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

Nakanishi, Norihiko; Renfer, Eduard; Technau, Ulrich; Rentzsch, Fabian

doi:10.1242/dev.071902

Cited by 154 publications

(249 citation statements)

References 72 publications

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“…As has been showed for the cnidarian Nematostella vectensis, post-transcriptional regulation by these proteins is an ancient feature shared by Cnidaria and Bilateria (Nakanishi et al, 2012).…”

Section: Adult Elav-positive Structuresmentioning

confidence: 74%

The nervous system of Xenacoelomorpha: a genomic perspective

Perea-Atienza

Gavilán

Chiodin

et al. 2015

Journal of Experimental Biology

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Xenacoelomorpha is, most probably, a monophyletic group that includes three clades: Acoela, Nemertodermatida and Xenoturbellida. The group still has contentious phylogenetic affinities; though most authors place it as the sister group of the remaining bilaterians, some would include it as a fourth phylum within the Deuterostomia. Over the past few years, our group, along with others, has undertaken a systematic study of the microscopic anatomy of these worms; our main aim is to understand the structure and development of the nervous system. This research plan has been aided by the use of molecular/developmental tools, the most important of which has been the sequencing of the complete genomes and transcriptomes of different members of the three clades. The data obtained has been used to analyse the evolutionary history of gene families and to study their expression patterns during development, in both space and time. A major focus of our research is the origin of 'cephalized' (centralized) nervous systems. How complex brains are assembled from simpler neuronal arrays has been a matter of intense debate for at least 100 years. We are now tackling this issue using Xenacoelomorpha models. These represent an ideal system for this work because the members of the three clades have nervous systems with different degrees of cephalization; from the relatively simple sub-epithelial net of Xenoturbella to the compact brain of acoels. How this process of 'progressive' cephalization is reflected in the genomes or transcriptomes of these three groups of animals is the subject of this paper.

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Section: Adult Elav-positive Structuresmentioning

confidence: 74%

The nervous system of Xenacoelomorpha: a genomic perspective

Perea-Atienza

Gavilán

Chiodin

et al. 2015

Journal of Experimental Biology

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“…Molecular developmental evidence suggests that the nervous systems of most animals (Ctenophora excepted) arose from cellular and molecular building blocks present in a common ancestor [1][2][3][4][5]. In 600 Myr of bilaterian radiation, nervous systems have diversified in structure and function.…”

Section: Resultsmentioning

confidence: 99%

Evolution of brain elaboration

Farris¹

2015

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Origin and evolution of the nervous system'. Large, complex brains have evolved independently in several lineages of protostomes and deuterostomes. Sensory centres in the brain increase in size and complexity in proportion to the importance of a particular sensory modality, yet often share circuit architecture because of constraints in processing sensory inputs. The selective pressures driving enlargement of higher, integrative brain centres has been more difficult to determine, and may differ across taxa. The capacity for flexible, innovative behaviours, including learning and memory and other cognitive abilities, is commonly observed in animals with large higher brain centres. Other factors, such as social grouping and interaction, appear to be important in a more limited range of taxa, while the importance of spatial learning may be a common feature in insects with large higher brain centres. Despite differences in the exact behaviours under selection, evolutionary increases in brain size tend to derive from common modifications in development and generate common architectural features, even when comparing widely divergent groups such as vertebrates and insects. These similarities may in part be influenced by the deep homology of the brains of all Bilateria, in which shared patterns of developmental gene expression give rise to positionally, and perhaps functionally, homologous domains. Other shared modifications of development appear to be the result of homoplasy, such as the repeated, independent expansion of neuroblast numbers through changes in genes regulating cell division. The common features of large brains in so many groups of animals suggest that given their common ancestry, a limited set of mechanisms exist for increasing structural and functional diversity, resulting in many instances of homoplasy in bilaterian nervous systems.

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“…[88][89][90]; but in none of these cases has any large concentration of neurons (ganglia) been identified [82]. Cnidarians often possess both endodermal and ectodermal NSs [91]. As highlighted by Koizumi et al [82], it has been observed that nerve cells residing either in ectoderm or the endoderm express different types of peptides.…”

Section: Transformation From Nerve Nets To Compact Brains In the Xenamentioning

confidence: 99%

Xenacoelomorpha: a case of independent nervous system centralization?

Gavilán

Perea-Atienza

Martı́nez

2016

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Centralized nervous systems (NSs) and complex brains are among the most important innovations in the history of life on our planet. In this context, two related questions have been formulated: How did complex NSs arise in evolution, and how many times did this occur? As a step towards finding an answer, we describe the NS of several representatives of the Xenacoelomorpha, a clade whose members show different degrees of NS complexity. This enigmatic clade is composed of three major taxa: acoels, nemertodermatids and xenoturbellids. Interestingly, while the xenoturbellids seem to have a rather 'simple' NS (a nerve net), members of the most derived group of acoel worms clearly have ganglionic brains. This interesting diversity of NS architectures (with different degrees of compaction) provides a unique system with which to address outstanding questions regarding the evolution of brains and centralized NSs. The recent sequencing of xenacoelomorph genomes gives us a privileged vantage point from which to analyse neural evolution, especially through the study of key gene families involved in neurogenesis and NS function, such as G protein-coupled receptors, helixloop-helix transcription factors and Wnts. We finish our manuscript proposing an adaptive scenario for the origin of centralized NSs (brains).

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

Cited by 154 publications

References 72 publications

The nervous system of Xenacoelomorpha: a genomic perspective

The nervous system of Xenacoelomorpha: a genomic perspective

Evolution of brain elaboration

Xenacoelomorpha: a case of independent nervous system centralization?

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