Patterning across the ascidian neural plate by lateral Nodal signalling sources

Abstract

Ascidians are invertebrate chordates with a simple larval tadpole form containing a notochord and an overlying dorsal neural tube. As in vertebrates,the neural tube of ascidian larvae displays positional differences along the rostral-caudal and dorsal-ventral axes in terms of neuronal cell types generated, morphology and gene expression. However, how these differences are established in this simple chordate remains largely unknown. In this study, we show that a single blastomere named b6.5, which is situated in a lateral position in the 32-cell-stage embryo, is a source of signal(s) required for patterning across the medial-lateral axis (future ventral-dorsal axis) of the neural plate. We identify this signal as a Ciona homologue of Nodal, Ci-Nodal. Transcriptional activation of Ci-Nodal in b6.5 depends upon vegetally derived Ci-FGF9/16/20. Using three distinct reagents to inhibit Nodal signals, we show that Nodal signalling is required for neural plate patterning across the medial-lateral axis and that, in the absence of this signal, the caudal-lateral part of the neural plate adopts a medial-like fate. Secondary muscle fate is similarly affected. We conclude that specification of the lateral neural plate is initiated by signalling sources laterally flanking the neural plate and involves a cell-fate choice between lateral and medial neural fates, with Nodal signalling promoting lateral fate. This role for Nodal signalling during ascidian neural plate patterning contrasts with that in vertebrates, where it is implicated in promoting a medial neural fate, the floor plate.

Nodal regulates neural tube formation in the Ciona intestinalis embryo

“…The expression is maintained in descendant cells of b6.5 blastomeres until the gastrula stage (Morokuma et al 2002;Imai et al 2004). Ci-nodal, a nodal-related gene in the ascidian Ciona intestinalis, patterns the neural plate along the medial-lateral axis (Hudson and Yasuo 2005). Ci-nodal is also required for induction of a subset of muscle and notochord cell fates Yasuo 2005, 2006).…”

Lophotrochozoa Get into the Game: The Nodal Pathway and Left/Right Asymmetry in Bilateria

“…The Nodal pathway is essential for endoderm and mesoderm formation in vertebrates (Shen 2007) and mesoderm patterning in Amphi oxus (Yu et al 2002). In ascidians, however, nodal signaling is not critical for endoderm and mesoderm specification because only secondary muscle induction seems to require nodal signaling (Hudson and Yasuo 2005). In addition, echinoderms specify germ layers independently of nodal activity (Duboc and Lepage 2008).…”

“…Besides germ-layer induction and axis specification, Nodal signaling is also required in neural patterning in vertebrates (Shen 2007) and ascidians (Hudson and Yasuo 2005). In vertebrates, generation of anterior neuronal tissue requires inhibition of signaling, although high levels of nodal activity in the posterior epiblast are necessary for ventral patterning of the neural tubes and maintenance of anterior forebrain territories (Shen 2007).…”

“…In vertebrates, generation of anterior neuronal tissue requires inhibition of signaling, although high levels of nodal activity in the posterior epiblast are necessary for ventral patterning of the neural tubes and maintenance of anterior forebrain territories (Shen 2007). In contrast, Nodal signaling is required for lateral fate in the neural tube of ascidians (Hudson and Yasuo 2005). In snails, nodal transcription is seen in the cephalic regions but in an asymmetric pattern.…”

Les embryons d’ascidies

“…Cette approche, couplée à un atlas spatio-temporel extensif des patrons d'expression de plus de 500 gènes de facteurs de transcription ou de signalisation [25,26], permet de dresser, à chaque stade du développement, un schéma précis des gènes exprimés dans chacune des cellules de l'embryon, puis de les relier à leurs régulateurs en amont et à leurs cibles en aval. De telles cascades géniques émergent pour le mésenchyme [6], le muscle [16], le coeur [27], la régionalisation de la plaque neurale [28] ou de l'épiderme de la queue [6,29]. L'analyse systématique de la perte de fonction d'une trentaine de gènes régulateurs exprimés au stade du zygote a conduit à l'émergence d'un réseau de régulation plus général couvrant l'embryon entier jusqu'au démarrage de la gastrulation, un succès qui n'a encore été atteint dans aucun autre système modèle [6].…”