Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms
Abstract
As 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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In the endoderm, many neurons follow the parietal muscles on either side of the eight mesenteries, forming prominent longitudinal tracts.
“In the endoderm, however, many neurons follow the parietal muscles on either side of the eight mesenteries, forming prominent longitudinal tracts [27].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [27]
The most aboral region, the apical organ, remains free of Elav1 and SoxB(2) neural cell bodies.
“Notably, the most aboral region, the ‘apical organ’, often referred to as a sensory centre, remains free of Elav1 and SoxB(2) neural cell bodies [27,29].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [27]
In Nematostella, both ectoderm and endoderm appear capable of producing neurons.
“While in bilaterians neurons originate from the ectoderm, in Nematostella, both ectoderm and endoderm appear to be capable of producing neurons [27].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [27]
Transplantation experiments between transgenic Elav1::memOrange and wild-type embryos showed that the endoderm can produce neurons independently of the ectoderm.
“By using transplantation experiments between transgenic Elav1::memOrange and wild-type embryos, Nakanishi et al. [27] have shown that the endoderm can produce neurons independently of the ectoderm.”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [27]
In the sea anemone Nematostella vectensis, neurons are generated throughout the ectoderm as well as in the endoderm.
“in the sea anemone Nematostella vectensis neurons are generated throughout the ectoderm as well as in the endoderm [98]”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [98]
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- Authors
- Nakanishi, N., Renfer, E., Technau, U., & Rentzsch, F.
- Affiliations
- University of Bergen (NO)
- University of Vienna (AT)
- Corresponding author
- Rentzsch, Fabian
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2012-01-15
- Volume
- 139
- Issue
- 2
- Pages
- 347-357
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2096081781
- Cited by
- 188
- References
- 82
- Citations by year
- 2026: 15 · 2025: 19 · 2024: 17 · 2023: 8 · 2022: 16 · 2021: 9 · 2020: 14 · 2019: 10 · 2018: 11 · 2017: 13 · 2016: 10 · 2015: 17 · 2014: 15 · 2013: 8 · 2012: 6
- FWCI
- 6.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Universitetet i Bergen
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Nematostella vectensis, neural development, interkinetic nuclear migration, gastrulation, planula, sensory neurons, ganglion cells, neurite guidance, neurite orientation, neuropeptides, neural stem cells
- MeSH terms
- Animals, Ectoderm, Endoderm, Immunohistochemistry, Nervous System, Neuropeptides, Sea Anemones, In Situ Hybridization, Fluorescence, Microscopy, Confocal, Animals, Genetically Modified, Microscopy, Electron, Transmission, ELAV Proteins, Neurogenesis, Morpholinos
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