Muscle cell type evolution and development – MYODEVO

The project is structured into 4 complementary tasks: (i) developing the scyphozoan Pelagia noctiluca as a functional model organism - generating culture laboratory strains, transcriptomic data and developing efficient functional methods, (ii) generating a comprehensive picture of the muscle cell types in Clytia and Pelagia life stages - integrating single cell transcriptomic data, in situ hybridization, cytological and ultrastructural data as well as physiological assays of contractility, (iii) characterizing the function of a selected array of structural muscle protein and transcription factors likely involved in myogenesis in Clytia and Pelagia, (iv) performing comparative analyses and reconstructing the early evolution of muscle cell types.

We could set up a system for rearing Pelagia noctiluca jellyfish, allowing completing the life cycle in the laboratory.
We have characterized the muscle cell types of the jellyfish Clytia hemisphaerica using single cell sequencing. These data contributed to the creation of a cell type atlas of the Clytia jellyfish, in collaboration with researchers from the California Institute of Technology (USA).
We could also demonstrate a key role for jellyfish muscle fibers in initiating mouth regeneration following injury in Clytia. These data reinforce the first observations obtained in various animals on the unexpected role of muscles in the initiation of regenerative processes.

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Sinigaglia C, Peron S, Eichelbrenner J, Chevalier S, Steger J, Barreau C, Houliston E, Leclère L. 2020. Pattern regulation in a regenerating jellyfish. eLife 9:e54868.
elifesciences.org/articles/54868

Chari T, Weissbourd B, Gehring J, Ferraioli A, Leclère L, Herl M, Gao F, Chevalier C, Copley RR, Houliston E, Anderson DJ, Pachter L. 2021. Whole animal multiplexed single-cell RNA-Seq reveals plasticity of Clytia medusa cell types. BioRxiv 01.22.427844.
www.biorxiv.org/content/10.1101/2021.01.22.427844v1

In the hundreds of millions of years of animal evolution since the cnidarian lineages diverged from those of the bilaterian animals, body plans, anatomies and behaviors have diversified widely, but in all cases these features are underpinned by complex neuromuscular systems. To what extent these systems can be traced back to ancestral neuromuscular systems in a common ancestor, or arose convergently, is a key question in animal evolution. While nervous system evolution is starting to attract considerable attention, muscle evolution is relatively unexplored. This is in part due to the low number of tractable genetic models for studying muscle development and function amongst non-bilaterian species, with no detailed molecular functional characterization yet reported.

The objective of this project is to characterize - molecularly, structurally and functionally - muscle cell types in two complementary cnidarian species, in order to reconstruct the early evolution of muscle genes and muscle cell types. The two species – Clytia hemisphaerica and Pelagia noctiluca – belong to two medusae-forming clades showing distinct anatomical and developmental features. They both produce free-swimming jellyfish (medusae) which harbor rapid-contracting striated swimming muscles as well as slow-contracting smooth epitheliomuscular cell types. Clytia is already well established as a laboratory experimental species, and boasts a large range of molecular resources and efficient gene analysis techniques. The abundant Mediterranean jellyfish Pelagia is an emerging model which provides a rare example of medusa directly developing from the embryo, rather than asexually budding from an intermediate polyp stage, thus facilitating the study of its development.

This project is structured into 4 complementary tasks: (i) developing the scyphozoan Pelagia noctiluca as a functional model organism - generating culture laboratory strains, transcriptomic data and developing efficient functional methods, (ii) generating a comprehensive picture of the muscle cell types in Clytia and Pelagia life stages - integrating single cell transcriptomic data, in situ hybridization, cytological and ultrastructural data as well as physiological assays of contractility, (iii) characterizing the function of a selected array of structural muscle protein and transcription factors likely involved in myogenesis in Clytia and Pelagia, (iv) performing comparative analyses and reconstructing the early evolution of muscle cell types.

Not only does muscle provide a fascinating paradigm for animal cell type evolution, but understanding its origins is likely to have wider implications for our thinking about metazoan evolution. This project will further lay the foundation for future studies of medusa development, biology and ecology through the development of Pelagia as a new model species.