Abstract
ABSTRACTEmbryonic tissues are shaped by the dynamic behaviours of their constituent cells. To understand such cell behaviours and how they evolved, new approaches are needed to map out morphogenesis across different organisms. Here, we apply a quantitative approach to learn how the notochord forms during the development of amphioxus: a basally branching chordate. Using a single-cell morphometrics pipeline, we quantify the geometries of thousands of amphioxus notochord cells, and project them into a common mathematical space, termed morphospace. In morphospace, notochord cells disperse into branching trajectories of cell shape change, revealing a dynamic interplay between cell shape change and growth that collectively contributes to tissue elongation. By spatially mapping these trajectories, we identify conspicuous regional variation, both in developmental timing and trajectory topology. Finally, we show experimentally that, unlike ascidians but like vertebrates, posterior cell division is required in amphioxus to generate full notochord length, thereby suggesting this might be an ancestral chordate trait that is secondarily lost in ascidians. Altogether, our novel approach reveals that an unexpectedly complex scheme of notochord morphogenesis might have been present in the first chordates. This article has an associated ‘The people behind the papers’ interview.
Highlights
A major challenge in biology is to understand how individual cells coordinate their behaviours during embryogenesis to generate tissues of the correct geometry and size, and how these behaviours are modified through evolution to generate morphological novelty
To build a complete picture of cell shape changes during amphioxus notochord development, we present a pipeline to segment and quantify the shapes of thousands of individual notochord cells, and embed them in a single-cell morphospace; a mathematical space in which cells disperse into trajectories of shape change
A single-cell morphospace captures branching trajectories of shape differentiation specific to cell type In amphioxus, notochord formation involves a radical change in cellular organisation from a seemingly disorganised array of rounded cells at the 6-somite stage, to a regular trilaminar array at 14 ss
Summary
A major challenge in biology is to understand how individual cells coordinate their behaviours during embryogenesis to generate tissues of the correct geometry and size, and how these behaviours are modified through evolution to generate morphological novelty. The notochord is a pivotal case study in this context It is a defining feature of the chordate body plan with diverse contributions to axial development. The notochord exerts essential roles in body plan formation. This includes contributions to axis elongation and mechanical stabilisation of the body axis (Stemple, 2005; Segade et al, 2016; Xiong et al, 2018 preprint), and, in vertebrates, the secretion of organising signals that provide dorsoventral patterning information to the adjacent neural tube and somites (Placzek et al, 1991; Pourquié et al, 1993; Yamada et al, 1993). The cephalochordate amphioxus provides a unique opportunity to fill this gap and further our understanding of morphogenetic principles common to all chordates, which are likely to have evolved from the common chordate ancestor
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