Abstract
BackgroundA stereotyped array of body wall muscles enables precision and stereotypy of animal movements. In Drosophila, each syncytial muscle forms via fusion of one founder cell (FC) with multiple fusion competent myoblasts (FCMs). The specific morphology of each muscle, i.e. distinctive shape, orientation, size and skeletal attachment sites, reflects the specific combination of identity transcription factors (iTFs) expressed by its FC. Here, we addressed three questions: Are FCM nuclei naive? What is the selectivity and temporal sequence of transcriptional reprogramming of FCMs recruited into growing syncytium? Is transcription of generic myogenic and identity realisation genes coordinated during muscle differentiation?ResultsThe tracking of nuclei in developing muscles shows that FCM nuclei are competent to be transcriptionally reprogrammed to a given muscle identity, post fusion. In situ hybridisation to nascent transcripts for FCM, FC-generic and iTF genes shows that this reprogramming is progressive, beginning by repression of FCM-specific genes in fused nuclei, with some evidence that FC nuclei retain specific characteristics. Transcription of identity realisation genes is linked to iTF activation and regulated at levels of both transcription initiation rate and period of transcription. The generic muscle differentiation programme is activated independently.ConclusionsTranscription reprogramming of fused myoblast nuclei is progressive, such that nuclei within a syncytial fibre at a given time point during muscle development are heterogeneous with regards to specific gene transcription. This comprehensive view of the dynamics of transcriptional (re)programming of post-mitotic nuclei within syncytial cells provides a new framework for understanding the transcriptional control of the lineage diversity of multinucleated cells.
Highlights
A stereotyped array of body wall muscles enables precision and stereotypy of animal movements
fusion competent myoblast (FCM) are naive myoblasts One key step in generating the stereotyped Drosophila skeletal muscle pattern is the specification of muscle progenitor cell (PC) and founder cell (FC) identity
All myoblasts in a given cluster express some identity transcription factor (iTF) in response to positional information. iTF expression is maintained in PCs and some FCs, while lost in FCMs (Fig. 1A) [16]
Summary
A stereotyped array of body wall muscles enables precision and stereotypy of animal movements. In Drosophila, each syncytial muscle forms via fusion of one founder cell (FC) with multiple fusion competent myoblasts (FCMs). The musculature of each animal species is composed of a complex array of body wall muscles that enable precise and stereotypic movements. Muscle formation involves fusion of mononucleated myoblasts. The coupling of muscle differentiation with multinucleation raises the general question of transcriptional (re)-programming of nuclei within a syncytium. Each muscle develops by fusion of one founder cell (FC) with a given number of fusion competent myoblasts (FCMs) [1]. Drosophila muscle development involves the mandatory asymmetric fusion of two cell types that display intrinsically different gene expression programmes.
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