bioRxiv Science⌕ Search

Biology subjects

Yasuo, H.

Publications and source records attributed to Yasuo, H..

3 recordsLinked to original sources

Early transcriptional similarities between two distinct neural lineages during ascidian embryogenesis

In chordates, the central nervous system arises from precursors that have distinct developmental and transcriptional trajectories. Anterior nervous systems are ontogenically associated with ectodermal lineages while posterior nervous systems are associated with mesoderm. Taking advantage of the well-documented cell lineage of ascidian embryos, we asked how the transcriptional states of the different neural lineages become similar during the course of progressive lineage restriction. We performed single-cell RNA sequencing (scRNA-seq) analyses on hand-dissected neural precursor cells of the two distinct lineages, together with those of their sister cell lineages, with a high temporal resolution covering five successive cell cycles from the 16-cell to neural plate stages. A transcription factor binding site enrichment analysis of neural specific genes at the neural plate stage revealed limited evidence for shared transcriptional control between the two neural lineages, consistent with their different ontogenies. Nevertheless, PCA analysis and hierarchical clustering showed that, by neural plate stages, the two neural lineages cluster together. Consistent with this, we identified a set of genes enriched in both neural lineages at the neural plate stage, including miR-124, CELF3/5/6, Zic.r-b, and Ets1/2.

developmental biology↗

Model of neural induction in the ascidian embryo

How cell specification can be controlled in a reproducible manner is a fundamental question in development biology. In ascidians, a group of marine invertebrate chordates, geometry plays a key role in achieving this control. Here, we use mathematical modeling to demonstrate that geometry dictates the neural-epidermal cell fate choice in the 32-cell stage ascidian embryo by a two-step process involving first the modulation of ERK signaling and second, the expression of the neural marker gene, Otx. The model describes signal transduction by the ERK pathway that is stimulated by FGF and repressed by ephrin, and ERK-mediated control of Otx gene expression, which involves both an activator and an inhibitor of transcription. Considering the measured area of cell surface contacts with FGF- or ephrin-expressing cells as inputs, the solutions of the model reproduce the experimental observations about ERK activation and Otx expression in the different cells under normal and perturbed conditions. Sensitivity analyses and computations of Hill coefficients allow to quantify the robustness of the specification mechanism controlled by cell surface area and to identify the respective role played by each signaling input. Simulations also predict in which conditions the dual control of gene expression by an activator and an inhibitor that are both under the control of ERK can induce a robust ON/OFF control of neural fate induction. Author summaryThe development of a single cell zygote into a multicellular embryo occurs thanks to the combination of cell division and cell specification. The latter process corresponds to the progressive acquisition by the embryonic cells of their final physiological and functional characteristics, which rely on well-defined signaling-controlled genetic programs. The origin of the great robustness of cell specification remains poorly understood. Here, we address this question in the framework of the embryonic neural fate induction in ascidians, which are marine invertebrates. At the 32-cells stage, four cells identified by their precise location in the embryo adopt neural fate. On the basis of experimental observations, we develop a mathematical model that predicts that the choice between the neural or epidermal fate is controlled by the cell surface areas of the cells in contact with two antagonistic signals, FGF and ephrin. Our findings provide a computational confirmation of the major role played by the geometry of the embryo in controlling cell lineage acquisition during ascidian development.

developmental biology↗

Nodal and Eph signalling relay drives the transition between apical constriction and apico-basal shortening during ascidian endoderm invagination

Gastrulation is the first major morphogenetic event during animal embryogenesis. Ascidian gastrulation starts with the invagination of 10 endodermal precursor cells between the 64- and late 112-cell stages. This process occurs in the absence of endodermal cell division and in two steps, driven by myosin-dependent contractions of the acto-myosin network. First, endoderm precursors constrict their apex. Second, they shorten apico-basally, while retaining small apical surfaces, thereby causing invagination. The mechanisms controlling the endoderm mitotic delay, the step 1 to step 2 transition, and apico-basal shortening have remained elusive. Here, we demonstrate the conserved role during invagination of Nodal and Eph signalling in two distantly related ascidian species (Phallusia mammillata and Ciona intestinalis). We show that the transition to step 2 is controlled by Nodal relayed by Eph signalling and that Eph signalling has a Nodal-independent role in mitotic delay. Interestingly, both Nodal and Eph signals are dispensable for endodermal germ layer fate specification. Summary statementIdentification of a regulatory developmental signalling sub-network driving endoderm cell shape changes during ascidian endoderm invagination, not involved in cell fate specification.

developmental biology↗