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PubMed2001

SNARE-dependent signaling at the Drosophila wing margin.

The wing of Drosophila melanogaster has long been used as a model system to characterize intermolecular interactions important in development. Implicit in our understanding of developmental processes is the proper trafficking and sorting of signaling molecules, although the precise mechanisms that regulate membrane trafficking in a developmental context are not well studied. We have therefore chosen the Drosophila wing to assess the importance of SNARE-dependent membrane trafficking during development. N-Ethylmaleimide-sensitive fusion protein (NSF) is a key component of the membrane-trafficking machinery and we constructed a mutant form of NSF whose expression we directed to the developing wing margin. This resulted in a notched-wing phenotype, the severity of which was enhanced when combined with mutants of VAMP/Synaptobrevin or Syntaxin, indicating that it results from impaired membrane trafficking. Importantly, we find that the phenotype is also enhanced by mutations in genes for wingless and components of the Notch signaling pathway, suggesting that these signaling pathways were disrupted. Finally, we used this phenotype to conduct a screen for interacting genes, uncovering two Notch pathway components that had not previously been linked to wing development. We conclude that SNARE-mediated membrane trafficking is an important component of wing margin development and that dosage-sensitive developmental pathways will act as a sensitive reporter of partial membrane-trafficking disruption.

Animals↗
PubMed2002

Localization of ecdysone receptor protein during colour pattern formation in wings of the butterfly Precis coenia (Lepidoptera: Nymphalidae) and co-expression with Distal-less protein.

Butterfly wing colour patterns are determined during late larval and early pupal development, a part of metamorphosis controlled by ecdysteroid hormones via their nuclear hormone receptors. We have sequenced a fragment of the common regions of the ecdysone receptor (EcR) from the butterflies Precis coenia and Bicyclus anynanaand found high identities (83.5% to 100%) to EcR from a moth, Manduca sexta. In P. coenia, we sequenced a putative EcR-B1 isoform with 80.4% identity with the A/B-region of the M. sexta-EcR-B1. Consequently, we used antibodies generated against MsEcR-B1 to localise EcR protein during wing development of P. coenia. Nuclear staining of EcR was observed in different cell types during the course of colour pattern formation. Major observations are as follows: EcR is expressed in cell nuclei corresponding to wing lacunae and prospective veins. EcR is expressed early in pupal wing development in "focal" cells which are thought to release determining signals in a process leading to eyespot formation. Scale forming cells differentiate first and show EcR signal in the eyespot foci and most of the wing sheet, but not in areas corresponding to prospective eyespots. In the eyespots, 20-24 h after pupation, EcR expression seems to play a role in formation of scale rows preceding a later expression (28 h) in scale-forming cells. The results demonstrate that EcR is locally expressed in correlation to all major events of wing development and colour pattern formation. In particular, EcR expression patterns in prospective eyespots show that these are special pattern elements which are specified in concert with other factors of colour pattern formation such as the transcription factor Distal-less. In eyespot foci, Distal-less is expressed simultaneously with EcR, but clearly precedes EcR expression in eyespot scale-forming cells. This indicates a potential interaction between "short-range" signalling systems and "long-range" hormonal systems.

Amino Acid Sequence↗
PubMed2005

Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae).

We here show an example of morphological novelties, which have evolved from insect wings into the specific structures controlling social behaviour in an ant species. Most ant colonies consist of winged queen(s) and wingless workers. In the queenless ponerine ant Diacamma sp. from Japan, however, all female workers have a pair of small thoracic appendages, called "gemmae", which are homologous to the forewings and acts as an organ regulating altruism expression. Most workers, whose gemmae are clipped off by other colony members, become nonreproductive helpers, while only a single individual with complete gemmae becomes functionally reproductive. We examined histologically the development of gemmae, and compared it with that of functional wings in males. Female larvae had well-developed wing discs for both fore- and hindwings. At pupation, however, the wing discs started to evaginate and later degenerate. The hindwing discs completely degenerated, while the degeneration of forewing discs was incomplete, leading to the formation of gemmae. The degeneration process involved apoptotic cell death as confirmed by TUNEL assay. In addition, glandular cells differentiated from the epithelial cells of the forewing buds after completion of pupation. The mechanism of developmental transition from wing to gemma can be regarded as an evolutionary gain of new function, which can be seen in insect appendages and vertebrate limbs.

Animals↗
PubMed2001

Ecdysteroid-induced programmed cell death and cell proliferation during pupal wing development of the silkworm, Bombyx mori.

The wing margin of adult wings of Lepidoptera is defined by the position of a "bordering lacuna"(BL). During adult wing development, cell proliferation and scale formation proximal to this lacuna and programmed cell death distal to the lacuna are generally observed. To determine the effect of 20-hydroxyecdysone (20E) on these events, we cultured the silkworm pupal wings with or without 20E and analyzed regional specificity for cell death by the TUNEL method and cell proliferation by 5-bromodeoxyuridine labeling. Programmed cell death was induced by 20E after 5 days of culture and was detected only in the region distal to BL. Cell proliferation after 1 day of culture and scale formation after 5 days of culture were also inducible by 20E and detected in the region proximal to BL. These results suggest that two types of pupal wing cells, which are divided by the position of the BL, respond to ecdysteroid in different manners. Higher concentrations of 20E (more than 1,000 ng/ml) repressed the scale formation, while such repression could not be observed in the peripheral cell death even with 5,000 ng/ml 20E. The ecdysteroid may work both as a trigger to make the wing margin and scales and as a developmental timer to arrange these cellular responses.

Animals↗
PubMed2000

Multiple roles of the Dcdc42 GTPase during wing development in Drosophila melanogaster.

The Rho sub-family of GTPases, comprising Rho, Rac and Cdc42. regulates many biological processes, including morphogenesis, cell polarity, migration, the cell cycle and gene expression. It is important to develop genetic approaches to allow the dissection, in vivo, of the mechanisms of GTPase regulation and signal transmission, and their biological consequences. In this regard, wing development in Drosophila melanogaster is an excellent model system. To investigate the functions of the Drosophila Cdc42 GTPase (Dcdc42), we generated phenotypes during wing development, by expression of the dominant-negative N17 and L89 mutants of Dcdc42. We have identified roles for Dcdc42 in wing growth, and in cell fate choice during the development of the wing veins and the peripheral nervous system. Reduction of Dcdc42 signalling following over-expression of Dcdc42N17 resulted in a broader but more diffuse domain characterised by wing-margin sensory bristles. This was correlated with a broadened stripe of wingless expression along the dorsal-ventral boundary of third-instar wing imaginal discs. Together with genetic interactions with loss- and gain-of-function Notch alleles, these data support a role for wild-type Dcdc42 as a negative regulator of Notch signalling.

Animals↗
PubMed2000

The Drosophila dominant wing mutation Dichaete results from ectopic expression of a Sox-domain gene.

The dominant Drosophila wing mutation Dichaete is characterised by the deletion of proximal wing structures. By analysing a number of new Dichaete alleles, phenotypic revertants and enhancer piracy lines, we show that the wing phenotype results from ectopic expression of the Sox-domain gene Dichaete. Ectopic expression of the Sox gene results in an increase in cell death in the proximal region of the wing imaginal disc and leads to alterations in the normal expression of wingless. Since ectopic expression of wingless in the proximal region of the wing disc can rescue aspects of the Dichaete phenotype, it is likely that Dichaete specifically interferes with the establishment or maintenance of a critical domain of wingless expression in the wing disc.

Alleles↗
PubMed1983

Neuronal pathfinding in developing wings of the moth Manduca sexta.

The neural pattern of the moth wing is a simple two-dimensional network nestled between the two epithelial monolayers that form the upper and lower surfaces of the wing. All neural elements within the wing blade are sensory and their axons grow proximally toward the mesothoracic ganglion. The sensory nerves of the wing are intimately associated with the basal lamina of the upper epithelial layer; and the molding of neural pattern is coupled with cues in the basal lamina. The global landscape of the basal lamina can be altered by exchange of epithelial grafts. Axons generally cross control grafts as well as grafts that have been displaced distally. However, axons generally avoid grafts that have been transposed proximally. This asymmetric response of growing axons implies that directional cues in the substratum are also asymmetric along the length of the wing. The asymmetric, graded distribution of extracellular matrix molecules associated with the basal lamina of the wing's upper epithelium could provide the short-range cues that guide sensory axons in a particular direction.

Animals↗
PubMed1992

Dynamic expression of a cell surface protein during rearrangement of epithelial cells in the Manduca wing monolayer.

The expression of cell surface protein 2F5 changes dynamically in space and time during morphogenesis of the Manduca wing pattern. Two cell types (generalized epithelial cells and scale precursors) rearrange within each of the two epithelial monolayers of the wing to form periodic rows of scale cells. These two monolayers also interact with each other during a brief period of adult development. Each cell type shows a different pattern of protein 2F5 expression during cell rearrangement and during interaction of the two wing monolayers. Before and after these morphogenetic movements of epithelial cells, the protein is expressed on only a small population of wing cells. In abdominal epithelia where scale cells are also present but are not arranged in periodic rows, the expression pattern of the surface protein is temporally and spatially very different. An earlier study (Nardi and Magee-Adams, Dev. Biol., 116, 278-290, 1986) had shown that basal processes only extend from epithelial cells during their period of rearrangement within a monolayer and during the transient apposition of the wing's upper and lower monolayers. The differential distribution of protein 2F5 on lateral surfaces and basal processes of scale precursor cells and generalized epithelial cells may account in part for their orderly segregation into alternating rows as well as for the transient interaction of the two wing monolayers.

Amino Acid Sequence↗
PubMed1990

Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary.

Previous analyses of the decapentaplegic (dpp) gene in Drosophila melanogaster have suggested that its product, a polypeptide of the transforming growth factor-beta family of secreted factors, acts at the level of intercellular communication to control several events in spatial pattern formation. In this report, we use clonal analysis to demonstrate a localized requirement for wild-type dpp expression along the anterior-posterior (A/P) compartment boundary of the developing wing primordium. Clonal analysis reveals that normal wing blade development is solely dependent on dpp+ function in those anterior compartment cells that border the anterior-posterior (A/P) compartment boundary of the wing imaginal disk. Conversely, the wing blade will not develop if these boundary cells lack dpp activity. The localized requirement for dpp coincides with the spatial distribution of dpp transcripts, which accumulate in a stripe of cells at or near the known A/P compartment boundary of the wing imaginal disk. Thus, only a small subset of the cells that normally comprise the wing must express dpp to permit development of the entire structure. We propose that this localized expression of dpp is essential to proximal-distal appendage development. We discuss the possibility that dpp expression serves as a landmark for establishing and/or maintaining positional information in imaginal disks.

Animals↗
PubMed2006

Butterfly wings, a new site of porphyrin synthesis and cleavage: studies on the expression of the lipocalin bilin-binding protein in Pieris brassicae.

The bilin-binding protein (BBP), a member of the lipocalin protein superfamily, is synthesized mainly in last instar larvae and in late pupae and newly emerged adults of Pieris brassicae, as previously reported. Here we present results from Northern blot analysis of the BBP gene transcript and from in vitro studies of holo-BBP biosynthesis with isolated wings using [14C]5-aminolevulinic acid as a precursor to the bilin ligand, [14C]-amino acids to label the apo-protein and inhibitors for both processes. Our combined data clearly demonstrate that BBP, which accumulates around pupa-adult transformation, is produced as holoprotein in the developing wings, while the BBP gene transcript is no longer detected in the rest of the body. Forewings and hind wings behave markedly different as the latter represent the major site of BBP synthesis, in agreement with the unequal distribution of BBP in the wings. The presence of an active pathway of porphyrin synthesis and cleavage in insect wings, shown here for the first time, and the role of the biliprotein during wing development remains an enigma so far. As part of this work sequences of fragments of the genes for actin and glyceraldehyde-3-phosphate dehydrogenase were obtained and examined as reference house-keeping genes in the expression studies.

Animals↗
PubMed2004

Transient apical polarization of Gliotactin and Coracle is required for parallel alignment of wing hairs in Drosophila.

In Drosophila, wing hairs are aligned in a distally oriented, parallel array. The frizzled pathway determines proximal-distal cell polarity in the wing; however, in frizzled pathway mutants, wing hairs remain parallel. How wing hairs align has not been determined. We have demonstrated a novel role for the septate junction proteins Gliotactin (Gli) and Coracle (Cora) in this process. Prior to prehair extension, Gli and Cora were restricted to basolateral membranes. During pupal prehair development, Gli and Cora transiently formed apical ribbons oriented from the distal wing tip to the proximal hinge. These ribbons were aligned beneath prehair bases and persisted for several hours. During this time, Gli was lost entirely from the basolateral domain. A Gliotactin mutation altered the apical polarization Gli and Cora and induced defects in hair alignment in pupal and adult stages. Genetic and cell biological assays demonstrated that Gli and Cora function to align hairs independently of frizzled. Taken together, our results indicate that Gli and Cora function as the first-identified members of a long-predicted, frizzled-independent parallel alignment mechanism. We propose a model whereby the apical polarization of Gli and Cora functions to stabilize and align prehairs relative to anterior-posterior cell boundaries during pupal wing development.

Animals↗
PubMed1998

Biomechanical aspects of the insect wing: an analysis using the finite element method.

Insect wings appear as highly functional and largely optimized mechanical constructions. A series of stabilizing constructional elements have been 'designed' to cope with loading during flight. One such element is the expenditure of material in constructing the wing, i.e. the vein system of the wing and its arrangement. It functions like a zig-zag folding framework which stiffens the wing against aerodynamic bending moments. To quantify the quality of material distribution, models of a dragonfly wing and of a fly wing were calculated using the finite element method (FEM).

Animals↗
PubMed2003

Further developmental roles of the Vestigial/Scalloped transcription complex during wing development in Drosophila melanogaster.

The Drosophila homologue of the human TEF-1 gene, scalloped (sd), is required for wing development. The SD protein forms part of a transcriptional activation complex with the protein encoded by vestigial (vg) that, in turn, activates target genes important for wing formation. One sd function involves a regulatory feedback loop with vg and wingless (wg) that is essential in this process. The dorsal-ventral (D/V) margin-specific expression of wg is lost in sd mutant wing discs while the hinge-specific expression appears normal. In the context of wing development, a VG::sdTEA domain fusion produces a protein that mimics the wild-type SD/VG complex and restores the D/V boundary-specific expression of wg in a sd mutant background. Further, targeted expression of wg at the D/V boundary in the wing disc was able to partially rescue the sd mutant phenotype. This infers that sd could function in either the maintenance or induction of wg at the D/V border. Another functional role for sd is the establishment of sensory organ precursors (SOP) of the peripheral nervous system at the wing margin. Thus, the relationship between sd and senseless (sens) in the development of these cells is also examined, and it appears that sd must be functional for proper sens expression, and ultimately, for sensory organ precursor development.

Animals↗
PubMed1999

Plasticity of Drosophila melanogaster wing morphology: effects of sex, temperature and density.

In this paper we use an adjusted ellipse to the contour of the wings of Drosophila as an experimental model to study phenotypic plasticity. The geometric properties of the ellipse describe the wing morphology. Size is the geometric mean of its two radii; shape is the ratio between them; and, the positions of the apexes of the longitudinal veins are determined by their angular distances to the major axis of the ellipse. Flies of an inbred laboratory strain of Drosophila melanogaster raised at two temperatures (16.5 degrees C and 25 degrees C) and two densities (10 and 100 larvae per vial) were used. One wing of at least 40 animals of each sex and environmental condition were analyzed (total = 380), a measurement of thorax length was also taken. Wing size variation could be approximately divided into two components: one related to shape variation and the other shape independent. The latter was influenced primarily by temperature, while the former was related to sex and density. A general pattern could be identified for the shape dependent variation: when wings become larger they become longer and the second, fourth and fifth longitudinal veins get closer to the tip of the wing.

Animals↗
PubMed2004

Heritability of wing morphology in a natural population of Drosophila gouveai.

The natural and laboratory heritabilities of a series of parameters related to wing size and shape were estimated in a population of Drosophila gouveai (repleta group) under field and laboratory conditions. A morphometric analysis was done using 17 wing parameters related to wing landmark positions obtained using the method of the best adjustment of an ellipse to the wing edge. Three parameters (thetaA, thetaC and thetaD) showed highly significant heritability in the wild (average 0.61), whereas only wing size (W(SI)) had significant heritability in the laboratory (0.71). The additive genetic variance of most parameters was greater in the wild than in the laboratory. These results showed that some parameters possessed a substantial genetic additive component in their phenotypic variance, and that morphometric parameters of D. gouveai wings are appropriate quantitative markers for assessing morphological differentiation among populations.

Animals↗
PubMedDate not supplied

Posterior-to-anterior transformation in engrailed wing imaginal disks of Drosophila.

Segments in the Drosophila adult are divided into clonally distinct anterior and posterior compartments. Mutations at the engrailed locus can affect the pattern of cuticular structures in the posterior compartments of segments, but have no obvious effect on anterior structures; for example, bristles that are normally seen only on the anterior wing margin in wild-type flies can be found on the posterior margin of engrailed wings. These and clonal analysis data led to the hypothesis that engrailed causes a transformation of posterior to anterior identity in the wing cells. Despite some striking examples of this transformation, a common engrailed phenotype is the disruption or elimination of posterior pattern elements, without a clear replacement by anterior structures; this, together with indications that localized cell death can mimic some of the observed posterior-to-anterior transformations, has led some investigators to question the original engrailed hypothesis. Recently, monoclonal antibodies displaying region-specific binding patterns on the wing imaginal disk have been described, and one of these antibodies in particular provides a novel probe for the engrailed phenotype in the larval precursors of the adult wing. Here I compare the antibody binding patterns on engrailed and wild-type wing disks. The results strongly support the notion that engrailed mutations cause a posterior-to-anterior transformation in these cells.

Animals↗
PubMed1989

Requirement for integrins during Drosophila wing development.

The position-specific (PS) integrins of Drosophila are highly homologous to vertebrate integrins, most of which are cell-surface receptors for extracellular matrix components. Integrins are heterodimers, each consisting of noncovalently associated alpha- and beta-subunits. As for the subfamilies of vertebrate integrins, the same beta-subunit is found in both Drosophila PS integrins, combined with a specific alpha-subunit to generate either a complete functional PS1 or PS2 integrin. Both alpha- and beta-subunits are large transmembrane proteins (relative molecular masses greater than 100,000). Either one or both of these two PS integrins are expressed in most fly tissues during development. A particularly intriguing pattern of expression is found in the mature wing imaginal disc, where the PS1 integrin is expressed primarily on the presumptive dorsal wing epithelium, and the PS2 integrin is found almost exclusively on the ventral epithelium. Immediately after pupariation, the central wing pouch evaginates, folding along its centre to appose the epithelia that will secret the dorsal and ventral surfaces of the adult wing blade. Here we report the results of a genetic analysis indicating that both of the PS integrins are required to maintain the close apposition of the dorsal and ventral wing epithelia during morphogenesis. Also, we conclude that the integrins are not necessary for the maintenance of the cell lineage restriction between the two presumptive wing surfaces in the developing imaginal disc.

Alleles↗
PubMed2001

Spanwise flow and the attachment of the leading-edge vortex on insect wings.

The flow structure that is largely responsible for the good performance of insect wings has recently been identified as a leading-edge vortex. But because such vortices become detached from a wing in two-dimensional flow, an unknown mechanism must keep them attached to (three-dimensional) flapping wings. The current explanation, analogous to a mechanism operating on delta-wing aircraft, is that spanwise flow through a spiral vortex drains energy from the vortex core. We have tested this hypothesis by systematically mapping the flow generated by a dynamically scaled model insect while simultaneously measuring the resulting aerodynamic forces. Here we report that, at the Reynolds numbers matching the flows relevant for most insects, flapping wings do not generate a spiral vortex akin to that produced by delta-wing aircraft. We also find that limiting spanwise flow with fences and edge baffles does not cause detachment of the leading-edge vortex. The data support an alternative hypothesis-that downward flow induced by tip vortices limits the growth of the leading-edge vortex.

Animals↗