Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen

Abstract Genomes of clonally reproducing fungal pathogens are often compartmentalized into conserved core and lineage-specific accessory regions (ARs), enriched in transposable elements (TEs). ARs and TEs are thought to promote pathogen adaptation, but direct experimental evidence is sparse. Using a...

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Published in:Nature Communications
Main Authors: Cristina López Díaz, Dilay Hazal Ayhan, Ana Rodríguez López, Lucía Gómez Gil, Li-Jun Ma, Antonio Di Pietro
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Online Access:https://doi.org/10.1038/s41467-025-62213-y
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author Cristina López Díaz
Dilay Hazal Ayhan
Ana Rodríguez López
Lucía Gómez Gil
Li-Jun Ma
Antonio Di Pietro
author_facet Cristina López Díaz
Dilay Hazal Ayhan
Ana Rodríguez López
Lucía Gómez Gil
Li-Jun Ma
Antonio Di Pietro
author_sort Cristina López Díaz
collection DOAJ
container_title Nature Communications
description Abstract Genomes of clonally reproducing fungal pathogens are often compartmentalized into conserved core and lineage-specific accessory regions (ARs), enriched in transposable elements (TEs). ARs and TEs are thought to promote pathogen adaptation, but direct experimental evidence is sparse. Using an evolve and re-sequence approach, we found that serial passaging of the cross-kingdom fungal pathogen Fusarium oxysporum through tomato plants or axenic media rapidly increased fitness under the selection condition. TE insertions were the predominant type of mutations in the evolved lines, with a single non-autonomous hAT-type TE accounting for 63% of total events detected. TEs are inserted preferentially at sites of histone H3 lysine 27 trimethylation, a hallmark of ARs. Recurrent evolutionary trajectories during plate adaptation led to increased proliferation concomitant with reduced virulence. Unexpectedly, adaptive mutations in accessory genes strongly impacted core functions such as growth, development, quorum sensing, or virulence. Thus, TEs and ARs drive rapid adaptation in this important fungal pathogen.
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spelling doaj-art-ca3425cb09ea4d5ca46ab85f7976e2b12025-08-20T03:05:10ZengNature PortfolioNature Communications2041-17232025-07-0116111610.1038/s41467-025-62213-yTransposons and accessory genes drive adaptation in a clonally evolving fungal pathogenCristina López Díaz0Dilay Hazal Ayhan1Ana Rodríguez López2Lucía Gómez Gil3Li-Jun Ma4Antonio Di Pietro5Departamento de Genética, Campus de Excelencia Internacional Agroalimentario ceiA3, Universidad de CórdobaDepartment of Biochemistry and Molecular Biology, University of Massachusetts AmherstDepartamento de Genética, Campus de Excelencia Internacional Agroalimentario ceiA3, Universidad de CórdobaDepartamento de Genética, Campus de Excelencia Internacional Agroalimentario ceiA3, Universidad de CórdobaDepartment of Biochemistry and Molecular Biology, University of Massachusetts AmherstDepartamento de Genética, Campus de Excelencia Internacional Agroalimentario ceiA3, Universidad de CórdobaAbstract Genomes of clonally reproducing fungal pathogens are often compartmentalized into conserved core and lineage-specific accessory regions (ARs), enriched in transposable elements (TEs). ARs and TEs are thought to promote pathogen adaptation, but direct experimental evidence is sparse. Using an evolve and re-sequence approach, we found that serial passaging of the cross-kingdom fungal pathogen Fusarium oxysporum through tomato plants or axenic media rapidly increased fitness under the selection condition. TE insertions were the predominant type of mutations in the evolved lines, with a single non-autonomous hAT-type TE accounting for 63% of total events detected. TEs are inserted preferentially at sites of histone H3 lysine 27 trimethylation, a hallmark of ARs. Recurrent evolutionary trajectories during plate adaptation led to increased proliferation concomitant with reduced virulence. Unexpectedly, adaptive mutations in accessory genes strongly impacted core functions such as growth, development, quorum sensing, or virulence. Thus, TEs and ARs drive rapid adaptation in this important fungal pathogen.https://doi.org/10.1038/s41467-025-62213-y
spellingShingle Cristina López Díaz
Dilay Hazal Ayhan
Ana Rodríguez López
Lucía Gómez Gil
Li-Jun Ma
Antonio Di Pietro
Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title_full Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title_fullStr Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title_full_unstemmed Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title_short Transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
title_sort transposons and accessory genes drive adaptation in a clonally evolving fungal pathogen
url https://doi.org/10.1038/s41467-025-62213-y
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