Cited by 376Genomics and Chromatin DynamicsChromosomal and Genetic VariationsChromatin Remodeling and Cancer

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Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression

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Ghavi-Helm, Yad, Jankowski, Aleksander, Meiers, Sascha, Viales, Rebecca R., Korbel, Jan O., Furlong, Eileen E. M.·2019·Nature Genetics

DOI 10.1038/s41588-019-0462-3PMC PMC7116017

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Abstract

Chromatin topology is intricately linked to gene expression, yet its functional requirement remains unclear. Here, we comprehensively assessed the interplay between genome topology and gene expression using highly rearranged chromosomes (balancers) spanning ~75% of the Drosophila genome. Using transheterozyte (balancer/wild-type) embryos, we measured allele-specific changes in topology and gene expression in cis, while minimizing trans effects. Through genome sequencing, we resolved eight large nested inversions, smaller inversions, duplications and thousands of deletions. These extensive rearrangements caused many changes to chromatin topology, disrupting long-range loops, topologically associating domains (TADs) and promoter interactions, yet these are not predictive of changes in expression. Gene expression is generally not altered around inversion breakpoints, indicating that mis-appropriate enhancer-promoter activation is a rare event. Similarly, shuffling or fusing TADs, changing intra-TAD connections and disrupting long-range inter-TAD loops does not alter expression for the majority of genes. Our results suggest that properties other than chromatin topology ensure productive enhancer-promoter interactions.

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Additional file 5 of High-resolution Hi-C maps highlight multiscale chromatin architecture reorganization during cold stress in Brachypodium distachyon
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Additional file 3 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
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Additional file 6 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
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Additional file 3 of Depletion of lamins B1 and B2 promotes chromatin mobility and induces differential gene expression by a mesoscale-motion-dependent mechanism
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Additional file 1 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
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Additional file 2 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
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Additional file 7 of Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics
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Additional file 1 of β-actin mediated H3K27ac changes demonstrate the link between compartment switching and enhancer-dependent transcriptional regulation
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Additional file 1 of Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics
Bayless, K. M., Trautwein, M., Meusemann, K., Shin, S., Petersen, M., Donath, A., Podsiadłowski, L., Mayer, C., Niehuis, O., Peters, R. S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13788006
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Additional file 4 of Depletion of lamins B1 and B2 promotes chromatin mobility and induces differential gene expression by a mesoscale-motion-dependent mechanism
Pujadas-Liwag, E. M., Wei, X., Acosta, N., Carter, L. M., Yang, J., Almassalha, L. M., Jain, S., Daneshkhah, A., Rao, S. S. P., Seker-Polat, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26696604
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Additional file 5 of Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics
Bayless, K. M., Trautwein, M., Meusemann, K., Shin, S., Petersen, M., Donath, A., Podsiadłowski, L., Mayer, C., Niehuis, O., Peters, R. S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13788018
Additional file 2 of β-actin mediated H3K27ac changes demonstrate the link between compartment switching and enhancer-dependent transcriptional regulation
Mahmood, S. R., Said, N. H. E., Gunsalus, K. C., & Percipalle, P. (2024) · Figshare · doi:10.6084/m9.figshare.26564034
Additional file 1 of GRiNCH: simultaneous smoothing and detection of topological units of genome organization from sparse chromatin contact count matrices with matrix factorization
Lee, D.-I., & Roy, S. (2021) · Figshare · doi:10.6084/m9.figshare.14676788
Additional file 3 of β-actin mediated H3K27ac changes demonstrate the link between compartment switching and enhancer-dependent transcriptional regulation
Mahmood, S. R., Said, N. H. E., Gunsalus, K. C., & Percipalle, P. (2024) · Figshare · doi:10.6084/m9.figshare.26564037
Additional file 1 of Depletion of lamins B1 and B2 promotes chromatin mobility and induces differential gene expression by a mesoscale-motion-dependent mechanism
Pujadas-Liwag, E. M., Wei, X., Acosta, N., Carter, L. M., Yang, J., Almassalha, L. M., Jain, S., Daneshkhah, A., Rao, S. S. P., Seker-Polat, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26696595
Additional file 6 of Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics
Bayless, K. M., Trautwein, M., Meusemann, K., Shin, S., Petersen, M., Donath, A., Podsiadłowski, L., Mayer, C., Niehuis, O., Peters, R. S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13788021
Additional file 1 of Systematic assessment of gene co-regulation within chromatin domains determines differentially active domains across human cancers
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Additional file 7 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
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Additional file 5 of Depletion of lamins B1 and B2 promotes chromatin mobility and induces differential gene expression by a mesoscale-motion-dependent mechanism
Pujadas-Liwag, E. M., Wei, X., Acosta, N., Carter, L. M., Yang, J., Almassalha, L. M., Jain, S., Daneshkhah, A., Rao, S. S. P., Seker-Polat, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26696607
Additional file 10 of Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics
Bayless, K. M., Trautwein, M., Meusemann, K., Shin, S., Petersen, M., Donath, A., Podsiadłowski, L., Mayer, C., Niehuis, O., Peters, R. S., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13788003
Additional file 4 of GRiNCH: simultaneous smoothing and detection of topological units of genome organization from sparse chromatin contact count matrices with matrix factorization
Lee, D.-I., & Roy, S. (2021) · Figshare · doi:10.6084/m9.figshare.14676797
Additional file 3 of Chromatin spatial organization of wild type and mutant peanuts reveals high-resolution genomic architecture and interaction alterations
Zhang, X., Pandey, M. K., Wang, J., Zhao, K., Ma, X., Li, Z., Zhao, K., Gong, F., Guo, B. Z., Varshney, R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17030603
Additional file 4 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
Hunt, G., Vaid, R., Pirogov, S., Pfab, A., Ziegenhain, C., Sandberg, R., Reimegård, J., & Mannervik, M. (2024) · Figshare · doi:10.6084/m9.figshare.26658859
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Additional file 5 of Tissue-specific RNA Polymerase II promoter-proximal pause release and burst kinetics in a Drosophila embryonic patterning network
Hunt, G., Vaid, R., Pirogov, S., Pfab, A., Ziegenhain, C., Sandberg, R., Reimegård, J., & Mannervik, M. (2024) · Figshare · doi:10.6084/m9.figshare.26658862
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Authors: Ghavi-Helm, Y., Jankowski, A., Meiers, S., Viales, R. R., Korbel, J. O., & Furlong, E. E. M.
Affiliations: Lyon 1 Université (FR)
European Molecular Biology Laboratory (DE)
Corresponding author: Ghavi-Helm, Yad
Korbel, Jan O.
Furlong, Eileen E. M.
ORCID: Ghavi-Helm, Yad
Jankowski, Aleksander
Meiers, Sascha
Viales, Rebecca R.
Korbel, Jan O.
Furlong, Eileen E. M.
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2019-07-15
Volume: 51
Issue: 8
Pages: 1272-1282
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/s41588-019-0462-3
PMC: PMC7116017
OpenAlex: W2958578938
Cited by: 354
References: 57
Citations by year: 2026: 16 · 2025: 33 · 2024: 41 · 2023: 54 · 2022: 60 · 2021: 74 · 2020: 56 · 2019: 19
FWCI: 17.94
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
HAL (submittedVersion)
Funders: Nature
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: chromatin topology, gene expression, balancer chromosomes, chromosomal inversions, topologically associating domains, enhancer-promoter interactions, cis effect, Drosophila, chromosomal duplication, chromosomal deletion
MeSH terms: Animals, Chromatin, Chromosome Mapping, Drosophila melanogaster, Enhancer Elements, Genetic, Female, Gene Expression Regulation, Male, Promoter Regions, Genetic, Gene Rearrangement, Genome, Insect, Chromosomes, Insect

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Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression

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