Cnidarian muscle development

The evolution of muscles was a fundamental invention in animal evolution, as it allowed animals to move, disperse, react by contraction to changes of the environment, catch prey, flee predators, thus, show any sort of behavior. Muscles generally arise by differentiation of the mesoderm, the third germ layer. While a great deal is known about the composition and development of bilaterian muscles, in particular in vertebrates, our knowledge about muscle development at the base of the animal tree is scarce. In the basal metazoan Cnidaria, the outgroup to the Bilateria, both smooth and striated-like muscles can be found, despite the fact that they lack a mesoderm. It is unclear, however, how bilaterian and cnidarian muscles are related. To address this question, we seek to understand the evolution of mesoderm and in particular muscle tissue during early animal evolution by investigating muscle development in two new cnidarian model systems, the sea anemone Nematostella vectensis (Anthozoa) and the medusozoan Clytia hemispherica (Hydrozoa). We have developped tools and resources to address these questions for the first time in cnidarians on a genetic and functional molecular level. With the genome sequence and extensive ESTs at hand we have isolated all structural components of smooth and striated muscles in these two cnidarians as well as putative crucial regulators of muscle development. Using a combination of classical methods and tools recently established in our lab, such as transgenic animals and gene knockdown techniques we will carry out a thorough analysis of the regulatory developmental circuitry and structural composition of cnidarian muscles, and compare this with existing knowledge in bilaterian species. We expect that our findings will shed light into the evolutionary origin of muscles at the base of the animal kingdom and how muscles can differentiate in the absence of mesoderm.

Muscles are an evolutionary innovation found only in animals. The emergence of muscles allowed them to escape or hunt, forage, disperse and explore new environments and find sex partners. Muscle cells, in particular the striated muscles are highly structured and are considered a complex cell type consisting of numerous proteins that have to interact in specific manners in order to maintain the structure and the contractibility. Yet, how muscles evolved is still unclear. To this end, we examined 22 fully sequenced genomes ranging from representative animals, fungi, protists and plants to trace the evolutionary origin of 47 muscle-specific proteins characterized in vertebrates or insects. We found that many proteins predate the origin of animals and are even found in protists, fungi or plants, whereas others originated relatively recently in specific animal lineages. Notably, several proteins that are crucially important for the structure or function of striated muscles in vertebrates and insects are absent from the genome of basal animals, like sea anemones and jellyfish. On the other hand, one of the crucial contractile proteins of striated muscles, the striated type myosin arose by a gene duplication that predated the origin of animals. This myosin has been maintained in all animals, even in those which do not have muscles, like sponges. Expression analysis of these genes in two cnidarians (a sea anemone and a medusa) and two sponges suggests that the striated type myosin is always expressed in fast-contracting cells. In conclusion, our studies strongly suggested that striated muscle cells have arisen independently in cnidarians and other animals - on the basis of an ancestral core set of proteins that predates the origin of animals. We also investigated the structure, development and anatomy of smooth and striated muscles in the sea anemone Nematostella vectensis and the medusa Clytia hemisphaerica. We found that retractor muscles of the body column in the sea anemone maintains a myoepithelial organisation, while those from the tentacle detach from the epithelium and take on a mesenchymal position, similar to muscles in vertebrates and insects. In the jellyfish, the muscle-bearing subumbrella does not, as commonly believed, derive from an expansion of the mouth field of the polyp, but rather from a fusion of four 4 tentacle anlagen during the budding process. We further revealed that the early medusa uses the same genetic toolkit that is used to make a polyp. Hence, medusa formation results from a modification of the developmental program in the polyp. We thus propose that medusa could evolve relatively easily from polyps.