Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen

David E Torres; H Martin Kramer; Vittorio Tracanna; Gabriel L Fiorin; David E Cook; Michael F Seidl; Bart P H J Thomma

doi:10.1038/s41467-024-45884-x

Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen

David E Torres, H Martin Kramer, Vittorio Tracanna, Gabriel L Fiorin, David E Cook, Michael F Seidl^*, Bart P H J Thomma^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

The spatial organization of eukaryotic genomes is linked to their biological functions, although it is not clear how this impacts the overall evolution of a genome. Here, we uncover the three-dimensional (3D) genome organization of the phytopathogen Verticillium dahliae, known to possess distinct genomic regions, designated adaptive genomic regions (AGRs), enriched in transposable elements and genes that mediate host infection. Short-range DNA interactions form clear topologically associating domains (TADs) with gene-rich boundaries that show reduced levels of gene expression and reduced genomic variation. Intriguingly, TADs are less clearly insulated in AGRs than in the core genome. At a global scale, the genome contains bipartite long-range interactions, particularly enriched for AGRs and more generally containing segmental duplications. Notably, the patterns observed for V. dahliae are also present in other Verticillium species. Thus, our analysis links 3D genome organization to evolutionary features conserved throughout the Verticillium genus.

Original language	English
Article number	1701
Number of pages	14
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-45884-x
Publication status	Published - 24 Feb 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Funding

This work was supported by the Consejo Nacional de Ciencia y Tecnología, México to D.E.T. (scholarship no. 2018-000009-01EXTF-00188), by a PhD grant of the Research Council Earth and Life Sciences (project 831.15.002) to H.M.K., and by Human Frontier Science Program Postdoctoral Fellowship (HFSP, LT000627/2014-L), by USDA’s National Institute of Food and Agriculture (award no. 2018-67013-28492) through the Plant Biotic Interactions Program, and by the National Science Foundation (award no. 1936800) Division of Molecular and Cellular Biosciences to DEC. Work in the laboratories of M.F.S. and B.P.H.J.T. is supported by the Research Council Earth and Life Sciences (ALW) of the Netherlands Organization of Scientific Research (NWO). B.P.H.J.T. acknowledges funding by the Alexander von Humboldt Foundation in the framework of an Alexander von Humboldt Professorship endowed by the German Federal Ministry of Education and Research is furthermore supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2048/1 – Project ID: 390686111.

Funders	Funder number
Research Council Earth and Life Sciences	831.15.002
National Science Foundation	1936800
Division of Molecular and Cellular Biosciences
Alexander von Humboldt-Stiftung
National Institute of Food and Agriculture	2018-67013-28492
Human Frontier Science Program	LT000627/2014-L
Deutsche Forschungsgemeinschaft	EXC 2048/1, 390686111
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Consejo Nacional de Ciencia y Tecnología, Paraguay	2018-000009-01EXTF-00188

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abstract = "The spatial organization of eukaryotic genomes is linked to their biological functions, although it is not clear how this impacts the overall evolution of a genome. Here, we uncover the three-dimensional (3D) genome organization of the phytopathogen Verticillium dahliae, known to possess distinct genomic regions, designated adaptive genomic regions (AGRs), enriched in transposable elements and genes that mediate host infection. Short-range DNA interactions form clear topologically associating domains (TADs) with gene-rich boundaries that show reduced levels of gene expression and reduced genomic variation. Intriguingly, TADs are less clearly insulated in AGRs than in the core genome. At a global scale, the genome contains bipartite long-range interactions, particularly enriched for AGRs and more generally containing segmental duplications. Notably, the patterns observed for V. dahliae are also present in other Verticillium species. Thus, our analysis links 3D genome organization to evolutionary features conserved throughout the Verticillium genus.",

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Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen

Abstract

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