| Peer-reviewed | Observational study | Animals |
Scientists have uncovered a key mechanism in jellyfish embryos that provides new insights into how the body plan of these animals develops along a central axis from their ‘head’ to ‘tail’.
The jellyfish, Clytia hemisphaerica. Image credit: Tsuyoshi Momose (CC BY 4.0)
The study, published as a Reviewed Preprint in eLife, is described by the editors as a significant and fundamental contribution to the field. They say the authors provide compelling evidence for their analysis of body plan development in the jellyfish Clytia hemisphaerica – which may contribute to a deeper understanding of the origin of Wnt signalling in the early animal kingdom. The findings will be of broad interest to developmental and evolutionary biologists.
Body axis specification – the process that establishes directional organisation in animals, such as head-to-tail alignment – is a crucial step that occurs during embryo development. Wnt signalling refers to a network of proteins that controls processes such as cell differentiation, and is known to play a role in body axis specification. It can be seen as a set of instructions that tells cells where to grow and how to form an animal’s body shape, including which end becomes the head and which becomes the tail. The jellyfish is a useful model organism for studies to help understand early multicellular animals, due to the relative simplicity of the larva and their evolutionary position as an outgroup to bilaterians – a branch of animals with bilateral symmetry which share a common ancestor.
“In our previous research, we have shown that a protein called Wnt3 is stored on one side of the egg – the animal pole – in the form of messenger RNA and works together with cellular proteins of the so-called Wnt/β-catenin pathway to locally define the future ‘mouth-end’ of jellyfish embryos,” explains lead author Julie Uveira, a laboratory engineer at the French National Centre for Scientific Research and at the Villefranche-sur-mer Developmental Biology Laboratory (CNRS/Sorbonne University), Paris, France. “In the current study, we aimed to find out how that process continues down the length of the embryo to generate the typical elongated ‘torpedo’ shape of the larva.”
To answer this question, Uveira and colleagues began by investigating the development of the body plan in jellyfish embryos that lacked Wnt3 activity. They found that these embryos do not have a central axis – their body organisation is more random instead. Additionally, the boundaries between cells looked wrinkly, suggesting a lack of the necessary tension and structure to give the cells their typical shape. When they reintroduced Wnt3 into a part of these embryos, the proper body shape was restored, highlighting its crucial role in axis formation.
Planar cell polarity (PCP) is a mechanism that aligns cells across animal tissues, ensuring they are pointed in the same direction. It is crucial for processes such as tissue elongation and the coordinated movement of cells. So, the team sought to investigate how Wnt3 interacts with PCP proteins in jellyfish embryos. Using fluorescent imaging of cilia – the hairy devices on cells that act as sensors or motors – they showed that Wnt3 causes cells to become concerted, all facing one end of the larva. Gradually, this polarity spreads to neighbouring cells until the entire body length of the jellyfish larva has a single aligned axis. This polarity likely contributes to a taut cell structure and provides a mechanical force so that the embryo forms its characteristic torpedo-shaped body.
This process is independent of Wnt3’s previously established interaction with β-catenin. The team demonstrated this by blocking β-catenin activity in jellyfish embryos whilst allowing normal Wnt3 function. In such embryos, Wnt3 was still able to direct PCP proteins to guide development along the body axis. In contrast, in the absence of PCP proteins, Wnt3 could not direct axis development, except for locally near its site of production. These experiments show that Wnt3 has two separate roles in body plan development: Wnt/β-catenin activation and PCP orientation.
“We have uncovered a two-step process that drives development along a central axis in jellyfish embryos,” explains senior author Tsuyoshi Momose, a researcher at the Villefranche-sur-mer Developmental Biology Laboratory (CNRS/Sorbonne University). “In the first step, Wnt3 defines the future mouth area in concert with β-catenin and also, without β-catenin, provides the directional cue to orient the central axis. In the second step, Wnt3 sets off a cascade of PCP polarisation which aligns this axis cohesively across the entire embryo.”
In addition to helping explain a key step in the process of early embryo development, the discovery may explain why so many animals share a central axis from head-to-tail and hints at how their body plans evolved. Similar processes have been detailed in fruit flies and many other animals, suggesting that this process evolved early on and persisted through the evolution of a wide array of animals.
“Evolutionary biology has not paid enough attention to cellular-level organisation such as adhesion and cell polarity,” explains Uveira. “Cell polarity is relatively important in simple animals such as jellyfish. Comparing these processes in animals that diverged at different time points in evolution may help us determine when and why this common feature emerged, diverged and persisted.”
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