The formation of syncytia within the visceral musculature of the Drosophila midgut is dependent on duf, sns and mbc.
The visceral musculature of the Drosophila midgut consists of an inner layer of circular and an outer layer of longitudinal muscles. Here, we show that the circular muscles are organised as binucleate syncytia that persist through metamorphosis. At stage 11, prior to the onset of the fusion processes, we detected two classes of myoblasts within the visceral trunk mesoderm. One class expresses the founder-cell marker rP298-LacZ in a one- to two-cells-wide strip along the ventralmost part of the visceral mesoderm, whereas the adjacent two to three cell rows are characterised by the expression of Sticks-and-stones (SNS). During the process of cell fusion at stage 12 SNS expression decreases within the newly formed syncytia that spread out dorsally over the midgut. At both margins of the visceral band several cells remain unfused and continue to express SNS. Additional rP298-LacZ-expressing cells arise from the posterior tip of the mesoderm, migrate anteriorly and eventually fuse with the remaining SNS-expressing cells, generating the longitudinal muscles. Thus, although previous studies proposed a separate primordium for the longitudinal musculature located at the posteriormost part of the mesoderm anlage, our cell lineage analyses as well as our morphological observations reveal that a second population of cells originates from the trunk mesoderm. Mutations of genes that are involved in somatic myoblast fusion, such as sns, dumbfounded (duf) or myoblast city (mbc), also cause severe defects within the visceral musculature. The circular muscles are highly unorganised while the longitudinal muscles are almost absent. Thus the fusion process seems to be essential for a proper visceral myogenesis. Our results provide strong evidence that the founder-cell hypothesis also applies to visceral myogenesis, employing the same genetic components as are used in the somatic myoblast fusion processes.
Klapper
Robert
R
Institut für Allgemeine Zoologie und Genetik der Westfälischen Wilhelms-Universität, Schlossplatz 5, 48149 Münster, Germany. klapper@nwz.uni-muenster.de
Stute
Christiana
C
Schomaker
Oliver
O
Strasser
Thomas
T
Janning
Wilfried
W
Renkawitz-Pohl
Renate
R
Holz
Anne
A
D000818:Animals; D030801:Animals, Genetically Modified; D002459:Cell Fusion; D003598:Cytoskeletal Proteins; D004064:Digestive System / Q000254:growth & development; D004330:Drosophila / Q000235:genetics* / Q000254:growth & development*; D029721:Drosophila Proteins / Q000235:genetics; D018507:Gene Expression Regulation, Developmental; D017344:Genes, Insect; D015726:Giant Cells; D049452:Green Fluorescent Proteins; D007136:Immunoglobulins / Q000235:genetics; D019476:Insect Proteins / Q000235:genetics; D007763:Lac Operon; D008164:Luminescent Proteins / Q000235:genetics; D008565:Membrane Proteins; D009124:Muscle Proteins; D009130:Muscle, Smooth / Q000254:growth & development; D009154:Mutation; D011994:Recombinant Proteins / Q000235:genetics
D003598:Cytoskeletal Proteins; D029721:Drosophila Proteins; D007136:Immunoglobulins; D019476:Insect Proteins; D008164:Luminescent Proteins; D008565:Membrane Proteins; D009124:Muscle Proteins; D011994:Recombinant Proteins; C410904:SNS protein, Drosophila; C413082:kirre protein, Drosophila; C107441:mbc protein, Drosophila; D049452:Green Fluorescent Proteins