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

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.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE222715 | GEO | 2023/02/17

REPOSITORIES: GEO

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Increased chromatin accessibility promotes the evolution of a transcriptional silencer in Drosophila [greenCUT&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 | GSE222716 | GEO

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

2023-02-17 | GSE222714 | GEO

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.

2020-02-25 | GSE141738 | GEO

Evolutionary co-option of a Drosophila enhancer of the yellow gene through shared chromatin accessibility input

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.

2020-07-28 | GSE142176 | GEO

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.

2021-10-10 | E-MTAB-10203 | biostudies-arrayexpress

Chromatin remodeling and expression dynamics reveal conserved and species-specific regulation during mouse and chicken limb development [RNA-seq]

Project description:Understanding the origin of morphological diversity across vertebrates is central to evolutionary developmental biology. cis-regulatory elements (CRE) such as enhancers and promoters interpret precise spatiotemporal cues to control and coordinate gene expression. To get insights into both conserved and species-specific variations during early limb patterning and outgrowth, we leverage genome-wide comprehensive assessment of chromatin accessibility and transcriptional changes during mouse forelimb and chicken wing bud development. Our analysis reveals temporal modulation of chromatin accessibility and expression as well as their temporal relationship during the progression of mouse forelimb and chicken wing bud development. Transcription factor binding site enrichment analysis and putative TF occupancy as inferred by integrating TF binding motifs and chromatin accessibility information reveal temporal TF-DNA interactions during forelimb/wing bud patterning. Finally, the integration of accessibility, expression, and TF binding site information allowed to identify candidate gene targets of HAND2 and GLI3 that include conserved as well as species-specific transcriptional regulator-gene interactions.

2021-07-31 | GSE164737 | GEO

Chromatin remodeling and expression dynamics reveal conserved and species-specific regulation during mouse and chicken limb development [ATAC-seq]

2021-07-31 | GSE164736 | GEO

Evolution of diapause in the African killifish by remodeling ancient gene regulatory landscape

Project description:Suspended animation (e.g. hibernation, diapause) allows organisms to survive extreme environments. But the mechanisms underlying the evolution of suspended animation states are unknown. The African turquoise killifish has evolved diapause as a form of suspended development to survive the complete drought that occurs every summer. Here, we show that gene duplicates – paralogs – exhibit specialized expression in diapause compared to normal development in the African turquoise killifish. Surprisingly, paralogs with specialized expression in diapause are evolutionarily very ancient and are present even in vertebrates that do not exhibit diapause. To determine if evolution of diapause is due to the regulatory landscape rewiring at ancient paralogs, we assessed chromatin accessibility genome-wide in fish species with or without diapause. This analysis revealed an evolutionary recent increase in chromatin accessibility at very ancient paralogs in African turquoise killifish. The increase in chromatin accessibility is linked to the presence of new binding sites for transcription factors, likely due to de novo mutations and transposable element (TE) insertion. Interestingly, accessible chromatin regions in diapause are enriched for lipid metabolism genes, and our lipidomics studies uncover a striking difference in lipid species in African turquoise killifish diapause, which could be critical for long-term survival. Together, our results show that diapause likely originated by repurposing pre-existing gene programs via recent changes in the regulatory landscape. This work raises the possibility that suspended animation programs could be reactivated in other species for long-term preservation via transcription factor remodeling and suggests a mechanism for how complex adaptations evolve in nature.

2021-08-05 | ST001898 | MetabolomicsWorkbench

Hormone-dependent control of developmental timing through regulation of chromatin accessibility

Project description:We identify a temporal cascade of ecdysone-inducible transcription factor gene expression during Drosophila wing development. This temporal cascade corresponds with dynamic changes in chromatin accesibility during wing development. We hypothesized that these temporally regulated transcription factors may coordinate these dynamic open chromatin changes. To test this, we investigate the ecdysone-inducible transcription factor, E93, which we determine is required for coordinating transitions in developmental stage by regulating chromatin accesibility of cis-regulatory elements.

2017-06-06 | GSE97956 | GEO

TE-associated chromatin variation in mice livers

Project description:Chromatin accessibility is a hallmark of active regulatory function in the genome and variation of chromatin accessibility across individuals has been shown to contribute to complex traits and disease susceptibility. However, the mechanisms responsible for chromatin variation among different individuals and how this variation contributes to phenotypic diversity remain poorly understood. We examined chromatin accessibility variation in liver tissue from seven strains of adult mice that have phenotypic diversity in response to a high-fat/high-sucrose diet. Remarkably, nearly 40% of the loci with the greatest degree of chromatin variability across the strains are associated with transposable elements (TEs), with evolutionarily younger TEs being particularly enriched for regions of chromatin variation. We found that evolutionary younger and older TEs have differential chromatin accessibility profiles and are enriched for binding sites of different transcription factors, indicating the role of TEs in the evolution of regulatory networks in the liver. We also demonstrate that TE polymorphisms and epigenetic regulation of TEs contribute to regulatory variation across different strains through providing binding sites for liver transcription factors. Intriguingly, variable chromatin loci that are associated with liver metabolism are primarily TE-associated. We demonstrate that TEs contribute to regulatory variation in liver and have downstream effects on metabolism. Our data reveal TEs as a novel and important contributor to regulatory and phenotypic variation in the liver and suggest that regulatory variation at TEs is a major contributor to phenotypic variation in populations. Examination of chromatin accessibility with FAIRE-seq in livers of male mice (A/J, AKR/J, BALB/cJ, C57BL/6J, C3H/HeJ, CBA/J, DBA/2J, BXH2/TyJ, and BXH19/TyJ) fed a high-fat, high-sucrose diet.

2016-07-14 | E-GEOD-75770 | biostudies-arrayexpress

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