1. Logics and properties of a genetic regulatory program that drives embryonic muscle development in an echinoderm
- Author
-
Chih-Yu Pai, Carmen Andrikou, Maria Ina Arnone, and Yi-Hsien Su
- Subjects
Mesoderm ,Transcription, Genetic ,QH301-705.5 ,Science ,Gene regulatory network ,gene regulatory network ,Biology ,Muscle Development ,Models, Biological ,General Biochemistry, Genetics and Molecular Biology ,sea urchin ,Forkhead Transcription Factors ,medicine ,Transcriptional regulation ,Myocyte ,FGF ,Animals ,Gene Regulatory Networks ,Biology (General) ,Genetics ,Deuterostome ,General Immunology and Microbiology ,Myogenesis ,General Neuroscience ,other ,Gene Expression Regulation, Developmental ,General Medicine ,biology.organism_classification ,medicine.anatomical_structure ,Developmental Biology and Stem Cells ,specification ,Genomics and Evolutionary Biology ,Evolutionary biology ,Medicine ,myogenesis ,Developmental biology ,Research Article ,Forkhead ,Echinodermata - Abstract
Evolutionary origin of muscle is a central question when discussing mesoderm evolution. Developmental mechanisms underlying somatic muscle development have mostly been studied in vertebrates and fly where multiple signals and hierarchic genetic regulatory cascades selectively specify myoblasts from a pool of naive mesodermal progenitors. However, due to the increased organismic complexity and distant phylogenetic position of the two systems, a general mechanistic understanding of myogenesis is still lacking. In this study, we propose a gene regulatory network (GRN) model that promotes myogenesis in the sea urchin embryo, an early branching deuterostome. A fibroblast growth factor signaling and four Forkhead transcription factors consist the central part of our model and appear to orchestrate the myogenic process. The topological properties of the network reveal dense gene interwiring and a multilevel transcriptional regulation of conserved and novel myogenic genes. Finally, the comparison of the myogenic network architecture among different animal groups highlights the evolutionary plasticity of developmental GRNs. DOI: http://dx.doi.org/10.7554/eLife.07343.001, eLife digest Muscles, bones, and blood vessels all develop from a tissue called the mesoderm, which forms early on in the development of an embryo. Networks of genes control which parts of the mesoderm transform into different cell types. The gene networks that control the development of muscle cells from the mesoderm have so far been investigated in flies and several species of animals with backbones. However, these species are complex, which makes it difficult to work out the general principles that control muscle cell development. Sea urchins are often studied in developmental biology as they have many of the same genes as more complex animals, but are much simpler and easier to study in the laboratory. Andrikou et al. therefore investigated the ‘gene regulatory network’ that controls muscle development in sea urchins. This revealed that proteins called Forkhead transcription factors and a process called FGF signaling are crucial for controlling muscle development in sea urchins. These are also important factors for developing muscles in other animals. Andrikou et al. then produced models that show the interactions between the genes that control muscle formation at three different stages of embryonic development. These models reveal several important features of the muscle development gene regulatory network. For example, the network is robust: if one gene fails, the network is connected in a way that allows it to still make muscle. This also allows the network to adapt and evolve without losing the ability to perform any of its existing roles. Comparing the gene regulatory network that controls muscle development in sea urchins with the networks found in other animals showed that many of the same genes are used across different species, but are connected into different network structures. Investigating the similarities and differences of the regulatory networks in different species could help us to understand how muscles have evolved and could ultimately lead to a better understanding of the causes of developmental diseases. DOI: http://dx.doi.org/10.7554/eLife.07343.002
- Published
- 2015