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

Abstract

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, multinuclear nascent myotubes appear on the anterior tips of the seminal vesicles. Here, we show that adhesion molecules are distinctly localized on the seminal vesicles; founder cell (FC)-like myoblasts express Dumbfounded (Duf) and Roughest (Rst), and fusion-competent myoblast (FCM)-like cells mainly express 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 probably act independently in this context. Despite reduced fusion in all of these RNAi-treated animals, myotubes migrated onto the testes, testes were shaped and coiled, muscle filaments were arranged as in the wild type and spermatogenesis proceeded normally. Hence, the testes muscles compensate for fusion defects so that the myofibres encircling the adult testes are indistinguishable from those of the wild type and male fertility is guaranteed.

Expression of Hbs, Kirre, and Rst during Drosophila ovarian development

“…This phenomenon is often associated with overlapping expression patterns that in processes such as myoblast fusion and eye development allow them, at least in part, to functionally substitute for each other (Strünkelnberg et al, ; Shelton et al, ; Bao et al, ; Machado et al, ). Investigation of IRM involvement in Drosophila gonadal development have so far been limited to their role in myoblast fusion of multinucleated smooth‐like muscle fibers that enclose the testis (Susic‐Jung et al, ; Kuckwa et al, ). In this developmental scenario, although all four genes appear to be required for muscle precursor fusion, their precise mode of action might not be identical to the one extensively characterized in both embryonic and adult somatic myogenesis (Gildor et al, ; Önel et al, ).…”

“…In this developmental scenario, although all four genes appear to be required for muscle precursor fusion, their precise mode of action might not be identical to the one extensively characterized in both embryonic and adult somatic myogenesis (Gildor et al, ; Önel et al, ). Particularly rst and kirre seem to act agonistically, rather than redundantly during myotube generation in the testis (Kuckwa et al, ). The complementary expression patterns of these two genes, presented here, also suggest a cooperative, instead of redundant, function during ovarian development, although direct functional evidence for this is still lacking.…”

Myotube migration to cover and shape the testis ofDrosophiladepends on Heartless, Cadherin/Catenin, and myosin II

“…During metamorphosis, the genital disc and pupal testes grow towards each other, and the developing seminal vesicles fuse with the terminal epithelium of the testes ( Kozopas et al, 1998 ; Nanda et al, 2009 ; Stern, 1941 ). Nascent myotubes migrate over the developing seminal vesicles onto the pupal testes and build the muscle sheath surrounding the adult testis ( Kozopas et al, 1998 ; Kuckwa et al, 2016 ). This musculature is composed of multinucleated, smooth-like myofibers ( Susic-Jung et al, 2012 ).…”

“…1 A). Founder-cell-like (FC-like) myoblasts and fusion-competent-myoblast-like (FCM-like) cells start to fuse around 28 h after puparium formation (APF) to build multinucleated myotubes ( Kuckwa et al, 2016 ). Around 30 h APF, the multinucleated nascent myotubes begin to migrate from the genital disc towards the testis, contact the gonad at the distal end, and migrate further to cover the entire testis ( Fig.…”

“…Around 30 h APF, the multinucleated nascent myotubes begin to migrate from the genital disc towards the testis, contact the gonad at the distal end, and migrate further to cover the entire testis ( Fig. 1 A′) ( Kozopas et al, 1998 ; Kuckwa et al, 2016 ). Migration of testis myotubes is independent of successful fusion of testis-relevant myoblasts ( Kuckwa et al, 2016 ).…”