DNA sequence encodes the position of DNA supercoils

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Abstract

The three-dimensional organization of DNA is increasingly understood to play a decisive role in vital cellular processes. Many studies focus on the role of DNA-packaging proteins, crowding, and confinement in arranging chromatin, but structural information might also be directly encoded in bare DNA itself. Here we visualize plectonemes (extended intertwined DNA structures formed upon supercoiling) on individual DNA molecules. Remarkably, our experiments show that the DNA sequence directly encodes the structure of supercoiled DNA by pinning plectonemes at specific sequences. We develop a physical model that predicts that sequence-dependent intrinsic curvature is the key determinant of pinning strength and demonstrate this simple model provides very good agreement with the data. Analysis of several prokaryotic genomes indicates that plectonemes localize directly upstream of promoters, which we experimentaly confirm for selected promotor sequences. Our findings reveal a hidden code in the genome that helps to spatially organize the chromosomal DNA.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. The previously published genome data for E. coli used in Figure 4B can be accessed here http://regulondb.ccg.unam.mx/menu/download/datasets/files/PromoterSet.txt; V. cholerae here http://www.pnas.org/highwire/filestream/618514/field_highwire_adjunct_files/2/pnas.1500203112.sd02.xlsx; B. methanolicus here https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4342826/bin/12864_2015_1239_MOESM2_ESM.xlsx; M. tuberculosis here https://ars.els-cdn.com/content/image/1-s2.0-S2211124713006153-mmc2.xlsx; and C. crescentus here https://doi.org/10.1371/journal.pgen.1004831.s012. The previously published genome data for D. melanogaster, C. elegans, A. thaliana, S. cerevisiae, and S. pombe used in Figure 4E can be accessed using the Eukaryotic Promotor Database (https://epd.vital-it.ch).

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Article and author information

Author details

Sung Hyun Kim

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9272-7036
Mahipal Ganji

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

Competing interests
The authors declare that no competing interests exist.
Eugene Kim

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

Competing interests
The authors declare that no competing interests exist.
Jaco van der Torre

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

Competing interests
The authors declare that no competing interests exist.
Elio Abbondanzieri

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

For correspondence
elio.abbondanzieri@rochester.edu

Competing interests
The authors declare that no competing interests exist.
Cees Dekker

Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

For correspondence
C.Dekker@tudelft.nl

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6273-071X

Funding

H2020 European Research Council (669598)

Cees Dekker

The Netherlands Organization for Scientific Research (the Frontiers of Nanoscience program)

Elio Abbondanzieri

H2020 European Research Council (304284)

Elio Abbondanzieri

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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