Pattern regulation in a regenerating jellyfish.

Chiara Sinigaglia,Sophie Peron,Lucas Leclère,Julia Steger,Carine Barreau,Evelyn Houliston,Jeanne Eichelbrenner,Sandra Chevalier

doi:10.7554/elife.54868

Abstract

Jellyfish, with their tetraradial symmetry, offer a novel paradigm for addressing patterning mechanisms during regeneration. Here we show that an interplay between mechanical forces, cell migration and proliferation allows jellyfish fragments to regain shape and functionality rapidly, notably by efficient restoration of the central feeding organ (manubrium). Fragmentation first triggers actomyosin-powered remodeling that restores body umbrella shape, causing radial smooth muscle fibers to converge around 'hubs' which serve as positional landmarks. Stabilization of these hubs, and associated expression of Wnt6, depends on the configuration of the adjoining muscle fiber 'spokes'. Stabilized hubs presage the site of the manubrium blastema, whose growth is Wnt/β-catenin dependent and fueled by both cell proliferation and long-range cell recruitment. Manubrium morphogenesis is modulated by its connections with the gastrovascular canal system. We conclude that body patterning in regenerating jellyfish emerges mainly from local interactions, triggered and directed by the remodeling process.

Highlights

Regrowth of new structures and their integration into existing body parts during animal regeneration require varying contributions from cell proliferation and tissue remodeling, an issue already highlighted by early studies on planarians (Morgan, 1901)
Restoration of medusa form involves both body remodeling and regrowth of organs In order to gain insight into the self-organizing properties of the jellyfish Clytia, we explored its responses to a diverse array of dissections (Figure 1E-J, 1-S1, 1-S2)
Functional manubria regenerated in 4 days (Figure 1E; n: 43/44), while gonads and tentacle bulbs reformed in about a week (Figure 1F,G, 1-S1; gonads: 48/48, bulbs: 45/52; after 8 days in fed jellyfish)

Summary

Introduction

Regrowth of new structures and their integration into existing body parts during animal regeneration require varying contributions from cell proliferation and tissue remodeling, an issue already highlighted by early studies on planarians (Morgan, 1901). The (re)specification of positional information has been largely attributed to organizer-like centers and gradients of diffusible morphogens, modeled to pattern the surrounding cells in a concentration-dependent manner Hydra polyps or vertebrate limbs, the site of injury transforms into a signaling center resetting positional information and triggering the regrowth of missing elements through proliferation and/or tissue remodeling (Chera et al, 2009; Owlarn et al, 2017). Alongside morphogen-based systems, structural and mechanical cues can contribute to patterning. In contrast the jellyfish (medusa), a dispersive and sexually reproductive form, generated asexually from the polyp stage of numerous species belonging to the Medusozoa clade (Leclère et al, 2016), has received relatively little attention

Methods

Results

Conclusion