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Increased chromatin accessibility promotes the evolution of a transcriptional silencer in Drosophila [ATAC-seq]

ABSTRACT: The loss of discrete morphological traits, the most common evolutionary transition, is typically driven by changes in expression of developmental genes. Mutations accumulating in regulatory elements of these genes can disrupt DNA binding sites for transcription factors patterning their spatial expression, or delete entire enhancers. Regulatory elements, however, may in principle be silenced through other mechanisms, including changes in chromatin accessibility, or the emergence of repressive elements. Here, we show that an increase in chromatin accessibility at the pigmentation gene yellow, combined with the gain of a repressor site, underlie the evolutionary loss of a spot pigmentation pattern on the wings of a Drosophila species. The evolutionary gain of accessibility of this repressive element is regulated by E93, a transcription factor governing the progress of metamorphosis. This convoluted evolutionary scenario contrasts with the classical parsimonious mutational paths generally envisioned and often documented for morphological losses. It illustrates for the first time how evolutionary changes in chromatin accessibility may directly contribute to morphological diversification. We profiled chromatin accessibility at selected stages in the pupal wings of D. melanogaster and D. biarmipes using ATAC-seq.

ORGANISM(S): Drosophila melanogaster Drosophila biarmipes

PROVIDER: GSE222714 | GEO | 2023/02/17

REPOSITORIES: GEO

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Increased chromatin accessibility promotes the evolution of a transcriptional silencer in Drosophila [CUT&RUN]

Project description:The loss of discrete morphological traits, the most common evolutionary transition, is typically driven by changes in expression of developmental genes. Mutations accumulating in regulatory elements of these genes can disrupt DNA binding sites for transcription factors patterning their spatial expression, or delete entire enhancers. Regulatory elements, however, may in principle be silenced through other mechanisms, including changes in chromatin accessibility, or the emergence of repressive elements. Here, we show that an increase in chromatin accessibility at the pigmentation gene yellow, combined with the gain of a repressor site, underlie the evolutionary loss of a spot pigmentation pattern on the wings of a Drosophila species. The evolutionary gain of accessibility of this repressive element is regulated by E93, a transcription factor governing the progress of metamorphosis. This convoluted evolutionary scenario contrasts with the classical parsimonious mutational paths generally envisioned and often documented for morphological losses. It illustrates for the first time how evolutionary changes in chromatin accessibility may directly contribute to morphological diversification.

2023-02-17 | GSE222715 | GEO

Increased chromatin accessibility promotes the evolution of a transcriptional silencer in Drosophila [greenCUT&RUN]

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Expression of E93 provides an instructive cue to control dynamic enhancer activity and chromatin accessibility during development

Project description:How temporal cues combine with spatial inputs to control gene expression during development is poorly understood. Here, we test the hypothesis that the Drosophila transcription factor E93 controls temporal gene expression by regulating chromatin accessibility. Precocious expression of E93 early in wing development reveals that it can simultaneously activate and deactivate different target enhancers. Notably, the precocious patterns of enhancer activity resemble the wild-type patterns that occur later in development, suggesting that provision of E93 alters the competence of enhancers to respond to spatial cues. Genomic profiling reveals that precocious E93 expression is sufficient to regulate chromatin accessibility at a subset of its targets. These accessibility changes mimic those that normally occur later in development, indicating that precocious E93 accelerates the wild-type developmental program. Further, we find that target enhancers that do not respond to precocious E93 in early wings become responsive after a developmental transition, suggesting that parallel temporal pathways work alongside E93. These findings support a model wherein E93 expression functions as an instructive cue that defines a broad window of developmental time through control of chromatin accessibility.

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Mi-2 and E93 coordinate robust cell cycle exit with terminal differentiation through enhancer decommissioning [ATAC-seq]

Project description:Many postmitotic tissues coordinate robust cell cycle exit with the progression of terminal differentiation. While the signals involved in initiating cell cycle exit during terminal differentiation for some tissues have been described, less is known about the mechanisms that maintain a stable, non-cycling state. We previously found that chromatin accessibility changes at a subset of rate-limiting cell cycle genes occurs during maintenance of cell cycle exit, suggesting chromatin remodelers may play a key role in maintaining a robust postmitotic state during terminal differentiation. Here we show that the chromatin remodeler Mi-2 is required to ensure a stable, postmitotic state in Drosophila eyes and wings. Mi-2 alters chromatin accessibility and gene expression during cell cycle exit and terminal differentiation. Mi-2 and a transcription factor involved in tissue maturation, E93, close chromatin accessibility at an overlapping subset of potential enhancers that include the rate-limiting mitotic regulator string (cdc25c) and genes involved in the progression of terminal differentiation. E93 is also required for a stable, postmitotic state and we verified in vivo that Mi-2 and E93 cooperate to decommission an enhancer for the essential mitotic regulator string, to coordinate the transition to a postmitotic state with terminal differentiation. Enhancer decommissioning at the string locus provides a molecular explanation for the long-term, nearly irreversible postmitotic state observed in many tissues as terminal differentiation progresses.

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Project description:The diversity of forms in multicellular organisms originates largely from the spatial redeployment of genes expressed during development. Several scenarios explain the emergence of cis-regulatory elements that govern novel aspects of a gene expression pattern. One scenario, enhancer co-option, holds that a DNA sequence producing an ancestral regulatory activity also becomes the template for a new regulatory activity and shares regulatory information. While enhancer co-option might fuel morphological diversification, it has rarely been documented and the regulatory mechanisms underlying this evolutionary process are elusive. Here we show how a novel enhancer of the Drosophila pigmentation gene yellow, the spot enhancer, has co-opted the ancestral wing blade enhancer. We mapped the sequences driving each regulatory activity, ancestral and derived, and identified a shared core element necessary for DNA accessibility in this regulatory region. Our results suggest a model where a new enhancer emerges by co-opting accessibility information intrinsic to an older enhancer, and gaining transcription factor binding sites that diversify its spatial activity.

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ATAC-seq data of Amphimedon queenslandica (Demosponge species) through eight developmental stages, from white stage (cleavage) to adult

Project description:We report a comprehensive DNA accessibility profile of the Demosponge species Amphimedon queenslandica using Assay for Transposase-Accessible Chromatin with sequencing (ATAC-seq) through six embryonic developmental stages, a larval stage and adult stage. We assessed the dynamics of chromatin accessibility and identified 40,218 consensus peaks, 4,751 of them were differentially accessible in at least one developmental stage. Cis-regulatory elements were more dynamically regulated while proximal elements were more likely to be constitutively active. Furthermore, we identify a shift towards repressive chromatin in mid and late developmental stages which coincide with the increase in expression of genes of Metazoan origin. Finally, we show that cis-regulatory regions are differentially enriched in different Transcription Factor binding sites (TFBS) which demarcate three main stages of development and importantly, they are predictive of cis-regulatory regions in other animal species but not in Capsaspora owczarzaki, a close relative of animals.

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