A tension-induced morphological transition shapes the avian extra-embryonic territory
Preprint posted on 8 February 2024 https://www.biorxiv.org/content/10.1101/2024.02.08.579502v1
“A Quail of Two Tissues in the Epibolic Saga " Ever wondered how a small embryo, sitting atop an egg yolk, grows to cover the whole yolk?
Selected by Sameer Thukral
Categories: cell biology, developmental biology
Background to the preprint:
How do the embryo, the surrounding extra-embryonic tissues, and the yolk interact mechanically to orchestrate the intricate process of gastrulation?
Extraembryonic tissues, encompassing structures such as the placenta, amnion, and serosa, serve crucial protective and nutritive functions. But do they have a mechanical role?
Epiboly, the spreading of the embryonic tissue over the yolk, is a pivotal event in the early stages of development in amniote embryos. In this study, the authors, using quail embryos explore how the embryo is able to stretch 200 fold, to engulf the entire huge (20mm diameter) yolk within a few days (Figure 1A). While epiboly is primarily driven by the outward migration of the epiblast border along the vitelline membrane, the precise mechanisms underlying this remarkable expansion have remained elusive (Figure 1B).
The epiblast, a 3mm disk, positioned atop the yolk, consists of two parts: Embryonic-Proper (EP) region and the Extra-Embryonic (EE) region. The EP region houses cells responsible for giving rise to the embryo’s body. Concentrically surrounding these, the Extra-Embryonic (EE) Region has cells that contribute to the formation of nutritive tissues. At the posterior margin between EE and EP, a crescent-shaped region contracts to form the primitive streak, the structure along which gastrulation takes place (Figure 1C). This posterior contraction provokes rotational vortex-like tissue flows across the entire EP.
How can the epiblast expand so quickly? Do the EE and EP mechanically influence each other? And how does this lead to primitive streak formation? The preprint addresses these interesting questions.
Figure 1. A: Expansion of the epiblast over the yolk. B: Expansion of the epiblast disc ex-ovo. C: Cartoon by the preLights author to highlight EE, EP and Primitive streak.
Key findings:
- A spatial pattern of areal expansion, mitosis and reversible cell stretching lead to cell flattening
Areal expansion: The authors found that during epiboly, cell area expansion predominantly occurs within the EE region and not in the EP region, highlighting a distinct mechanical response of the two regions. High-resolution imaging and segmentation demonstrated that EE cells extensively increase their apical area in response to tissue expansion. Tracking cell divisions verified that it is predominantly an increase in cell area, supplemented by increase in cell number due to division, which contributes to this rapid expansion.
Cell Shape Flattening: The analysis revealed a remarkable cellular response in the EE, wherein initially columnar cells undergo stretching and flatten into a squamous morphology. Upon laser-ablations to induce relaxation, the squamous cells reverted back to their original columnar conformation, indicating the reversibility of this process. Importantly, this columnar to squamous transition was observed exclusively within the EE region and not in the EP region.
Thus, the cell area expansion is driven by cell flattening and is a reversible phenomenon, driven by epiboly-driven tension.
- Same tension but two different effects: Modelling resolves the conflict
How can the same tension of epiboly cause cell expansion of the EE region and rotational flow in the EP region? Is it necessarily true that EE and EP cells are built differently?
To answer this, the authors formulated a viscoelastic model that incorporated reversible area changes and irreversible shear flow to simulate the mechanical behaviours. Simply put, shear flows arising from differences in tension at the margin lead to permanent cell shape changes, while the isotropic tension induced by epiboly would cause reversible cell area expansion.
In the tissue, average margin tension shields the EP region from epiboly-induced tension, thereby restricting area expansion to the EE region. Differences in tension along the EE/EP margin were hypothesised to drive rotational tissue flows associated with primitive streak formation.
- Testing the model predictions
To experimentally validate this, the authors marked cells within the two regions using photoconversion. The results showed distinct responses: EP regions exhibited minimal changes in cell area, whereas EE regions underwent significant stretching. Interestingly, regions near the margin displayed an intermediate behaviour.
Lastly, the authors followed the photo-converted cells when the epiboly driven tension was abrogated by detaching the epiblast from the surface. As hypothesised by the computational model, all photo-converted regions returned to their initial area but the shape changes remained. This verified their model in which areal expansion is tension driven and reversible, while causing shape changes driven by shear deformation are irreversible.
Why I think this work is significant:
By linking tissue-scale mechanics with cellular changes, this study uncovers a new mechanical role for extra-embryonic tissues beyond their known functions of nutrition and protection. It shows the tension that shapes the EE tissue does not propagate to the EP, while it was previously thought that the entire embryo was under tension. The margin at the interface between EP and EE shields the EP from the epiboly-induced tension while promoting the formation of the primitive streak. The modelling in this study is simple and elegant, requiring no need for tissue-specific responses but solely focusing on differences in how tissues experience that tension. From flies to fish, perhaps we need to see EE tissues in a fresh (mechanical) light.
Questions to the authors and future directions:
- Is there a gradient of EE areal expansion or cell height spanning from the edge of epiboly to the margin?
- What characterises the EE/EP margin?
- Is there a bias in cell division orientation along the direction of tension in the EE?
- What happens to the primitive streak in the EE-ablated tissue? Can a more varied tension at the border change the vortex direction?
Posted on: 14 March 2024
doi: https://doi.org/10.1242/prelights.36816
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