Developing compound eye in lozenge mutants of Drosophila: lozenge expression in the R7 equivalence group

 The lozenge locus is genetically complex, containing two functionally distinct units, cistrons A and B, that influence the structure of the compound eye. Extreme mutations of either cistron produce adult phenotypes that share similarities and that have striking differences. We have analyzed the expression of several developmentally important eye genes including boss, scabrous, rhomboid, seven-up, and Bar in lozenge mutant backgrounds representing both cistrons. This analysis follows the progressive recruitment of photoreceptor neurons during eye development and has confirmed that the initial development of photoreceptors is normal up to the five cell precluster stage (R8, R2/5 and R3/4). However, when lozenge is mutant, further eye development is perturbed. As cells R1, R6 and R7 are recruited, patterns of gene expression for seven-up and Bar become abnormal. We have also characterized the expression of two different enhancer trap alleles of lozenge. The lozenge product(s) appear to be first expressed in the eye disc in undifferentiated cells shortly after the five cell precluster forms. Then, as distinct cells are recruited to a fate, lozenge expression persists and is refined in those cells. Our data suggests that lozenge functions in cone cells and pigment cells as well as in specific glia. With respect to photoreceptor neurons, lozenge biases the developmental potential of cells R1, R6 and R7, by directly influencing the expression of genes important for establishing cell fate. Received: 26 July 1996 / Accepted: 6 January 1997     

Ommatidial development in Drosophila eye disc fragments

We have tested the hypothesis that the leading edge of the growing Drosophila compound eye acts as a template that organizes unpatterned cells of the retinal epithelium into the accurate cellular mosaic of the eye. Unpatterned fragments of the epithelium, not containing the leading edge of the growing field, were transplanted into larval hosts. After hosts pupated, the implants were recovered; most contained ommatidia, demonstrating that the leading edge of the growing eye pattern is not required for its propagation. In a second set of experiments, implants were recovered before hosts pupated and examined for ommatidia using a monoclonal antibody. These implants likewise differentiated ommatidia and the temporal progress of retinal development in the implants mirrored that of normal development. A schedule of ommatidial development thus appears to be mapped onto the retinal epithelium in advance of the leading edge.     

senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye.

An outstanding model to study how neurons differentiate from among a field of equipotent undifferentiated cells is the process of R8 photoreceptor differentiation during Drosophila eye development. We show that in senseless mutant tissue, R8 differentiation fails and the presumptive R8 cell adopts the R2/R5 fate. We identify senseless repression of rough in R8 as an essential mechanism of R8 cell fate determination and demonstrate that misexpression of senseless in non-R8 photoreceptors results in repression of rough and induction of the R8 fate. Surprisingly, there is no loss of ommatidial clusters in senseless mutant tissue and all outer photoreceptor subtypes can be recruited, suggesting that other photoreceptors can substitute for R8 to initiate recruitment and that R8-specific signaling is not required for outer photoreceptor subtype assignment. A genetic model of R8 differentiation is presented.     

Neuronal development in the Drosophila compound eye: Photoreceptor cells R1, R6, and R7 fail to differentiate in the retina aberrant in pattern (rap) mutant

The compound eye of Drosophila is a reiterated pattern of 800 unit eyes known as ommatidia. In each ommatidium there are eight photoreceptor neurons (R1–R8) and an invariant number of accessory cells organized in a precise manner. In the developing eye, specification of cell fates is triggered by sequential inductive events mediated by cell-cell interactions. The R8 photoreceptor neuron is the first cell to differentiate and is thought to play a central role in the recruitment of the remaining photoreceptor cells. Our previous work demonstrated that mutations in the retina aberrant in pattern (rap) locus lead to abnormal pattern formation in the compound eye. Genetic mosaic experiments demonstrated that for normal retinal patterning to occur, rap gene function is required only in the photoreceptor cell R8. In this study we analyzed the R cell composition of developing as well as the adult eyes of rap mutants employing a variety of R cell specific markers. We show that in rap mutants, although some of the R8-specific markers show normal expression patterns, other aspects of the R8 cell differentiation are abnormal. In addition, the cells R1, R6, and R7 fail to differentiate properly in rap mutants. These results suggest that the rap gene encodes an R8-specific function that plays a role in the determination of the photoreceptor cells R1, R6, and R7. © 1996 John Wiley & Sons, Inc.     

A dose-sensitive modifier of the of Drosophila melanogaster ectopic eye

Ectopic eyes induced in a wing serve as a system for studying developmental plasticity in Drosophila. We used a set of chromosome deficiencies covering the second chromosome to ask whether there are dose-sensitive modifiers of the process. We identified three overlapping deletions showing the enlargement of ectopic eyes. The study of the genes localized in the region of interest suggests that the mutation in the sxc (super sex combs) gene (PcG group) is responsible for the observed phenotype.     

Over-expression of transglutaminase in the Drosophila eye imaginal disc induces a rough eye phenotype

Transglutaminases (TGs) catalyze the cross-linking of proteins and are involved in various biological processes in mammals. In invertebrates, except for the involvement in the hemolymph clotting, the functions of TG have not been revealed. Drosophila has a single TG gene (CG7356), from which two kinds of mRNAs (dTG-RA and dTG-RB) are formed. RT-PCR analyses indicated that both dTGs-RA and -RB are synthesized in all the developmental stages tested. To reveal the roles of dTG during the development, we examined a phenotype induced through the ectopic expression of dTG by using a GAL4-UAS targeted expression system. Over-expression of dTG-A in the eye imaginal disc of larva induced a rough eye phenotype in adult compound eyes. Co-expression of P35, an inhibitor of apoptosis, suppressed the rough eye phenotype, suggesting that the rough eye phenotype induced by the over-expression of dTG-A in the eye imaginal disc is due to the occurrence of apoptosis. The rough eye phenotype induced by the over-expression of dTG-A was suppressed by the crossing with mutant fly lines lacking Drosophila JNK gene basket (bsk) or Drosophila JNKK gene hemipterous. FLP-out experiments using an enhancer trap line showed that the over-expression of dTG-A in the eye imaginal disc increased the puckered enhancer activity, a reporter of Bsk activity. These results suggested that the rough eye phenotype induced by the over-expression of dTG-A is related to an enhancement of JNK signaling pathway.     

The pineapple eye gene is required for survival of Drosophila imaginal disc cells

Each ommatidium of the Drosophila eye is constructed by precisely 19 specified precursor cells, generated in part during a second mitotic wave of cell divisions that overlaps early stages of ommatidial cell specification. Homozygotes for the pineapple eye mutation lack sufficient precursor cells due to apoptosis during the period of fate specification. In addition development is delayed by apoptosis during earlier imaginal disc growth. Null alleles are recessive lethal and allelic to l(2)31Ek; heteroallelic combinations can show developmental delay, abnormal eye development, and reduced fertility. Mosaic clones autonomously show extensive cell death. The pineapple eye gene was identified and predicted to encode a novel 582-amino-acid protein. The protein contains a novel, cysteine-rich domain of 270 amino acids also found in predicted proteins of unknown function from other animals.     

Intragenic somatic recombination in the lozenge cistron of Drosophila

Summary In Drosophila melanogaster intragenic mitotic recombination between the two lozenge alleles, lz ³⁶ and lz ^y4, separated from each other by 0.14 meiotic recombination units, was observed. Among 48 725 females of the genotype w ⁺lz³⁶/w lz^y4 which had been irradiated by a dose of 1000 r X-rays as larvae 41–47 hours after oviposition, a total of 11 faceted eye spots (not lz) were induced. All 11 spots were w ⁺, none w. Possible reasons for the lack of the expected w, faceted spots were checked. Inversion of the X chromosome which would suppress recombination between the w and lz loci was not involved. Gene order of lz ³⁶-lz^y4-kinetochore was confirmed by meiotic recombination test. Nonautonomy of lz gene action was not a factor, as tested by gynanders which showed that lz ^y4 and lz ^s were autonomous. Possibility of reverse mutation was not likely as shown by the large scale control experiments. Gene conversion is suggested as a likely mechanism for the lack of the expected w, faceted spots although the possibility of unequal crossing over induced by X-rays can not be excluded, nor can the preferential z-segregation hypothesis.     

The development of the Drosophila genital disc

The imaginal discs of Drosophila melanogaster, which form the adult epidermal structures, are a good experimental model for studying morphogenesis. The genital disc forms the terminalia, which are the most sexually dimorphic structures of the fly. Both sexes of Drosophila have a single genital disc formed by three primordia. The female genital primordium is derived from 8(th) abdominal segment and is located anteriorly, the anal primordium (10 and 11(th) abdominal segments) is located posteriorly, and the male genital primordium from the 9(th) abdominal segment lies between them. In both sexes, only two of these three primordia develop to form the adult terminalia. The anal primordium develops in both sexes but, depending on the genetic sex, will form either male or female analia. However, only one of the genital primordia develops in each sex, forming either the male or the female genitalia. This depends on the genetic sex of the fly. Therefore, the genital disc is a very good experimental model of how the sex-determination and homeotic genes - which determine cell identity - interact to direct the development of a population of cells into male or female terminalia. It has been proposed that the sexually dimorphic development of the genital disc is the result of an integrated genetic input, made up by the sex-determination gene doublesex and the homeotic gene Abdominal-B. This input acts by modulating the response to Hedgehog, Wingless, and Decapentaplegic morphogenetic signals.     

semang affects the development of a subset of cells in the Drosophila compound eye

semang (sag), a mutation isolated as a suppressor of Drosophila Src42A, has previously been shown to affect some receptor tyrosine kinase mediated embryonic processes. Here we show that sag specifically affects the development of R1, R6 and R7 photoreceptor cells in a cell-autonomous manner. These cells are absent in the mutant at the time when they normally appear in the ommatidial pre-clusters. Genetic analyses suggest that sag functions downstream of, or parallel to, Mapk and Yan in the photoreceptor differentiation pathway. The autonomous requirement of sag for R1/R6/R7 development could be explained by a selective impairment of the late, but not early, rounds of Egfr-induced precursor cell assembly by the sag mutations. Egfr signaling is highly regulated by autocrine or paracrine mechanisms in different cells. Knowing that the photoreceptor cluster formation is a complex process involving dynamic changes in cell-cell contact, our hypothesis is that the sag alleles affected certain special aspects of Egfr-signaling that are unique for the recruitment of R1/R6/R7 cells.     

The embryonic development of larval muscles in Drosophila

Each of the abdominal hemisegments A2-A7 in the Drosophila larva has a stereotyped pattern of 30 muscles. The pattern is complete by 13 h after egg laying, but the development of individual muscles has begun with the definition of precursors at least by the onset of germ band shortening, some 5.5 h earlier. The earliest signs of muscle differentiation are cell fusions, which occur in the ventralmost mesoderm overlying the CNS and at stereotyped positions in the rest of the mesoderm as the germ band shortens. At the end of shortening, the pattern of muscle precursors produced by these fusions is complete. Precursors filled with dye reveal extensive fine processes probably involved initially in cell fusion and, subsequently, in navigation over the epidermis to form attachment points. The muscle pattern is formed before innervation and without cell death. Thus, neither of these processes is involved in determining the distribution of precursors. Evidence is presented for the view that the development of the larval muscle pattern in Drosophila depends on a prior segregation of founder cells at appropriate locations in the mesoderm with which other cells fuse to form the precursors.     

Growing pains: development of the larval nocifensive response in Drosophila

The ability to perceive and avoid harmful substances or stimuli is key to an organism's survival. The neuronal cognate of the perception of pain is known as nociception, and the reflexive motion to avoid pain is termed the nocifensive response. As the nocifensive response is an ancient and evolutionarily conserved behavioral response to nociceptive stimuli, it is amenable to study in relatively simple and genetically tractable model systems such as Drosophila. Recent studies have taken advantage of the useful properties of Drosophila larvae to begin elucidating the neuronal connectivity and molecular machinery underlying the nocifensive response. However, these studies have primarily utilized the third-instar larval stage, and many mutations that potentially influence nociception survive only until earlier larval stages. Here we characterize the nocifensive responses of Drosophila throughout larval development and find dramatic changes in the nature of the behavior. Notably, we find that prior to the third instar, larvae are unable to perform the characteristic "corkscrew-like roll" behavior. Also, we identify an avoidance behavior consistent with a nocifensive response that is present immediately after larval hatching, representing a paradigm that may be useful in examining mutations with an early lethal phenotype.     

Determination and development of the larval muscle pattern in Drosophila melanogaster

This review describes briefly what is known about the early steps of mesoderm differentiation in the fruitfly Drosophila melanogaster. After a summary of general aspects including mesoderm differentiation, mesoderm cell migration and subdivision of the mesoderm, more detail is given about the specification of muscle progenitor cells, due to their role as the earliest obvious landmarks in muscle fiber development in Drosophila. Particular focus is given to recent results on the role of asymmetric cell division in muscle differentiation. Furthermore a short summary of myoblast fusion is provided.