Chromatin loops are an ancestral hallmark of the animal regulatory genome

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  • dc.contributor.author Kim, Iana V.
  • dc.contributor.author Navarrete Hernández, Cristina
  • dc.contributor.author Grau Bové, Xavier
  • dc.contributor.author Iglesias, Marta
  • dc.contributor.author Elek, Anamaria
  • dc.contributor.author Zolotarov, Grygoriy
  • dc.contributor.author Bykov, Nikolai S.
  • dc.contributor.author Montgomery, Sean A.
  • dc.contributor.author Ksiezopolska, Ewa
  • dc.contributor.author Cañas Armenteros, Didac
  • dc.contributor.author Soto-Angel, Joan J.
  • dc.contributor.author Leys, Sally P.
  • dc.contributor.author Burkhardt, Pawel
  • dc.contributor.author Suga, Hiroshi
  • dc.contributor.author Mendoza, Alex de
  • dc.contributor.author Marti-Renom, Marc A.
  • dc.contributor.author Sebé-Pedrós, Arnau
  • dc.date.accessioned 2025-09-05T06:25:22Z
  • dc.date.available 2025-09-05T06:25:22Z
  • dc.date.issued 2025
  • dc.description.abstract In bilaterian animals, gene regulation is shaped by a combination of linear and spatial regulatory information. Regulatory elements along the genome are integrated into gene regulatory landscapes through chromatin compartmentalization1,2, insulation of neighbouring genomic regions3,4 and chromatin looping that brings together distal cis-regulatory sequences5. However, the evolution of these regulatory features is unknown because the three-dimensional genome architecture of most animal lineages remains unexplored6,7. To trace the evolutionary origins of animal genome regulation, here we characterized the physical organization of the genome in non-bilaterian animals (sponges, ctenophores, placozoans and cnidarians)8,9 and their closest unicellular relatives (ichthyosporeans, filastereans and choanoflagellates)10 by combining high-resolution chromosome conformation capture11,12 with epigenomic marks and gene expression data. Our comparative analysis showed that chromatin looping is a conserved feature of genome architecture in ctenophores, placozoans and cnidarians. These sequence-determined distal contacts involve both promoter-enhancer and promoter-promoter interactions. By contrast, chromatin loops are absent in the unicellular relatives of animals. Our findings indicate that spatial genome regulation emerged early in animal evolution. This evolutionary innovation introduced regulatory complexity, ultimately facilitating the diversification of animal developmental programmes and cell type repertoires.
  • dc.description.sponsorship We thank I. Maeso and M. Irimia for critical comments on the manuscript. We thank A. Hino and S. Denbo for greatly helping us to re-sequence and annotate the Capsaspora genome de novo. We are very grateful to S. B. Johnson, S. Haddock, MBARI and the David and Lucile Packard Foundation for sending us H. californensis samples. Research in A.S-P.’s group was supported by the European Research Council (grant no. ERC-StG 851647) and the Spanish Ministry of Science and Innovation (grant no. PID2021-124757NB-I00). I.V.K. was supported by a Juan de la Cierva postdoctoral fellowship (grant no. FJC2020-043131-I) from the Spanish Ministry of Science and Innovation. X.G.-B. is supported by the European Union’s H2020 research and innovation programme under Marie Sklodowska-Curie grant agreement no. 101031767. A.E. and C.N. are supported by FPI PhD fellowships from the Spanish Ministry of Science and Innovation. S.A.M. is supported by the EMBO postdoctoral fellowship grant no. ALTF 066-2022. H.S. acknowledges the financing support from MEXT/JSPS KAKENHI grant no. JP22K06343 and PUH Research Grant Programmes in 2015 and 2016. S.P.L. was supported by NSERC Discovery grant (no. 2016-15446). J.J.S.-A. and P.B. were supported by the Michael Sars Centre core budget from the University of Bergen. A.d.M. is supported by the European Research Council (grant no. ERC-StG 950230). M.A.M.-R. acknowledges support by the Spanish Ministerio de Ciencia e Innovación (grant no. PID2020-115696RB-I00).
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Kim IV, Navarrete C, Grau-Bové X, Iglesias M, Elek A, Zolotarov G, et al. Chromatin loops are an ancestral hallmark of the animal regulatory genome. Nature. 2025 Jun;642(8069):1097-105. DOI: 10.1038/s41586-025-08960-w
  • dc.identifier.doi http://dx.doi.org/10.1038/s41586-025-08960-w
  • dc.identifier.issn 0028-0836
  • dc.identifier.uri http://hdl.handle.net/10230/71118
  • dc.language.iso eng
  • dc.publisher Nature Research
  • dc.relation.ispartof Nature. 2025 Jun;642(8069):1097-105
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/851647
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-124757NB-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/101031767
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/950230
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2020-115696RB-I00
  • dc.rights © The Author(s) 2025. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.keyword Chromatin structure
  • dc.subject.keyword Comparative genomics
  • dc.subject.keyword Evolution
  • dc.subject.keyword Gene regulation
  • dc.title Chromatin loops are an ancestral hallmark of the animal regulatory genome
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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