Dataset Information

Chorion patterning: a window into gene regulation and Drosophila species' relatedness.

ABSTRACT: Changes in gene regulation are associated with the evolution of morphologies. However, the specific sequence information controlling gene expression is largely unknown and discovery is time and labor consuming. We use the intricate patterning of follicle cells to probe species' relatedness in the absence of sequence information. We focus on one of the major families of genes that pattern the Drosophila eggshell, the Chorion protein (Cp). Systematically screening for the spatiotemporal patterning of all nine Cp genes in three species (Drosophila melanogaster, D. nebulosa, and D. willistoni), we found that most genes are expressed dynamically during mid and late stages of oogenesis. Applying an annotation code, we transformed the data into binary matrices that capture the complexity of gene expression. Gene patterning is sufficient to predict species' relatedness, consistent with their phylogeny. Surprisingly, we found that expression domains of most genes are different among species, suggesting that Cp regulation is rapidly evolving. In addition, we found a morphological novelty along the dorsalmost side of the eggshell, the dorsal ridge. Our matrix analysis placed the dorsal ridge domain in a cluster of epidermal growth factor receptor associated domains, which was validated through genetic and chemical perturbations. Expression domains are regulated cooperatively or independently by signaling pathways, supporting that complex patterns are combinatorially assembled from simple domains.

SUBMITTER: Niepielko MG

PROVIDER: S-EPMC3879450 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Chorion patterning: a window into gene regulation and Drosophila species' relatedness.

Niepielko Matthew G MG Marmion Robert A RA Kim Kenneth K Luor David D Ray Chelsea C Yakoby Nir N

Molecular biology and evolution 20131008 1

Changes in gene regulation are associated with the evolution of morphologies. However, the specific sequence information controlling gene expression is largely unknown and discovery is time and labor consuming. We use the intricate patterning of follicle cells to probe species' relatedness in the absence of sequence information. We focus on one of the major families of genes that pattern the Drosophila eggshell, the Chorion protein (Cp). Systematically screening for the spatiotemporal patterning ...[more]

PMID: 24109603

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Project description:In early development, genes are expressed in spatial patterns which later define cellular identities and tissue locations. The mechanisms of such pattern formation have been studied extensively in early Drosophila (fruit fly) embryos. The gap gene hunchback (hb) is one of the earliest genes to be expressed in anterior-posterior (AP) body segmentation. As a transcriptional regulator for a number of downstream genes, the spatial precision of hb expression can have significant effects in the development of the body plan. To investigate the factors contributing to hb precision, we used fine spatial and temporal resolution data to develop a quantitative model for the regulation of hb expression in the mid-embryo. In particular, modelling hb pattern refinement in mid nuclear cleavage cycle 14 (NC14) reveals some of the regulatory contributions of simultaneously-expressed gap genes. Matching the model to recent data from wild-type (WT) embryos and mutants of the gap gene Krüppel (Kr) indicates that a mid-embryo Hb concentration peak important in thoracic development (at parasegment 4, PS4) is regulated in a dual manner by Kr, with low Kr concentration activating hb and high Kr concentration repressing hb. The processes of gene expression (transcription, translation, transport) are intrinsically random. We used stochastic simulations to characterize the noise generated in hb expression. We find that Kr regulation can limit the positional variability of the Hb mid-embryo border. This has been recently corroborated in experimental comparisons of WT and Kr- mutant embryos. Further, Kr regulation can decrease uncertainty in mid-embryo hb expression (i.e. contribute to a smooth Hb boundary) and decrease between-copy transcriptional variability within nuclei. Since many tissue boundaries are first established by interactions between neighbouring gene expression domains, these properties of Hb-Kr dynamics to diminish the effects of intrinsic expression noise may represent a general mechanism contributing to robustness in early development.

Project description:Differences in the level, timing, or location of gene expression can contribute to alternative phenotypes at the molecular and organismal level. Understanding the origins of expression differences is complicated by the fact that organismal morphology and gene regulatory networks could potentially vary even between closely related species. To assess the scope of such changes, we used high-resolution imaging methods to measure mRNA expression in blastoderm embryos of Drosophila yakuba and Drosophila pseudoobscura and assembled these data into cellular resolution atlases, where expression levels for 13 genes in the segmentation network are averaged into species-specific, cellular resolution morphological frameworks. We demonstrate that the blastoderm embryos of these species differ in their morphology in terms of size, shape, and number of nuclei. We present an approach to compare cellular gene expression patterns between species, while accounting for varying embryo morphology, and apply it to our data and an equivalent dataset for Drosophila melanogaster. Our analysis reveals that all individual genes differ quantitatively in their spatio-temporal expression patterns between these species, primarily in terms of their relative position and dynamics. Despite many small quantitative differences, cellular gene expression profiles for the whole set of genes examined are largely similar. This suggests that cell types at this stage of development are conserved, though they can differ in their relative position by up to 3-4 cell widths and in their relative proportion between species by as much as 5-fold. Quantitative differences in the dynamics and relative level of a subset of genes between corresponding cell types may reflect altered regulatory functions between species. Our results emphasize that transcriptional networks can diverge over short evolutionary timescales and that even small changes can lead to distinct output in terms of the placement and number of equivalent cells.

Dataset Information

Chorion patterning: a window into gene regulation and Drosophila species' relatedness.

Publications

Chorion patterning: a window into gene regulation and Drosophila species' relatedness.

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