Muscle cell type evolution and development – MYODEVO

The project is structured around four complementary axes:
1. Development of Pelagia noctiluca as a functional model: establishment of lab-maintained lines, generation of transcriptomic data, and optimization of gene disruption approaches.
2. Characterization of muscle types in Clytia and Pelagia through single-cell transcriptomic analyses, in situ hybridization, cytological and ultrastructural observations, and contractility measurements.
3. Functional analysis of key genes: investigation of the role of genes encoding structural muscle proteins and transcription factors involved in myogenesis in Pelagia.
4. Evolutionary comparison: comparative analyses to reconstruct the evolution of muscle cell types and propose an evolutionary scenario for muscles in cnidarians.

Major Project Findings:

• Demonstration of a key role for muscle fibers in initiating oral regeneration after injury in Clytia hemisphaerica.
• Detailed characterization of the molecular architecture of sarcomeres in juvenile Pelagia noctiluca, particularly the organization of the actomyosin complex in striated muscles.
• Identification and functional validation of several essential molecular regulators of sarcomere assembly, leading to the proposal of an original evolutionary scenario for striated muscles in cnidarians.

These studies make a significant contribution to our understanding of the evolution of muscle and cellular systems in metazoans.

The project has resulted in eight scientific publications.

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.