The Hox gene Antennapedia regulates wing development through 20-hydroxyecdysone in insect (original) (raw)
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European Journal of Biochemistry, 2004
The IAL-PID2 cells derived from imaginal wing discs of the last larval instar of Plodia interpunctella were responsive to 20-hydroxyecdysone (20E). These imaginal cells respond to 20E by proliferative arrest followed by a morphological differentiation. These 20E-induced late responses were inhibited in presence of juvenile hormone (JH II). From these imaginal wing cells, we have cloned a cDNA sequence encoding a P. interpunctella ecdysone receptor-B1 isoform (PIEcR-B1). The amino acid sequence of PIEcR-B1 showed a high degree of identity with EcR-B1 isoforms of Bombyx mori, Manduca sexta and Choristoneura fumiferana. The pattern of PIEcR-B1 mRNA induction by 20E was characterized by a biphasic response with peaks at 2 h and 18 h. The presence of the protein synthesis inhibitor anisomycin induced a slight reduction in level of PIEcR-B1 mRNA and prevented the subsequent declines observed in 20E-treated cells. Therefore, PIEcR-B1 mRNA was directly induced by 20E and its downregulation depended on protein synthesis. An exposure of imaginal wing cells to 20E in the presence of JH II caused an increased expression of Plodia E75-B and HR3 transcription factors but inhibited the second increase of PIEcR-B1 mRNA. These findings showed that in vitro JH II was able to prevent the 20E-induced differentiation of imaginal wing cells. This effect could result from a JH II action on the 20E-induced genetic cascade through a modulation of EcR-B1, E75-B and HR3 expression.
Hox dosage contributes to flight appendage morphology in Drosophila
Nature Communications, 2021
Flying insects have invaded all the aerial space on Earth and this astonishing radiation could not have been possible without a remarkable morphological diversification of their flight appendages. Here, we show that characteristic spatial expression profiles and levels of the Hox genes Antennapedia (Antp) and Ultrabithorax (Ubx) underlie the formation of two different flight organs in the fruit fly Drosophila melanogaster. We further demonstrate that flight appendage morphology is dependent on specific Hox doses. Interestingly, we find that wing morphology from evolutionary distant four-winged insect species is also associated with a differential expression of Antp and Ubx. We propose that variation in the spatial expression profile and dosage of Hox proteins is a major determinant of flight appendage diversification in Drosophila and possibly in other insect species during evolution.
Proceedings of the National Academy of Sciences, 2004
Diversification of leg appendages is one of the hallmarks of morphological evolution in insects. In particular, insect hind (T3) legs exhibit a whole spectrum of morphological diversification, ranging from uniform to extremely modified. To elucidate the developmental basis of T3 leg evolution, we have examined the expression patterns of two homeotic genes, Ultrabithorax and abdominal-A (collectively referred to as UbdA), in a broad range of species. First, our results show that UbdA expression in hemimetabolous insects is localized only in specific T3 leg segments undergoing differential growth (compared to their foreleg counterparts). In contrast, in basal hexapod and insect lineages, the absence of the UbdA signal coincides with uniform leg morphology. The same situation exists in first instar larvae of holometabolous insects, in which absence of UbdA expression in the embryonic T3 legs is associated with the lack of larval T3 leg diversification. Second, there is a clear difference in the timing of expression between species with greatly enlarged T3 leg, such as crickets and grasshoppers, and species that exhibit more moderate enlargement of hind legs, such as mantids and cockroaches. In the former, the UbdA expression starts much earlier, coinciding with the elongation of T3 limb buds. In the latter, however, the UbdA expression starts at much later stages of development, coinciding with the establishment of distinct leg segments. These results suggest that diversification of insect hind legs was influenced by changes in both the spatial and temporal regulation of the UbdA expression.
Specific transcriptional responses to juvenile hormone and ecdysone in Drosophila
Insect Biochemistry and Molecular Biology, 2007
Previous studies have shown that ecdysone (E), and its immediate downstream product 20-hydroxyecdysone (20E), can have different biological functions in insects, suggesting that E acts as a distinct hormone. Here, we use Drosophila larval organ culture in combination with microarray technology to identify genes that are transcriptionally regulated by E, but which show little or no response to 20E. These genes are coordinately expressed for a brief temporal interval at the onset of metamorphosis, suggesting that E acts together with 20E to direct puparium formation. We also show that E74B, pepck, and CG14949 can be induced by juvenile hormone III (JH III) in organ culture, and that CG14949 can be induced by JH independently of protein synthesis. In contrast, E74A and E75A show no response to JH in this system. These studies demonstrate that larval organ culture can be used to identify Drosophila genes that are regulated by hormones other than 20E, and provide a basis for studying crosstalk between multiple hormone signaling pathways. r
Development, 2000
The Drosophila wing imaginal disc gives rise to three body parts along the proximo-distal (P-D) axis: the wing blade, the wing hinge and the mesonotum. Development of the wing blade initiates along part of the dorsal/ventral (D/V) compartment boundary and requires input from both the Notch and wingless (wg) signal transduction pathways. In the wing blade, wg activates the gene vestigial (vg), which is required for the wing blade to grow. wg is also required for hinge development, but wg does not activate vg in the hinge, raising the question of what target genes are activated by wg to generate hinge structures. Here we show that wg activates the gene homothorax (hth) in the hinge and that hth is necessary for hinge development. Further, we demonstrate that hth also limits where along the D/V compartment boundary wing blade development can initiate, thus helping to define the size and position of the wing blade within the disc epithelium. We also show that the gene teashirt (tsh), wh...
Development Genes and Evolution, 1998
The two genes vestigial (vg) and scalloped (sd) are required for wing development in Drosophila melanogaster. They present similar patterns of expression in second and third instar wing discs and similar wing mutant phenotypes. vg encodes a nuclear protein without any recognized nucleic acid-binding motif. Sd is a transcription factor homologous to the human TEF-1 factor whose promoter activity depends on cell-specific cofactors. We postulate that Vg could be a cofactor of Sd in the wing morphogenetic process and that, together, they could constitute a functional transcription complex. We investigated genetic interactions between the two genes. We show here that vg and sd co-operate in vivo in a manner dependent on the structure of the Vg protein.
Comparative analysis of Hox downstream genes in Drosophila
Development, 2007
Functional diversification of body parts is dependent on the formation of specialized structures along the various body axes. In animals, region-specific morphogenesis along the anteroposterior axis is controlled by a group of conserved transcription factors encoded by the Hox genes. Although it has long been assumed that Hox proteins carry out their function by regulating distinct sets of downstream genes, only a small number of such genes have been found, with very few having direct roles in controlling cellular behavior. We have quantitatively identified hundreds of Hox downstream genes in Drosophila by microarray analysis, and validated many of them by in situ hybridizations on loss-and gain-of-function mutants. One important finding is that Hox proteins, despite their similar DNA-binding properties in vitro, have highly specific effects on the transcriptome in vivo, because expression of many downstream genes respond primarily to a single Hox protein. In addition, a large fraction of downstream genes encodes realizator functions, which directly affect morphogenetic processes, such as orientation and rate of cell divisions, cell-cell adhesion and communication, cell shape and migration, or cell death. Focusing on these realizators, we provide a framework for the morphogenesis of the maxillary segment. As the genomic organization of Hox genes and the interaction of Hox proteins with specific co-factors are conserved in vertebrates and invertebrates, and similar classes of downstream genes are regulated by Hox proteins across the metazoan phylogeny, our findings represent a first step toward a mechanistic understanding of morphological diversification within a species as well as between species.
Developmental Dynamics, 2006
Blowflies are the primary facultative agent in causing myiasis of domestic sheep in the whole world and, at the same time, it is an important tool for forensic medicine. Surprisingly, and in contrast to its importance, almost no data regarding the embryology and molecular markers are known for this insect. In this report, we present a detailed description of the blowfly Lucilia sericata embryogenesis and of imaginal disc development. The embryogenesis of Lucilia strongly resembles that of Drosophila, despite their apparent size difference. Moreover, imaginal disc development appears to be equally well conserved. Through cloning, expression, and functional studies, we show that the Lucilia Wingless (Wg) protein is highly conserved between the two species. We further show that parasegments are established in Lucilia, however, engrailed expression shows a more dynamic expression pattern than expected in comparison to Drosophila.
In contrast to the important role of hormones in the development of sexual dimorphic traits in vertebrates [1], the differentiation of these traits in insects is attributed exclusively to variation in cell-autonomous mechanisms controlled by members of the sex determination pathway [2], such as doublesex (dsx). Although hormones can shape the development of sexual traits in insects, and interact with dsx to create dimorphisms, variation in hormone levels are not known to cause dimorphism in these traits [3]. Here we show that butterflies use sex-specific differences in 20-hydroxyecdysone (20E) hormone titers to create sexually dimorphic wing ornaments, without the local involvement of dsx. Females of the dry season (DS) form ofBicyclus anynanadisplay a larger sexual ornament on their wings than males, whereas in the wet season (WS) form both sexes have similarly sized ornaments [4]. High levels of circulating 20E during larval development in DS females and WS forms cause proliferati...
DER signaling restricts the boundaries of the wing field during Drosophila development
Proceedings of the National Academy of Sciences, 2000
Arthropod and vertebrate limbs develop from secondary embryonic fields. In insects, the wing imaginal disk is subdivided early in development into the wing and notum subfields. The activity of the Wingless protein is fundamental for this subdivision and seems to be the first element of the hierarchy of regulatory genes promoting wing formation. Drosophila epidermal growth factor receptor (DER) signaling has many functions in fly development. Here we show that antagonizing DER signaling during the second larval instar leads to notum to wing transformations and wing mirror-image duplications. DER signaling is necessary for confining the wing subregion in the developing wing disk and for the specification of posterior identity. To do so, DER signaling acts by restricting the expression of Wingless to the dorsal-posterior quadrant of wing discs, suppressing wing-organizing activities, and by cooperating in the maintenance of Engrailed expression in posterior compartment cells.