A New Level of Plasticity: Drosophila Smooth-like Testes Muscles Compensate Failure of Myoblast Fusion

The testis of Drosophila resembles an individual testis tubule of mammals. Both are surrounded by a sheath of smooth muscles, which in Drosophila are multinuclear and originate from a pool of myoblasts that are set aside in the embryo and accumulate on the genital disc later in development. These muscle stem cells start to differentiate early during metamorphosis and give rise to all muscles of the inner male reproductive system. Shortly before the genital disc and the developing testes connect to each other, multinuclear nascent myotubes appear on the anterior tips of the seminal vesicles. Here we show that adhesion molecules were distinctly localized on the seminal vesicles; founder cell-like myoblasts (FC-like) expressed Dumbfounded (Duf) and Roughest (Rst), and fusion-competent myoblast-like cells (FCM-like) mainly expressed Sticks and stones (Sns). The smooth but multinuclear myotubes of the testes arose by myoblast fusion. RNAi-mediated attenuation of Sns or both Duf and Rst severely reduced the number of nuclei in the testes muscles. Duf and Rst likely acted independently in this context. Despite reduced fusion, myotubes migrated onto the testes, testes were shaped and coiled, muscle filaments arranged as in the wild-type, and spermatogenesis proceeded normally. Hence, the testes muscles compensated for fusion defects so that the myofibres encircling the adult testes are indistinguishable from those of the wild- type and male fertility is guaranteed.