial or bilateral (3,6,9,10). Alternatively, this family of ligands may have evolved to play one of the non-axis-forming roles of DPP͞BMP2͞4 before the divergence of the Cnidaria from the rest of the Metazoa.…”

Section: Resultssupporting

confidence: 79%

Localized expression of a dpp / BMP2 / 4 ortholog in a coral embryo

Hayward

Samuel

Pontynen

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

124

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As the closest outgroup to the Bilateria, the Phylum Cnidaria is likely to be critical to understanding the origins and evolution of body axes. Proteins of the decapentaplegic (DPP)͞bone morphogenetic protein (BMP) 2͞4 subfamily are central to the specification of the dorsoventral (D͞V) axis in bilateral animals, albeit with an axis inversion between arthropods and chordates. We show that a dpp͞BMP2͞4 ortholog (bmp2͞4-Am) is present in the reef-building scleractinian coral, Acropora millepora (Class Anthozoa) and that it is capable of causing phenotypic effects in Drosophila that mimic those of the endogenous dpp gene. We also show that, during coral embryonic development, bmp2͞4-Am expression is localized in an ectodermal region adjacent to the blastopore. Thus, a representative of the DPP͞BMP2͞4 subfamily of ligands was present in the common ancestor of diploblastic and triploblastic animals where it was probably expressed in a localized fashion during development. A localized source of DPP͞BMP2͞4 may have already been used in axis formation in this ancestor, or it may have provided a means by which an axis could evolve in triploblastic animals.

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Section: Resultssupporting

confidence: 79%

Localized expression of a dpp / BMP2 / 4 ortholog in a coral embryo

Hayward

Samuel

Pontynen

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

124

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“…Indeed, studies have revealed considerable conservation of regulatory genes between the diploblastic cnidarians and chordates (Galliot andSchmid, 2002, Hayward et al, 2002), increasing the likelihood that there is overlap in the mechanisms of eye development between jellyfish and vertebrates. In addition, an investigation of the early embryogenesis of the marine hydrozoan jellyfish, Podocoryne carnea, suggested that the nervous system developed from anterior to posterior in serially repeated patterns, characteristic of bilaterally symmetrical metazoans (Groger and Schmid, 2001). Since jellyfish differ sufficiently from vertebrates, we anticipate that detailed studies of their eye development should provide new insights into whether eyes are monophyletic, convergent, or a combination of both as well as provide new information on eye development in general.…”

Section: Cubozoan Eyes With Special Reference To Tripedaliamentioning

confidence: 96%

Cubozoan jellyfish: an Evo/Devo model for eyes and other sensory systems

Piatigorsky

Kozmík²

2004

Int. J. Dev. Biol.

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Cnidaria are the most basal phylum containing a well-developed visual system located on specialized sensory structures (rhopalia) with eyes and statocyts. We have been exploring the cubozoan jellyfish, Tripedalia cystophora. In addition to containing simple photoreceptive ocelli, each rhopalium in Tridedalia has a large and small complex, camera-type eye with a cellular lens containing three distinct families of crystallins which apparently serve non-lenticular functions. Thus, Tridpedalia recruited crystallins by a gene sharing strategy as have mollusks and vertebrates. Tripedalia has a single Pax gene, PaxB, which encodes a structural and functional Pax 2/5/8-like paired domain as well as an octapeptide and Pax6-like homeodomain. PaxB binds to and activates Tripedalia crystallin promoters (especially J3-crystallin) and the Drosophila rhodopsin rh6 gene in transfection tests and induces ectopic eyes in Drosophila. In situ hybridization showed that PaxB and crystallin genes are expressed in the lens, retina and statocysts. We suggest from these results that an ancestral PaxB gene was a primordial gene in eye evolution and that eyes and ears (mechanoreceptors) may have had a common evolutionary origin. Thus, the numerous structural and molecular features of Tridpalia rhopalia indicate that ancient cubozoan jellyfish are fascinating models for evo/devo insights into eyes and other sensory systems.

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“…For example, strictly aboral orientation of early ectodermal neurites in the hydrozoan Podocoryne is restricted to neurons in the oral region (Groger and Schmid, 2001;Momose and Schmid, 2006), whereas RFamide-positive ectodermal neurites in the scyphozoan Aurelia (Nakanishi et al, 2008) and the anthozoan Acropora millepora (Hayward et al, 2001) develop oral and aboral projections. Similarly, the extensive endodermal nervous system development in planulae observed in N. vectensis has not been described in other cnidarians (de Jong et al, 2006;Groger and Schmid, 2001;Martin, 2000;Nakanishi et al, 2008;Piraino et al, 2011). Additional studies of nervous system formation at high temporal and spatial resolution in these and other cnidarians are needed for a detailed reconstruction of the evolutionary histories of cnidarian neural development.…”

Section: Evolution Of Cnidarian Nervous System Developmentmentioning

confidence: 99%

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms

et al. 2012

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SUMMARYAs a sister group to Bilateria, Cnidaria is important for understanding early nervous system evolution. Here we examine neural development in the anthozoan cnidarian Nematostella vectensis in order to better understand whether similar developmental mechanisms are utilized to establish the strikingly different overall organization of bilaterian and cnidarian nervous systems. We generated a neuron-specific transgenic NvElav1 reporter line of N. vectensis and used it in combination with immunohistochemistry against neuropeptides, in situ hybridization and confocal microscopy to analyze nervous system formation in this cnidarian model organism in detail. We show that the development of neurons commences in the ectoderm during gastrulation and involves interkinetic nuclear migration. Transplantation experiments reveal that sensory and ganglion cells are autonomously generated by the ectoderm. In contrast to bilaterians, neurons are also generated throughout the endoderm during planula stages. Morpholino-mediated gene knockdown shows that the development of a subset of ectodermal neurons requires NvElav1, the ortholog to bilaterian neural elav1 genes. The orientation of ectodermal neurites changes during planula development from longitudinal (in early-born neurons) to transverse (in late-born neurons), whereas endodermal neurites can grow in both orientations at any stage. Our findings imply that elav1-dependent ectodermal neurogenesis evolved prior to the divergence of Cnidaria and Bilateria. Moreover, they suggest that, in contrast to bilaterians, almost the entire ectoderm and endoderm of the body column of Nematostella planulae have neurogenic potential and that the establishment of connectivity in its seemingly simple nervous system involves multiple neurite guidance systems.

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Larval development in Cnidaria: A connection to bilateria?

Cited by 65 publications

References 25 publications

Localized expression of a dpp / BMP2 / 4 ortholog in a coral embryo

Localized expression of a dpp / BMP2 / 4 ortholog in a coral embryo

Cubozoan jellyfish: an Evo/Devo model for eyes and other sensory systems

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms

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