Impact of DNA methylation on 3D genome structure

Diana Buitrago, Mireia Labrador, Juan Pablo Arcon, Rafael Lema, Oscar Flores, Anna Esteve-Codina, Julie Blanc, Nuria Villegas, David Bellido, Marta Gut, Pablo D. Dans, Simon C. Heath, Ivo G. Gut, Isabelle Brun Heath () and Modesto Orozco ()
Additional contact information
Diana Buitrago: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Mireia Labrador: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Juan Pablo Arcon: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Rafael Lema: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Oscar Flores: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Anna Esteve-Codina: CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Julie Blanc: CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Nuria Villegas: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
David Bellido: Universitat de Barcelona
Marta Gut: CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Pablo D. Dans: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Simon C. Heath: CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Ivo G. Gut: CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Isabelle Brun Heath: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)
Modesto Orozco: Institute for Research in Biomedicine (IRB Barcelona) - The Barcelona Institute of Science and Technology (BIST)

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract Determining the effect of DNA methylation on chromatin structure and function in higher organisms is challenging due to the extreme complexity of epigenetic regulation. We studied a simpler model system, budding yeast, that lacks DNA methylation machinery making it a perfect model system to study the intrinsic role of DNA methylation in chromatin structure and function. We expressed the murine DNA methyltransferases in Saccharomyces cerevisiae and analyzed the correlation between DNA methylation, nucleosome positioning, gene expression and 3D genome organization. Despite lacking the machinery for positioning and reading methylation marks, induced DNA methylation follows a conserved pattern with low methylation levels at the 5’ end of the gene increasing gradually toward the 3’ end, with concentration of methylated DNA in linkers and nucleosome free regions, and with actively expressed genes showing low and high levels of methylation at transcription start and terminating sites respectively, mimicking the patterns seen in mammals. We also see that DNA methylation increases chromatin condensation in peri-centromeric regions, decreases overall DNA flexibility, and favors the heterochromatin state. Taken together, these results demonstrate that methylation intrinsically modulates chromatin structure and function even in the absence of cellular machinery evolved to recognize and process the methylation signal.

Date: 2021
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DOI: 10.1038/s41467-021-23142-8

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