Intrinsic control of muscle attachment sites matching.

Alexandre Carayon,Yannick Carrier,Jean-Louis Frendo,Laetitia Bataillé,Antoine Wystrach,Alain Vincent,Aurore Pelletier,Gaëlle Lebreton,Laurence Dubois

doi:10.7554/elife.57547

Abstract

Myogenesis is an evolutionarily conserved process. Little known, however, is how the morphology of each muscle is determined, such that movements relying upon contraction of many muscles are both precise and coordinated. Each Drosophila larval muscle is a single multinucleated fibre whose morphology reflects expression of distinctive identity Transcription Factors (iTFs). By deleting transcription cis-regulatory modules of one iTF, Collier, we generated viable muscle identity mutants, allowing live imaging and locomotion assays. We show that both selection of muscle attachment sites and muscle/muscle matching is intrinsic to muscle identity and requires transcriptional reprogramming of syncytial nuclei. Live-imaging shows that the staggered muscle pattern involves attraction to tendon cells and heterotypic muscle-muscle adhesion. Unbalance leads to formation of branched muscles, and this correlates with locomotor behavior deficit. Thus, engineering Drosophila muscle identity mutants allows to investigate, in vivo, physiological and mechanical properties of abnormal muscles.

Highlights

The musculature of each animal is composed of an array of body wall muscles allowing precision and stereotypy of movements
founder cell (FC) originate from asymmetric division of progenitor cells (PCs) themselves selected from equivalence groups of myoblasts, called promuscular clusters (PMCs)
It is subsequently maintained in two PCs, one FC, the DA3 FC, and is activated in fusion-competent myoblasts (FCMs) nuclei recruited into the DA3 growing fibre (Crozatier and Vincent, 1999; Figure 1A)

Summary

Introduction

The musculature of each animal is composed of an array of body wall muscles allowing precision and stereotypy of movements. Carayon et al managed to selectively deactivate Collier in just one muscle per body section in the larvae of fruit flies This showed that the transcription factor is needed throughout muscle development; in particular, it is required for muscle fibres to select the correct attachment sites, and to be properly oriented. Removal of an auto-regulatory cis-module located in L-CRM abolishes col activation in syncytial nuclei fusing with the DA3 FC This leads to incomplete DA3 transformations and the formation of bifid/ branched muscles of mixed DA3/DA2 morphology. Our data show that i) the FC transcriptional program must be propagated to syncytial nuclei for a muscle to adopt a specific morphology; ii) the precise matching of muscle/muscle attachments over the intersegmental border, which leads to a staggered rows pattern, involves a process of selective adhesion controlled by iTFs; iii) branched muscles affect larval locomotion performance.

Results

Discussion

Materials and methods

Funding Funder