Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

• Published in: Developmental biology 2016-12, Vol.420 (1), p.43-59
• Main Authors: Aghajanian, Patrick, Takashima, Shigeo, Paul, Manash, Younossi-Hartenstein, Amelia, Hartenstein, Volker
• Format: Article
• Language: English
• Subjects: Animals; Basement Membrane - metabolism; Cell Dedifferentiation; Cell Proliferation; Clone Cells; Drosophila; Drosophila melanogaster - growth & development; Drosophila melanogaster - ultrastructure; Intestine; Intestines - cytology; Intestines - growth & development; Intestines - ultrastructure; Larva - growth & development; Lineage; Metamorphosis; Metamorphosis, Biological; Morphogenesis; Muscles - metabolism; Muscles - ultrastructure; Myoblasts - cytology; Stem Cells - cytology; Stem Cells - metabolism; Viscera - growth & development; Viscera - ultrastructure; Visceral muscle
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2016.10.011

The visceral musculature of the Drosophila intestine plays important roles in digestion as well as development. Detailed studies investigating the embryonic development of the visceral muscle exist; comparatively little is known about postembryonic development and metamorphosis of this tissue. In this study we have combined the use of specific markers with electron microscopy to follow the formation of the adult visceral musculature and its involvement in gut development during metamorphosis. Unlike the adult somatic musculature, which is derived from a pool of undifferentiated myoblasts, the visceral musculature of the adult is a direct descendant of the larval fibers, as shown by activating a lineage tracing construct in the larval muscle and obtaining labeled visceral fibers in the adult. However, visceral muscles undergo a phase of remodeling that coincides with the metamorphosis of the intestinal epithelium. During the first day following puparium formation, both circular and longitudinal syncytial fibers dedifferentiate, losing their myofibrils and extracellular matrix, and dissociating into mononuclear cells (“secondary myoblasts”). Towards the end of the second day, this process is reversed, and between 48 and 72h after puparium formation, a structurally fully differentiated adult muscle layer has formed. We could not obtain evidence that cells apart from the dedifferentiated larval visceral muscle contributed to the adult muscle, nor does it appear that the number of adult fibers (or nuclei per fiber) is increased over that of the larva by proliferation. In contrast to the musculature, the intestinal epithelium is completely renewed during metamorphosis. The adult midgut epithelium rapidly expands over the larval layer during the first few hours after puparium formation; in case of the hindgut, replacement takes longer, and proceeds by the gradual caudad extension of a proliferating growth zone, the hindgut proliferation zone (HPZ). The subsequent elongation of the hindgut and midgut, as well as the establishment of a population of intestinal stem cells active in the adult midgut and hindgut, requires the presence of the visceral muscle layer, based on the finding that ablation of this layer causes a severe disruption of both processes. •Drosophila visceral muscle fibers directly descends from larval fibers.•Larval visceral muscles dedifferentiate into “secondary myoblasts”, losing their myofibrils and extracellular matrix.•Secondary myoblasts re-