Dataset Information

Neuronal remodeling during metamorphosis is regulated by the alan shepard (shep) gene in Drosophila melanogaster.

ABSTRACT: Peptidergic neurons are a group of neuronal cells that synthesize and secrete peptides to regulate a variety of biological processes. To identify genes controlling the development and function of peptidergic neurons, we conducted a screen of 545 splice-trap lines and identified 28 loci that drove expression in peptidergic neurons when crossed to a GFP reporter transgene. Among these lines, an insertion in the alan shepard (shep) gene drove expression specifically in most peptidergic neurons. shep transcripts and SHEP proteins were detected primarily and broadly in the central nervous system (CNS) in embryos, and this expression continued into the adult stage. Loss of shep resulted in late pupal lethality, reduced adult life span, wing expansion defects, uncoordinated adult locomotor activities, rejection of males by virgin females, and reduced neuropil area and reduced levels of multiple presynaptic markers throughout the adult CNS. Examination of the bursicon neurons in shep mutant pharate adults revealed smaller somata and fewer axonal branches and boutons, and all of these cellular phenotypes were fully rescued by expression of the most abundant wild-type shep isoform. In contrast to shep mutant animals at the pharate adult stage, shep mutant larvae displayed normal bursicon neuron morphologies. Similarly, shep mutant adults were uncoordinated and weak, while shep mutant larvae displayed largely, although not entirely, normal locomotor behavior. Thus, shep played an important role in the metamorphic development of many neurons.

SUBMITTER: Chen D

PROVIDER: S-EPMC4125399 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Neuronal remodeling during metamorphosis is regulated by the alan shepard (shep) gene in Drosophila melanogaster.

Chen Dahong D Qu Chunjing C Bjorum Sonia M SM Beckingham Kathleen M KM Hewes Randall S RS

Genetics 20140614 4

Peptidergic neurons are a group of neuronal cells that synthesize and secrete peptides to regulate a variety of biological processes. To identify genes controlling the development and function of peptidergic neurons, we conducted a screen of 545 splice-trap lines and identified 28 loci that drove expression in peptidergic neurons when crossed to a GFP reporter transgene. Among these lines, an insertion in the alan shepard (shep) gene drove expression specifically in most peptidergic neurons. she ...[more]

PMID: 24931409

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Project description:BACKGROUND:Drosophila melanogaster undergoes a complete metamorphosis, during which time the larval male and female forms transition into sexually dimorphic, reproductive adult forms. To understand this complex morphogenetic process at a molecular-genetic level, whole genome microarray analyses were performed. RESULTS:The temporal gene expression patterns during metamorphosis were determined for all predicted genes, in both somatic and germline tissues of males and females separately. Temporal changes in transcript abundance for genes of known functions were found to correlate with known developmental processes that occur during metamorphosis. We find that large numbers of genes are sex-differentially expressed in both male and female germline tissues, and relatively few are sex-differentially expressed in somatic tissues. The majority of genes with somatic, sex-differential expression were found to be expressed in a stage-specific manner, suggesting that they mediate discrete developmental events. The Sex-lethal paralog, CG3056, displays somatic, male-biased expression at several time points in metamorphosis. Gene expression downstream of the somatic, sex determination genes transformer and doublesex (dsx) was examined in two-day old pupae, which allowed for the identification of genes regulated as a consequence of the sex determination hierarchy. These include the homeotic gene abdominal A, which is more highly expressed in females as compared to males, as a consequence of dsx. For most genes regulated downstream of dsx during pupal development, the mode of regulation is distinct from that observed for the well-studied direct targets of DSX, Yolk protein 1 and 2. CONCLUSION:The data and analyses presented here provide a comprehensive assessment of gene expression during metamorphosis in each sex, in both somatic and germline tissues. Many of the genes that underlie critical developmental processes during metamorphosis, including sex-specific processes, have been identified. These results provide a framework for further functional studies on the regulation of sex-specific development.

Project description:As organisms age the environment fluctuates, exerting differential selection across ontogeny. In particular, highly seasonal environments expose life stages to often drastically different thermal environments. This developmental variation is particularly striking in organisms with complex life cycles, wherein life history stages also exhibit distinct morphologies, physiologies, and behaviors. Genes acting pleiotropically on thermal responses may produce genetic correlations across ontogeny, constraining the independent evolution of each life stage to their respective thermal environments. To investigate whether developmental genetic correlations constrain the evolution thermal hardiness of the fly Drosophila melanogaster, we applied quantitative genetic analyses to cold hardiness measured in both larvae and adults from isogenic lines of the Drosophila Genetic Reference Panel (DGRP), using survival at stressful low temperatures as the phenotypic metric. Using full genome resequencing data for the DGRP, we also implemented genome-wide association (GWA) analysis using Bayesian Sparse Linear Mixed Models (BSLMMs) to estimate associations between naturally segregating variation and cold hardiness for both larvae and adults. Quantitative genetic analyses revealed no significant genetic correlation for cold hardiness between life stages, suggesting complete genetic decoupling of thermal hardiness across the metamorphic boundary. Both quantitative genetic and GWA analyses suggested that polygenic variation underlies cold hardiness in both stages, and that associated loci largely affected one stage or the other, but not both. However, reciprocal enrichment tests and correlations between BSLMM parameters for each life stage support some shared physiological mechanisms that may reflect common cellular thermal response pathways. Overall, these results suggest no developmental genetic constraints on cold hardiness across metamorphosis in D. melanogaster, an important consideration in evolutionary models of responses to changing climates. Genetic correlations for environmental sensitivity across ontogeny remains largely unexplored in other organisms, thus assessing the generality of genetic decoupling will require further quantitative or population genetic analysis in additional species.

Project description:Regulation of transcription is one of the mechanisms involved in animal development, directing changes in patterning and cell fate specification. Large temporal data series, based on microarrays across the life cycle of the fly Drosophila melanogaster, revealed the existence of groups of genes which expression increases or decreases temporally correlated during the life cycle. These groups of genes are enriched in different biological functions. Here, instead of searching for temporal coincidence in gene expression using the entire genome expression data, we searched for temporal coincidence in gene expression only within predefined catalogues of functionally related genes and investigated whether a catalogue's expression profile can be used to generate larger catalogues, enriched in genes necessary for the same function. We analyzed the expression profiles from genes already associated with early neurodevelopment and late neurodifferentiation, at embryonic stages 16 and 17 of Drosophila life cycle. We hypothesized that during this interval we would find global downregulation of genes important for early neuronal development together with global upregulation of genes necessary for the final differentiation of neurons. Our results were consistent with this hypothesis. We then investigated if the expression profile of gene catalogues representing particular processes of neural development matched the temporal sequence along which these processes occur. The profiles of genes involved in patterning, neurogenesis, axogenesis or synaptic transmission matched the prediction, with largest transcript values at the time when the corresponding biological process takes place in the embryo. Furthermore, we obtained catalogues enriched in genes involved in temporally matching functions by performing a genome-wide systematic search for genes with their highest expression levels at the corresponding embryonic intervals. These findings imply the use of gene expression data in combination with known biological information to predict the involvement of functionally uncharacterized genes in particular biological events.

Dataset Information

Neuronal remodeling during metamorphosis is regulated by the alan shepard (shep) gene in Drosophila melanogaster.

Publications

Neuronal remodeling during metamorphosis is regulated by the alan shepard (shep) gene in Drosophila melanogaster.

Similar Datasets

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