Clustering of Drosophila housekeeping promoters facilitates their expression
- Marc Corrales1,2,4,
- Aránzazu Rosado1,2,4,
- Ruggero Cortini1,2,
- Joris van Arensbergen3,
- Bas van Steensel3 and
- Guillaume J. Filion1,2
- 1Centre for Genomic Regulation (CRG), The Barcelona Institute for Science and Technology, 08003 Barcelona, Spain;
- 2Universitat Pompeu Fabra (UPF), Barcelona, Spain;
- 3Division of Gene Regulation, Netherlands Cancer Institute (NKI), 1066CX Amsterdam, The Netherlands
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↵4 These authors contributed equally to this work.
Abstract
Housekeeping genes of animal genomes cluster in the same chromosomal regions. It has long been suggested that this organization contributes to their steady expression across all the tissues of the organism. Here, we show that the activity of Drosophila housekeeping gene promoters depends on the expression of their neighbors. By measuring the expression of ∼85,000 reporters integrated in Kc167 cells, we identified the best predictors of expression as chromosomal contacts with the promoters and terminators of active genes. Surprisingly, the chromatin composition at the insertion site and the contacts with enhancers were less informative. These results are substantiated by the existence of genomic “paradoxical” domains, rich in euchromatic features and enhancers, but where the reporters are expressed at low level, concomitant with a deficit of interactions with promoters and terminators. This indicates that the proper function of housekeeping genes relies not on contacts with long distance enhancers but on spatial clustering. Overall, our results suggest that spatial proximity between genes increases their expression and that the linear architecture of the Drosophila genome contributes to this effect.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.211433.116.
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Freely available online through the Genome Research Open Access option.
- Received June 15, 2016.
- Accepted April 12, 2017.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
