Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis

Lebo, Matthew S.; Sanders, Laura E.; Sun, Fengzhu; Arbeitman, Michelle N.

doi:10.1186/1471-2164-10-80

Cited by 50 publications

(73 citation statements)

References 65 publications

(84 reference statements)

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“…Cluster 13, which contains genes highly expressed in females at P20, is over-represented with genes encoding structural constituents of the chitin-based cuticle (P0.029). This result could mean that females and males deposit cuticle at different times, and supports the previous finding that cuticle-related genes show sex-differential expression during metamorphosis (Lebo et al, 2009). …”

Section: Research Articlesupporting

confidence: 80%

The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development inDrosophila

et al. 2011

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Regulatory networks driving morphogenesis of animal genitalia must integrate sexual identity and positional information. Although the genetic hierarchy that controls somatic sexual identity in the fly Drosophila melanogaster is well understood, there are very few cases in which the mechanism by which it controls tissue-specific gene activity is known. In flies, the sex-determination hierarchy terminates in the doublesex (dsx) gene, which produces sex-specific transcription factors via alternative splicing of its transcripts. To identify sex-specifically expressed genes downstream of dsx that drive the sexually dimorphic development of the genitalia, we performed genome-wide transcriptional profiling of dissected genital imaginal discs of each sex at three time points during early morphogenesis. Using a stringent statistical threshold, we identified 23 genes that have sex-differential transcript levels at all three time points, of which 13 encode transcription factors, a significant enrichment. We focus here on three sex-specifically expressed transcription factors encoded by lozenge (lz), Drop (Dr) and AP-2. We show that, in female genital discs, Dsx activates lz and represses Dr and AP-2. We further show that the regulation of Dr by Dsx mediates the previously identified expression of the fibroblast growth factor Branchless in male genital discs. The phenotypes we observe upon loss of lz or Dr function in genital discs explain the presence or absence of particular structures in dsx mutant flies and thereby clarify previously puzzling observations. Our time course of expression data also lays the foundation for elucidating the regulatory networks downstream of the sex-specifically deployed transcription factors.

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Section: Research Articlesupporting

confidence: 80%

The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development inDrosophila

et al. 2011

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“…during early morphogensis; Lebo et al, 2009). We find that 68 unique transcripts significantly differentially expressed in apple relative to hawthorn flies during our simulated winter treatments are also at least 2-fold differentially expressed (in the same direction) at 24 h relative to 0 h post-pupal formation in D. melanogaster (see R script and gene list deposited in Dryad; D. melanogaster data archived in NCBI GEO GSE11313).…”

Section: Discussion Winter Diapause Developmentmentioning

confidence: 97%

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

Meyers

Powell

Walden

et al. 2016

Journal of Experimental Biology

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The duration of dormancy regulates seasonal timing in many organisms and may be modulated by day length and temperature. Though photoperiodic modulation has been well studied, temperature modulation of dormancy has received less attention. Here, we leverage genetic variation in diapause in the apple maggot fly, Rhagoletis pomonella, to test whether gene expression during winter or following spring warming regulates diapause duration. We used RNAseq to compare transcript abundance during and after simulated winter between an apple-infesting population and a hawthorn-infesting population where the apple population ends pupal diapause earlier than the hawthorn-infesting population. Marked differences in transcription between the two populations during winter suggests that the 'early' apple population is developmentally advanced compared with the 'late' hawthorn population prior to spring warming, with transcripts participating in growth and developmental processes relatively up-regulated in apple pupae during the winter cold period. Thus, regulatory differences during winter ultimately drive phenological differences that manifest themselves in the following summer. Expression and polymorphism analysis identify candidate genes in the Wnt and insulin signaling pathways that contribute to population differences in seasonality. Both populations remained in diapause and displayed a pattern of up-and then down-regulation (or vice versa) of growth-related transcripts following warming, consistent with transcriptional repression. The ability to repress growth stimulated by permissive temperatures is likely critical to avoid mismatched phenology and excessive metabolic demand. Compared with diapause studies in other insects, our results suggest some overlap in candidate genes/pathways, though the timing and direction of changes in transcription are likely species specific.

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“…Act57B contributes to developmental processes and cytoskeleton dynamics but has also been shown to play a role in courtship conditioning (Winbush et al 2012). Kank, a gene that affects muscle tendon development, has been shown to be differentially expressed downstream of dsx (Lebo et al 2009), suggesting AI regulation in the sex determination pathway in virgins only. p24-1 has sex-specific expression (Boltz et al 2007) and has been shown to play a role in the neural signaling involved in female egglaying defects and reproductive behavior (Saleem et al 2012).…”

Section: Environmental Effects On Allelic Imbalancementioning

confidence: 99%

Buffering of Genetic Regulatory Networks inDrosophila melanogaster

et al. 2016

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Regulatory variation in gene expression can be described by cis-and trans-genetic components. Here we used RNA-seq data from a population panel of Drosophila melanogaster test crosses to compare allelic imbalance (AI) in female head tissue between mated and virgin flies, an environmental change known to affect transcription. Indeed, 3048 exons (1610 genes) are differentially expressed in this study. A Bayesian model for AI, with an intersection test, controls type I error. There are 200 genes with AI exclusively in mated or virgin flies, indicating an environmental component of expression regulation. On average 34% of genes within a cross and 54% of all genes show evidence for genetic regulation of transcription. Nearly all differentially regulated genes are affected in cis, with an average of 63% of expression variation explained by the cis-effects. Trans-effects explain 8% of the variance in AI on average and the interaction between cis and trans explains an average of 11% of the total variance in AI. In both environments cis-and trans-effects are compensatory in their overall effect, with a negative association between cis-and trans-effects in 85% of the exons examined. We hypothesize that the gene expression level perturbed by cis-regulatory mutations is compensated through trans-regulatory mechanisms, e. g., trans and cis by trans-factors buffering cis-mutations. In addition, when AI is detected in both environments, cis-mated, cis-virgin, and trans-mated-trans-virgin estimates are highly concordant with 99% of all exons positively correlated with a median correlation of 0.83 for cis and 0.95 for trans. We conclude that the gene regulatory networks (GRNs) are robust and that trans-buffering explains robustness.

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Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis

Cited by 50 publications

References 65 publications

The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development inDrosophila

The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development inDrosophila

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

Buffering of Genetic Regulatory Networks inDrosophila melanogaster

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