The development of adult muscles in Drosophila: ablation of identified muscle precursor cells

Abstract

A small subset of mesodermal cells continues to express twist in the late embryo of Drosophila. These cells are the precursors of adult muscles. Each late twist-expressing cell begins to divide early in the second larval instar and division continues throughout the second and third instars, resulting in a small clone of twist-expressing cells at puparium formation. Treatment with a DNA-synthesis inhibitor, hydroxyurea (HU), ablates these cells if applied during S-phase of their replication cycle. We ablated twist-expressing lineages in the larva and demonstrated that this results in the absence of subsets of muscles in the adult abdomen and leg. HU treatment during this larval period has no discernible effect on the adult epidermis or innervation. We conclude that the twist-expressing cells identified in the late embryo are the unique primordia of adult muscles. Each primordium is fated to establish 6–10 adult muscle fibres, defined here as a ‘muscle fibre group’. Each primordium has a unique fate and, after ablation, is not replaced by neighbouring cells. This unique fate does not rest with a particular founder cell within the primordium but is specified at the primordium level: ablation of a subset of cells within a muscle primordium does not result in an ablation of the resulting muscle group or in a decrease in the number of fibres within that muscle group, but rather results in a uniform decrease in the number of nuclei/fibres throughout the entire muscle. Thus, the twist-expressing primordia in the abdomen appear to be fated to give rise to a particular muscle group but act as an equivalent precursor pool in the formation of that muscle group. Our results permit the conclusion that specific muscle groups in the adult leg arise from restricted pools of twist-expressing adepithelial cells in the larval imaginal disc in a similar fashion. We conclude that the fate restriction of myoblast pools in early development defines elements of the final adult muscle pattern. The fate restriction of myoblast cells may be a result of genetic determination to form a specified muscle group or, alternatively, reflect the spatial isolation of otherwise equivalent cells to form muscle-specific precursor pools.