Specification of the somatic musculature in Drosophila

Abstract

The somatic muscle system formed during Drosophila embryogenesis is required for larvae to hatch, feed, and crawl. This system is replaced in the pupa by a new adult muscle set, responsible for activities such as feeding, walking, and flight. Both the larval and adult muscle systems are comprised of distinct muscle fibers to serve these specific motor functions. In this way, the Drosophila musculature is a valuable model for patterning within a single tissue: while all muscle cells share properties such as the contractile apparatus, properties such as size, position, and number of nuclei are unique for a particular muscle. In the embryo, diversification of muscle fibers relies first on signaling cascades that pattern the mesoderm. Subsequently, the combinatorial expression of specific transcription factors leads muscle fibers to adopt particular sizes, shapes, and orientations. Adult muscle precursors (AMPs), set aside during embryonic development, proliferate during the larval phases and seed the formation of the abdominal, leg, and flight muscles in the adult fly. Adult muscle fibers may either be formed de novo from the fusion of the AMPs, or are created by the binding of AMPs to an existing larval muscle. While less is known about adult muscle specification compared to the larva, expression of specific transcription factors is also important for its diversification. Increasingly, the mechanisms required for the diversification of fly muscle have found parallels in vertebrate systems and mark Drosophila as a robust model system to examine questions about how diverse cell types are generated within an organism.

Acting on identity: Myoblast fusion and the formation of the syncytial muscle fiber

“…The adult muscle system forms during the pupal stage of development. In contrast to the larva, each single adult muscle is composed of multiple muscle fibers and thus more closely resembles the muscle organization found in vertebrate skeletal muscle (reviewed by Dobi et al, 2015, Taylor, 2006). This pertains in particular to the indirect flight muscles, the largest and best-studied muscle set of the adult fly.…”

“…In Drosophila , the allocation of somatic mesoderm depends on the crosstalk between the mesoderm and the ectoderm (Azpiazu et al, 1996; Frasch, 1995; Staehling-Hampton et al, 1994), as well as the combination of transcription factors that are expressed in the mesoderm (reviewed in Baylies et al, 1998; Dobi et al, 2015). After the allocation of the somatic mesoderm, the bHLH protein Lethal of Scute (L’sc) is expressed in clusters of promuscle cells (Figure 2A), under the control of the Receptor Tyrosine Kinase (RTK) pathway (Carmena et al, 1995).…”

“…This also holds true for nautilus , the fly ortholog of vertebrate MYOD, which is a key regulator of myogenic differentiation in Drosophila (Michelson et al, 1990; reviewed by (Abmayr and Keller, 1998)). As discussed below, Nautilus interacts with other transcription and chromatin regulators, and determines muscle identity, morphology, and size (reviewed in (Dobi et al, 2015)).…”

Rewiring of an ancestral Tbx1/10-Ebf-Mrf network for pharyngeal muscle specification in distinct embryonic lineages

“…Muscle identity is determined by the cooperation of Myf5, Mrf4 and MyoD (Braun et al, 1994;Summerbell et al, 2002;Kassar-Duchossoy et al, 2004), whereas myogenin is required for differentiation in all parts of the head and body (Nabeshima et al, 1993;Hasty et al, 1993). By contrast, MRF-family genes play a less central role in development of skeletal muscle-like muscles in various non-chordate clades (Andrikou and Arnone, 2015;Dobi et al, 2015;Moncaut et al, 2013). The sole Drosophila MRF-family homologue, nautilus (nau), is myogenic when expressed ectopically (Keller et al, 1997), but it is only expressed in a subset of founder cell myoblasts (Michelson et al, 1990), and it is required in vivo for founder cell patterning of the somatic musculature (Wei et al, 2007).…”

Diaphanous regulates SCAR complex localization during Drosophila myoblast fusion

“…When a na€ ıve FCM fuses with a FC, the newly added myonucleus is reprogrammed to adopt the founder cell nucleus identity, and another round of fusion is initiated. 6 During fusion, formation of an actin-rich focus occurs at the fusion site; 7,8 this actin focus provides an invasive force from the FCM into the FC/myotube, promoting fusion. 9 Actin polymerization at the fusion site is regulated by Arp2/3, a branched actin nucleating complex.…”