Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos

Coulcher, Joshua F; Roure, Agnès; Chowdhury, Rafath; Robert, Méryl; Lescat, Laury; Bouin, Aurélie; Cadavid, Juliana Carvajal; Nishida, Hiroki; Darras, Sébastien

doi:10.7554/elife.59157

Cited by 10 publications

(55 citation statements)

References 80 publications

(155 reference statements)

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“…We first determined whether gene expression was conserved in the model species that we have used here, namely the ascidian Phallusia mammillata and the European amphioxus B. lanceolatum . In C. intestinalis , the dynamic of expression for TFs and signaling molecules in the vPNS is as follows [ 27 ] (Fig. 1 ).…”

Section: Resultsmentioning

confidence: 99%

“…From tailbud stages, Dlk , Pou4 , Myt1 , Atoh1/7 , Atoh8 , Celf3/4/5/6 and Slc17a6/7/8 (also known as Vglut ) are expressed in both dorsal and ventral ESNs. We have previously shown that several neurogenic midlines and ESNs markers have a conserved expression in P. mammillata [ 27 ]. Here, we report the expression of additional orthologous genes in Phallusia (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…2 D, E). Interestingly, we previously described Ascl1/2 expression in two ascidians that have diverged from Ciona and Phallusia almost 400 My ago, and its expression was detected in a subset of the VML only, possibly more similar to the expression in amphioxus [ 27 ].…”

Section: Resultsmentioning

confidence: 99%

“…Interestingly, these genes are also expressed in the dorsal midline (DML) that derives from the NPB and that is also a neurogenic territory giving rise to dorsal CESNs. A recent study proposes that Msx directly activates the expression of Klf1/2/4/17 and Nkxtun3 while Tox would be under the control of Ascl1/2.b, suggesting the involvement of two separate modules during the establishment of the neurogenic territory [ 27 ]. Within this region, lateral inhibition by future neurons, expressing the Notch ligand Dlk, will prevent adjacent epidermal cells from adopting a neuronal fate, thus avoiding the formation of an excessive number of CESNs [ 18 ].…”

Section: Introductionmentioning

confidence: 99%

“…They ultimately regulate CESN fate acquisition that can be revealed by the expression of the pan-neuronal marker Celf3/4/5/6 (previously known as Celf3.a ) [ 24 ]. Interestingly, we have recently shown a high degree of conservation of the molecular mechanisms regulating caudal PNS formation within ascidians [ 27 ].

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Highly distinct genetic programs for peripheral nervous system formation in chordates

et al. 2022

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Background Vertebrates develop their peripheral nervous system (PNS) from transient unique embryonic structures, the neural crest, and the ectodermal placodes that are located at the border of the forming central nervous system. By contrast, in the invertebrate chordates, amphioxus and ascidians, a large part of the PNS originates at the opposite of the embryo, in the ventral ectoderm. In both groups, a biphasic mechanism regulates ventral PNS formation: high BMP levels specify a neurogenic territory within which glutamatergic epidermal sensory neuron formation is controlled by the Notch pathway. Given these similarities and the phylogenetic relationships within chordates, it is likely that ventral PNS is an ancestral feature in chordates and that it has been lost in vertebrates. Results In order to get insights into the molecular control of ventral PNS formation and to test the hypothesis of their homology and potential contribution to the emergence of vertebrate PNS, we undertook a close comparison of ventral PNS formation in the ascidian Phallusia mammillata and the amphioxus Branchiostoma lanceolatum. Using timed RNA-seq series, we identified novel markers of the ventral PNS during different phases of its development in both species. By extensively determining the expression of paralogous and orthologous genes, we observed that only a minority of genes have a shared expression in the ventral PNS. However, a large fraction of ventral PNS orthologous genes are expressed in the dorsally forming PNS of vertebrates. Conclusions Our work has significantly increased the molecular characterization of ventral PNS formation in invertebrate chordates. The low observed conservation of gene expression in the ventral PNS suggests that the amphioxus and ascidian ventral PNS are either not homologous, or alternatively extensive drift has occurred in their regulatory mechanisms following a long period (600 My) of separate evolution and accelerated evolution in the ascidian lineage. The homology to genes expressed in the dorsally forming PNS of vertebrates suggests that ancestral sensory neurons gene networks have been redeployed in vertebrates.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Highly distinct genetic programs for peripheral nervous system formation in chordates

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Genomic Resources and Annotations for a Colonial Ascidian, the Light-Bulb Sea Squirt Clavelina lepadiformis

Daric,

Lanoizelet,

Mayeur

et al. 2024

Genome Biology and Evolution

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Ascidian embryos have been studied since the birth of experimental embryology at the end of the 19th century. They represent textbook examples of mosaic development characterized by a fast development with very few cells and invariant cleavage patterns and lineages. Ascidians belong to tunicates, the vertebrate sister group, and their study is essential to shed light on the emergence of vertebrates. Importantly, deciphering developmental gene regulatory networks has been carried out mostly in two of the three ascidian orders, Phlebobranchia and Stolidobranchia. To infer ancestral developmental programs in ascidians, it is thus essential to carry out molecular embryology in the third ascidian order, the Aplousobranchia. Here, we present genomic resources for the colonial aplousobranch Clavelina lepadiformis: a transcriptome produced from various embryonic stages, and an annotated genome. The assembly consists of 184 contigs making a total of 233.6 Mb with a N50 of 8.5 Mb and a L50 of 11. The 32,318 predicted genes capture 96.3% of BUSCO orthologs. We further show that these resources are suitable to study developmental gene expression and regulation in a comparative framework within ascidians. Additionally, they will prove valuable for evolutionary and ecological studies.

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Regulation of anterior neurectoderm specification and differentiation by BMP signaling in ascidians

Roure

Chowdhury

Darras

2022

Preprint

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Three palps make the most anterior structure of the ascidian larva. These ectodermal derivatives have both a sensory and adhesive functions essential for metamorphosis. They derive from the anterior neural border and their formation is regulated by signaling pathways such as FGF and Wnt. Since they also share gene expression profiles with vertebrate anterior neural tissue and cranial placodes, their study should shed light on the emergence of the unique vertebrate telencephalon. Here, we show that BMP signaling regulates two phases of palps formation in Ciona intestinalis. During gastrula stages, the anterior neural border marked by Foxc is specified in a domain of inactive BMP signaling, and activating BMP prevented its formation. Later on, inhibiting BMP led to the formation of a single large palp, most likely of dorsal identity. Our results indicate that BMP signaling regulates papilla vs inter-papilla fate decision within the palps forming region. Finally, we showed that modulating BMP signaling led to similar palps phenotypes in another ascidian species Phallusia mammillata. This led us to screen transcriptomic data and identify novel palps markers. Collectively, we provide a better molecular description of palps formation in ascidians that will be instrumental for comparative studies within ascidians and between ascidians and other chordates.

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Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos

Cited by 10 publications

References 80 publications

Highly distinct genetic programs for peripheral nervous system formation in chordates

Highly distinct genetic programs for peripheral nervous system formation in chordates

Genomic Resources and Annotations for a Colonial Ascidian, the Light-Bulb Sea Squirt Clavelina lepadiformis

Regulation of anterior neurectoderm specification and differentiation by BMP signaling in ascidians

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