org Interactive Fly, Drosophila




bagpipe expression begins shortly after tinman at 4-6 hours after fertilization. In contrast to tin expression, which is continuous, bap expression is segmentally interrupted. The 11 patches of bap expression are located in the region of the mesoderm corresponding to parasegments 2-12 of the epidermis. This region will give rise to the visceral mesoderm. Expression ends at stage 11 approximately 2.5 hours after onset. In addition to the middle body region, bap is expressed in mesodermal cells of the proctodeum and stomodeum [Image] that will develop into visceral mesoderm of hindgut and foregut. Following stage 12, bap expression appears in a subset of heart progenitors. Only 30-40% of the bap-expressing cells develop into viseral mesoderm, and the remainder presumably give rise to somatic mesoderm.

Each of the somatic cell types of the gonad arises from mesodermal cells that constitute the embryonic gonad. The functions of the homeotic genes abdominal A and Abdominal B are both required for the development of gonadal precursors. Each plays a distinct role. abd A activity alone specifies anterior somatic gonadal precursor (SGP) fates, whereas abd A and Abd B act together to specify a posterior subpopulation of gonadal precursors. Once specified, gonadal precursors born within posterior parasegments move to the site of gonad formation. clift has been identified as a regulator of Drosophila gonadogenesis. Using clift as a marker, it has been shown that the anteroposterior and dorsoventral position of the somatic gonadal precursor cells within a parasegment are established by the secreted growth factor Wingless, acting from the ectoderm, coupled with a gene regulatory hierarchy involving abd A within the mesoderm. Initial dorsoventral positioning of somatic gonadal precursors relies on a regulatory cascade that establishes dorsal fates within the mesoderm. tinman appears to mediate the role of ectodermally expressed decapentaplegic; in tinman mutants few or no SGP cells are detected. clift expression is subsequently refined through negative regulation by bagpipe, a gene that specifies nearby visceral mesoderm (Boyle, 1997).

Fusion of Bagpipe-expressing visceral muscle precursors

The embryonic Drosophila midgut is enclosed by a latticework of longitudinal and circular visceral muscles. These muscles are syncytial. Like somatic muscles they are generated by the prior segregation of two populations of cells: fusion-competent myoblasts and founder myoblasts specialized to seed the formation of particular muscles. Visceral muscle founders are of two classes: those that seed circular muscles and those that seed longitudinal muscles. These specializations are revealed in mutant embryos where myoblast fusion fails. In the absence of fusion, founders make mononucleate circular or longitudinal fibers, while their fusion-competent neighbors remain undifferentiated (Martin, 2001).

Earlier descriptions of the midgut visceral muscles in flies reported that the fibers are mononucleate rather than syncytial. However, it has now been shown that dumbfounded (duf) and sticks and stones (sns), genes characteristically required for myoblast fusion, are both expressed in the visceral mesoderm of the midgut. Duf is an Ig domain protein that acts as a myoblast attractant (Ruiz-Gómez, 2000), while fusion-competent cells express a second Ig domain protein, Sns (Bour, 2000). In addition, the morphology of the midgut is abnormal in embryos mutant for genes that are required for myoblast fusion, including duf and sns. In such embryos the fore and hind gut appear relatively normal but the usual constrictions of the midgut fail to develop properly. Because of the apparent inconsistency between these findings and the earlier reports, the roles of duf and sns in the development of the midgut were investigated. The two genes are expressed in distinct, non-overlapping populations of cells. The following patterns of expression were detected. (1) A conspicuous population of cells migrates to the midgut from the region of the forming hindgut visceral mesoderm. These are the cells of the caudal visceral mesoderm that have previously been shown to express bHLH54F and to form the longitudinal visceral muscles of the midgut. At late stage 12, when these cells are distributed along the midgut primordium, they begin to express duf. (2) duf is also expressed in a continuous, undulating line of cells in the trunk mesoderm that have been described as the progenitors of the circular visceral muscles. (3) sns is expressed in a more extensive population abutting this line of duf-expressing cells. The ventrolateral margin of the sns domain is delimited by the continuous file of duf-expressing cells (Martin, 2001).

Populations (2) and (3) constitute the trunk visceral mesoderm and are derived from the clusters of dorsolateral bagpipe (bap)-expressing cells that move internally at stage 10. Initially these clusters appear uniform but by early stage 11 bap expression is downregulated in the more ventral marginal cells, and these cells become conspicuous by their orderly arrangement and their columnar morphology. These orderly marginal cells (the future duf-expressing cells) form a series of arches that border the looser aggregation of cells (the sns-expressing cells) that constitute the remainder of the original bap domain. Both populations of cells in the trunk visceral mesoderm are labelled by the expression of Fasciclin III (Fas III), with stronger expression in the columnar, duf-expressing cells of the margin. Later the marginal cells divide once in a predominantly dorsoventral orientation to produce a double file of duf-expressing cells delimiting the domain of their sns-expressing neighbors. This lineage for the columnar duf-expressing cells resembles the origin of sibling founders for somatic muscles by the division of muscle progenitor cells (Martin, 2001).

Taken together, these observations suggest that the columnar duf-expressing cells of the trunk visceral mesoderm and the migratory duf-expressing cells of the caudal visceral mesoderm are founders for circular and longitudinal muscles respectively, while the sns-expressing cells are a population of fusion-competent myoblasts contributing to both sets of muscles. To substantiate this idea the expression of hairy, a gene whose expression in the somatic mesoderm is limited to fusion-competent myoblasts, was examined. In the visceral mesoderm Hairy is confined to the loose aggregates of Fas III-expressing cells in the trunk visceral mesoderm. These are the cells that express sns. Hairy is not present in the immediately adjacent line of columnar, duf-expressing cells, nor is it in the migratory duf-expressing population of the caudal visceral mesoderm. To show that the hairy-expressing cells actually contribute to circular and longitudinal visceral muscles, advantage was taken of the perdurance of ß-gal expression driven by a hairy-ß-gal construct. This persistent expression confirms that hairy-positive nuclei are incorporated into both kinds of visceral muscles. It is concluded that the sns-expressing cells of the trunk visceral mesoderm are a population of fusion-competent myoblasts that contribute to both longitudinal and circular visceral muscle, while the duf-expressing cells of the trunk and caudal visceral mesoderm are two distinct populations of muscle founders that initiate the formation of circular and longitudinal muscles respectively (Martin, 2001).

In the somatic mesoderm, founder myoblasts express particular combinations of genes that endow these cells and the muscles they give rise to with unique characteristics. If the view that the duf-expressing cells are founder myoblasts for visceral muscle is correct, then it would be expected that localized patterns of gene expression in the visceral mesoderm would be initiated in these cells, and later spread to the syncytia that these cells seed. To test this idea the expression patterns of several genes known to be expressed in restricted domains of the circular midgut musculature was re-examined. Without exception it was found that expression for each of the genes analysed (connectin, wingless, decapentaplegic and abdominal-A) is initiated in a subset of the marginal columnar cells of the trunk visceral mesoderm. Expression later spreads to the full dorsoventral extent of the visceral muscles that these cells give rise to by fusion. In mutants where fusion fails expression remains confined to the columnar founder cells (Martin, 2001).

As the germ band retracts, the band of Fas III-expressing visceral myoblasts in the trunk visceral mesoderm shortens and begins to adopt the characteristic palisade-like morphology of the mature circular visceral muscles. The loose aggregates of Fas III/Hairy-expressing cells become closely apposed to their columnar neighbors which begin to elongate in a dorsoventral direction. Gradually cells are incorporated into the forming palisade of the circular visceral muscles. Fas III expression now reveals a single cell type, namely the elongating columns of immature circular visceral muscles. In mutants where myoblast fusion fails, these events are disrupted in a characteristic and informative way. Mutations in mbc appear to block fusion by interfering with events subsequent to the aggregation of fusion-competent myoblasts on founder cells. In the somatic mesoderm this is revealed as a phenotype where clusters of unfused myoblasts accumulate at sites where muscles would normally form. In the visceral mesoderm, the loose aggregates of Fas III-expressing myoblasts and their duf-expressing neighbors become closely apposed, but then fail to fuse. Mutations in duf and sns, however, interfere with myoblast aggregation and in the case of duf it is known that the protein acts as an attractant for fusion-competent myoblasts. In the visceral mesoderm of such mutants, both populations of Fas III-expressing myoblasts form, but they remain distinct as the germ band retracts and show no sign of the close adhesion between them that develops in wild-type embryos and in mutants of mbc. From this it is inferred that, as in the somatic mesoderm, duf expression in the columnar cells serves to attract the associated clusters of sns-expressing myoblasts prior to fusion occurring. Thus it appears that an exactly analogous sequence of events unfolds in the somatic and visceral mesoderm as a prelude to the formation of syncytial muscles. In both, two populations of myoblasts are formed: duf-expressing founders and sns-expressing fusion-competent cells. duf-expressing founders attract to them sns-expressing myoblasts, and if either gene is mutated this attractive mechanism fails. In mutants where later events in fusion are blocked, the two populations adhere tightly but do not fuse: this adhesion is evident in the somatic mesoderm as clusters of aggregated myoblasts and in the visceral mesoderm as the two closely apposed populations of cells that normally give rise to the palisade of circular visceral muscles. In addition, in non-fusion mutants, the duf-expressing visceral founders, like their somatic counterparts, continue to show specific patterns of gene expression and grow out with the appropriate orientations for the circular and longitudinal visceral muscles. In contrast their sns, hairy-expressing neighbors do not elongate and do not manifest specific patterns of gene expression (Martin, 2001).

An important point here is that these syncytial visceral muscle fibers represent a second population of muscles formed by myoblast fusion and therefore provide a test of the generality of the model for myotube formation that has been put forward for the somatic musculature. The somatic muscles consist of a remarkably diverse population of 30 different myotubes in each hemisegment of the body wall. Each myotube has its own specific set of characteristics, including its size, shape, sites of insertion on the body wall, and innervation by particular motorneurons. These properties of the syncytial myotubes seem to be largely dictated by the particular set of transcription factors expressed in each group of fused myoblasts as it differentiates to form a mature muscle fiber. These expression patterns derive from the specification of a single founder myoblast for each myotube. The specified founder attracts neighboring fusion-competent myoblasts to fuse with it and at the same time recruits these cells to its own characteristic patterns of gene expression (Martin, 2001).

The founders for the visceral longitudinal muscles originate in the region of the hindgut visceral mesoderm and migrate anteriorly. As they migrate they become oriented at right angles to the palisade of the circular muscles of the midgut and maintain this orientation as they begin to fuse, thus generating syncytial precursors of longitudinal muscles that are spread out over the entire territory of the forming midgut depending on the distance that each precursor has covered in its migration. By contrast, the founders of the circular muscles arise in situ, first as cells at the margin of the bap-expressing clusters that move inwards at stage 10 and later joining the marginal cells from neighboring clusters to form a continuous line of founders along the length of the future midgut. From this line of founders the palisade of circular muscles will arise as each syncytium grows out by extending in the dorsoventral axis. Because these cells arise along the length of the anteroposterior axis of the trunk, they potentially retain information as to their position in this axis and they acquire locally distinct patterns of gene expression. Some of these are repetitive, e.g., connectin, while others such as wg, dpp and abd-A are unique to particular regions of the embryo and endow the cells at these points, and the muscles they give rise to, with locally specific properties. Thus the overall class of circular founders and muscles is refined by the expression of such genes to produce a regionally variegated set of fibers whose distinctive characteristics are required for the proper patterning and morphogenesis of the midgut (Martin, 2001).

There appear to be distinct populations of founders and fusion-competent cells for the somatic and visceral muscles. However, this distinction is based solely on the locations of the cells and their patterns of gene expression. What evidence is there that the two populations are really separate and that mixing does not occur? As far as can be seen, mixing could only occur if somatic and visceral founders were able to recruit cells from each other's pools of fusion-competent myoblasts. It is thought unlikely that such mixing would occur in normal development because founders and fusion-competent cells arise in close proximity to each other, or in the case of the founders for longitudinal visceral muscles, migrate into the region of the visceral fusion-competent cells. Thus local interactions would ensure that fusion-competent myoblasts would only fuse with their immediately adjacent founders. However, it is known that the myoblast attractant Duf acts over distances of several cell diameters, thus in abnormal circumstances it might be possible for visceral myoblasts to be attracted to somatic founders, or vice versa. It could be that the expression of Fas III in the midgut visceral mesoderm tends to hold this population of cells together so that the likelihood of cells migrating away from the region of forming visceral muscles is reduced. At the same time it is observed that in even-skipped mutant embryos where the midgut visceral mesoderm of the trunk is absent, the bHLH54F-expressing founders of longitudinal muscles still develop and migrate into the region where the midgut would normally form. These cells however, remain mononucleate, despite the fact that they are adjacent to the pool of fusion-competent myoblasts from which somatic muscles will form. Thus in this instance at least there seems to be a block to the intermingling and fusion of cells across the two populations. Interestingly, the adhesive properties of the longitudinal visceral muscle founders seem to depend on their origin from a brachyenteron (byn)-expressing subset of the mesoderm. If byn is misexpressed throughout the mesoderm, the migration of the longitudinal founders is deranged and there is a generalized adhesion between somatic and visceral mesoderm cells, which makes them difficult to separate. Whether there is fusion between somatic and visceral myoblasts under these conditions is not clear. In general it is thought likely that there is a real barrier to mixing between the two cell populations, reflecting their very different origins in the embryo. Such barriers might be an important mechanism for partitioning the available population of myogenic cells between different muscle-forming tasks in the embryo (Martin, 2001).

In the two myogenic pathways, visceral and somatic, myotubes form as a result of the prior segregation of seed myoblasts and others that act as feeders. In such a myogenic pathway, the properties of each syncytium can be dictated autonomously by the patterns of gene expression specific to particular classes of founder cells. At the same time, the number of myotubes and the locations where they will be formed are set by the local specification of founder myoblasts. It is not known how general this model for myotube formation may be. The weight of evidence in vertebrates (where myotubes are far less diverse) might be taken to indicate that in these organisms myoblasts simply align together and fuse to form myotubes. One question that this model leaves unresolved is how the number and location of forming myotubes would be regulated in such a system. Control could be exerted if the initial step in the formation of a myotube were a seeding event analogous to those described in Drosophila. It would not be essential for such seeding events to be so tightly controlled as in the fly, nor would the initiating event necessarily be in a participating myoblast. In other organisms it could either be that the environment provides local cues for the initiation of fusion, or that contact with such a local cue renders one myoblast capable of seeding fusion with its neighbors. The possibility that such seeding events may be widespread and important is strengthened by the discovery of another such system in the fly (Martin, 2001).


Drosophila metamorphosis is characterized by diverse developmental phenomena, including cellular proliferation, tissue remodeling, cell migration, and programmed cell death. Cells undergo one or more of these processes in response to the hormone 20-hydroxyecdysone (ecdysone), which initiates metamorphosis at the end of the third larval instar and before puparium formation (PF) via a transcriptional hierarchy. Additional pulses of ecdysone further coordinate these processes during the prepupal and pupal phases of metamorphosis. Larval tissues such as the gut, salivary glands, and larval-specific muscles undergo programmed cell death and subsequent histolysis. The imaginal discs undergo physical restructuring and differentiation to form rudimentary adult appendages such as wings, legs, eyes, and antennae. Ecdysone also triggers neuronal remodeling in the central nervous system (White, 1999).

Wild-type patterns of gene expression in D. melanogaster during early metamorphosis were examined by assaying whole animals at stages that span two pulses of ecdysone. Microarrays were constructed containing 6240 elements that included more than 4500 unique cDNA expressed sequence tag (EST) clones along with a number of ecdysone-regulated control genes having predictable expression patterns. These ESTs represent approximately 30% to 40% of the total estimated number of genes in the Drosophila genome. In order to gauge expression levels, microarrays were hybridized with fluorescent probes derived from polyA+ RNA isolated from developmentally staged animals. The time points examined are relative to PF, which last approximately 15 to 30 min, during which time the larvae cease to move and evert their anterior spiracles. Nineteen arrays were examined representing six time points relative to PF: one time point before the late larval ecdysone pulse; one time point just after the initiation of this pulse (4 hours BPF), and time points at 3, 6, 9, and 12 hours after PF (APF). The prepupal pulse of ecdysone occurs 9 to 12 hours APF (White, 1999).

In order to manage, analyze, and disseminate the large amount of data, a searchable database was constructed that includes the average expression differential at each time point. The analysis set consists of all elements that reproducibly fluctuate in expression threefold or more at any time point relative to PF, leaving 534 elements containing sequences represented by 465 ESTs and control genes. More than 10% of the genes represented by the ESTs display threefold or more differential expression during early metamorphosis. This may be a conservative estimate of the percentage of Drosophila genes that change in expression level during early metamorphosis, because of the stringent criteria used for their selection (White, 1999).

To interpret these data, genes were grouped according to similarity of expression patterns by two methods. The first relied on pairwise correlation statistics, and the second relied on the use of self-organizing maps (SOMs). Differentially expressed genes fall into two main categories. The first category contains genes that are expressed at >18 hours BFP (before the late larval ecdysone pulse) but then fall to low or undetectable levels during this pulse. These genes are potentially repressed by ecdysone and make up 44% of the 465 ESTs identified in this set. The second category consists of genes expressed at low or undetectable levels before the late larval ecdysone pulse but then are induced during this pulse. These genes are potentially induced by ecdysone and make up 31% of the 465 ESTs. Consequently, 75% of genes that changed in expression by threefold or more do so during the late larval ecdysone pulse that marks the initial transition from larva to prepupa. This result is consistent with the extreme morphological changes that are about to occur in these animals. There are clearly discrete subdivisions of gene expression within these categories (White, 1999).

Gene expression changes during metamorphosis also foreshadow both larval muscle breakdown and adult myogenesis. At approximately 2 hours APF, the anterior larval musculature begins to break down. This breakdown lasts until approximately 6 hours APF. Genes encoding both structural and regulatory components of muscle formation are down-regulated as early as 4 hours BPF (see Muscle-specific genes regulated during metamorphosis). In addition to the repression of genes encoding components of thin and thick filaments, genes encoding other muscle-specific molecules are also repressed, including factors that compose the mesh in which these filaments lie and regulatory factors involved in the specification of muscle tissue. The mRNAs of all these repressed genes decrease substantially many hours before histolysis of the anterior larval muscles and therefore predict the occurrence of this morphological event well before it begins. Twenty-four hours APF, adult myogenesis is well underway. The genes DMef-2, bagpipe, and tinman are all up-regulated at 12 hours APF from the baseline at PF, coincident with the prepupal pulse of ecdysone. It is suggested that induction of these regulatory factors initiates the development of the adult musculature, which will establish itself several hours later (White, 1999).

Effects of Mutation or Deletion

In embryos mutant for bap, visceral mesoderm formation is strongly disrupted. Most cells of the visceral mesoderm fail to differentiate properly, and a portion of them are transformed into body wall musculature and gonadal mesoderm. In tin mutant embryos, bap expression is not activated in the dorsal mesoderm (Azpiazu, 1993).

The tinman and bagpipe genes are members of the NK homeobox gene family of Drosophila, so that tin occupies a higher position than bap in the regulatory hierarchy. Little is known about the level and pattern of genetic polymorphism in homeobox genes. Nucleotide polymorphism was analyzed in 27 strains of Drosophila melanogaster and one each of D. simulans and D. sechellia, within two closely linked regions encompassing a partial sequence of tin and the complete sequence of bap. The two genes exhibit different levels and patterns of nucleotide diversity. Two sets of sharply divergent sequence types are detected for tin. The haplotype structure of bap is more complex: about half of the sequences are identical (or virtually so), while the rest are fairly heterogeneous. The level of silent nucleotide variability is 0.0063 for tin but significantly higher, 0.0141, for bap, a level of polymorphism comparable to the most polymorphic structural genes of D. melanogaster. Recombination rate and gene conversion are also higher for bap than for tin. There is strong linkage disequilibrium, with the highest values in the introns of both genes and exon II of bap. The patterns of polymorphism in tin and bap are not compatible with an equilibrium model of selective neutrality. It is suggested that negative selection and demographic history are the major factors shaping the pattern of nucleotide polymorphism in the tin and bap genes; moreover, there are clear indications of positive selection in the bap gene (Balakireva, 2004).


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bagpipe: Biological Overview | Evolutionary Homologs | Regulation | Developmental Biology | Effects of Mutation

date revised: 20 June 2012

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