The ascidian mouth opening is derived from the anterior neuropore: Reassessing the mouth/neural tube relationship in chordate evolution

Veeman, Michael; Newman-Smith, Erin; El‐Nachef, Danny; Smith, William C.

doi:10.1016/j.ydbio.2010.04.028

Cited by 49 publications

(54 citation statements)

References 38 publications

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“…FoxB, Snail, and ETR regulatory sequences have been reported previously (Corbo et al, 1997;Imai et al, 2009;Veeman et al, 2010). The Mnx −5 kb regulatory sequence was amplified from genomic DNA using the primers F-TATGGCGCGCCTCCTGATGTGACGGATTTATGACTG, R-TATG-CGGCCGCTAGCATCATTTTAAATCTTAAATATCAAAGGTTC and cloned into a H2B:Cherry-containing expression vector using NotI and AscI restriction sites.…”

Section: Molecular Cloningmentioning

confidence: 99%

Nodal and FGF coordinate ascidian neural tube morphogenesis

Navarrete

Levine

2016

Development

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Formation of the vertebrate neural tube represents one of the premier examples of morphogenesis in animal development. Here, we investigate this process in the simple chordate Ciona intestinalis. Previous studies have implicated Nodal and FGF signals in the specification of lateral and ventral neural progenitors. We show that these signals also control the detailed cellular behaviors underlying morphogenesis of the neural tube. Live-imaging experiments show that FGF controls the intercalary movements of ventral neural progenitors, whereas Nodal is essential for the characteristic stacking behavior of lateral cells. Ectopic activation of FGF signaling is sufficient to induce intercalary behaviors in cells that have not received Nodal. In the absence of FGF and Nodal, neural progenitors exhibit a default behavior of sequential cell divisions, and fail to undergo the intercalary and stacking behaviors essential for normal morphogenesis. Thus, cell specification events occurring prior to completion of gastrulation coordinate the morphogenetic movements underlying the organization of the neural tube.

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Section: Molecular Cloningmentioning

confidence: 99%

Nodal and FGF coordinate ascidian neural tube morphogenesis

Navarrete

Levine

2016

Development

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“…The orientation of most of the adult urochordates is difficult to make out because of their metamorphoses with the rotation of the gut, but the development of certain ascidians, such as Ciona and Clavelina, shows that the stomodaeum/mouth is situated at the same side as the neural tube, which then ought to be described as ventral (Seeliger andHartmeyer, 1893-1911;Veeman et al, 2010). The ascidian larvae have a neural tube without nerve cells in the tail and an anterior brain vesicle, in some species with an eye, a statocyte and various other sensory structures (Burighel and Cloney, 1997).…”

Section: Deuterostomiamentioning

confidence: 99%

“…This implies that the mouth (stomodaeum) should develop inside the brain area or be a completely new structure. In the urochordates (ascidians), the stomodaeum is derived from the anterior neuropore, which is situated at the anterior edge of the neural plate (Veeman et al, 2010). In vertebrates (Xenopus), the mouth develops from the anterior part of the neural fold, which extends forward in a narrow line and appears to become pinched off from the neural tube (Drysdale and Elinson, 1991).…”

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confidence: 99%

Larval nervous systems: true larval and precocious adult

Nielsen

2015

Journal of Experimental Biology

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The apical organ of ciliated larvae of cnidarians and bilaterians is a true larval organ that disappears before or at metamorphosis. It appears to be sensory, probably involved in metamorphosis, but knowledge is scant. The ciliated protostome larvae show ganglia/nerve cords that are retained as the adult central nervous system (CNS). Two structures can be recognized, viz. a pair of cerebral ganglia, which form the major part of the adult brain, and a blastoporal (circumblastoporal) nerve cord, which becomes differentiated into a perioral loop, paired or secondarily fused ventral nerve cords and a small perianal loop. The anterior loop becomes part of the brain. This has been well documented through cell-lineage studies in a number of spiralians, and homologies with similar structures in the ecdysozoans are strongly indicated. The deuterostomes are generally difficult to interpret, and the nervous systems of echinoderms and enteropneusts appear completely enigmatic. The ontogeny of the chordate CNS can perhaps be interpreted as a variation of the ontogeny of the blastoporal nerve cord of the protostomes, and this is strongly supported by patterns of gene expression. The presence of 'deuterostomian' blastopore fates both in an annelid and in a mollusk, which are both placed in families with the 'normal' spiralian gastrulation type, and in the chaetognaths demonstrates that the chordate type of gastrulation could easily have evolved from the spiralian type. This indicates that the latest common ancestor of the deuterostomes was very similar to the latest common pelago-benthic ancestor of the protostomes as described by the trochaea theory, and that the neural tube of the chordates is morphologically ventral. KEY WORDS: Deuterostomy, Metamorphosis, Nervous systems, Dorsal-ventral orientation IntroductionStudies on ontogeny are very important for our understanding of nervous system evolution and diversification, and new methods have made important contributions to knowledge of the structure and development of larval nervous systems and their relationships to adult nervous systems.The nervous system has for a long time been considered one of the most conservative animal organ systems and has therefore been given high importance in studies of animal evolution. More than a century ago, Hatschek (Hatschek, 1888) introduced the names Zygoneura (now Protostomia), Ambulacraria and Chordonia (now Chordata) for three major groups of the Bilateria, based on the structure and position of the central nervous system (CNS). The Zygoneura were characterized by a paired longitudinal ventral nerve cord [a cluster of nervous cells including their cell bodies, as opposed to a nerve, which is a bundle of axons (Richter et al., 2010); the ventral nerve cord may REVIEWThe Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.*Author for correspondence (cnielsen@snm.ku.dk) be specialized into rows of ganglia connected by connectives] and the Chordonia by an unpaired dorsal n...

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“…Eggs from a dmrt1 +/-adult were crossed to a line carrying a stably integrated transgene composed of the regulatory region of the C. savignyi Etr1 gene fused to the cDNA for Venus fluorescent protein (Veeman et al, 2010). Venus protein was visualized by immunostaining, and actin with Bodipy-FL phallacidin, as described previously (Veeman et al, 2008).…”

Section: Immunostainingmentioning

confidence: 99%

“…For this study we crossed the dmrt1 mutant line with a line carrying a stably integrated transgene composed of the regulatory region of the early pan-neural gene etr1 (Yagi and Makabe, 2001) driving expression of the fluorescent protein Venus (etr1-Venus) (Veeman et al, 2010). Expression of the transgene could be detected by antibody staining as early as the gastrula stage, whereas direct fluorescence of Venus could not be detected until the neurula stage.…”

Section: Timecourse Of Phenotypic Onsetmentioning

confidence: 99%

doublesex/mab3 related-1 (dmrt1) is essential for development of anterior neural plate derivatives in Ciona

et al. 2010

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SUMMARYAscidian larvae have a hollow, dorsal central nervous system that shares many morphological features with vertebrate nervous systems yet is composed of very few cells. We show here that a null mutation in the gene dmrt1 in the ascidian Ciona savignyi results in profound abnormalities in the development of the sensory vesicle (brain), as well as other anterior ectodermal derivatives, including the palps and oral siphon primordium (OSP). Although the phenotype of the mutant embryos is variable, the majority have a complete loss of the most anterior structures (palps and OSP) and extensive disruption of sensory structures, such as the light-sensitive ocellus, in the sensory vesicle. dmrt1 is expressed early in the blastula embryo in a small group of presumptive ectodermal cells as they become restricted to anterior neural, OSP and palp fates. Despite the early and restricted expression of dmrt1, we were unable, using several independent criteria, to observe a defect in the mutant embryos until the early tailbud stage. We speculate that the variability and late onset in the phenotype may be due to partially overlapping activities of other gene products.KEY WORDS: Ascidian, Brain, Doublesex, Nervous system doublesex/mab3 related-1 (dmrt1) is essential for development of anterior neural plate derivatives in Ciona

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The ascidian mouth opening is derived from the anterior neuropore: Reassessing the mouth/neural tube relationship in chordate evolution

Cited by 49 publications

References 38 publications

Nodal and FGF coordinate ascidian neural tube morphogenesis

Nodal and FGF coordinate ascidian neural tube morphogenesis

Larval nervous systems: true larval and precocious adult

doublesex/mab3 related-1 (dmrt1) is essential for development of anterior neural plate derivatives in Ciona

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