A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen

Genome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typ...

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Autores principales: Ursula Oggenfuss, Thomas Badet, Thomas Wicker, Fanny E Hartmann, Nikhil Kumar Singh, Leen Abraham, Petteri Karisto, Tiziana Vonlanthen, Christopher Mundt, Bruce A McDonald, Daniel Croll
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Publicado: eLife Sciences Publications Ltd 2021
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Acceso en línea:https://doaj.org/article/f8a534c8ab65452484980ce5e8202dff
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spelling oai:doaj.org-article:f8a534c8ab65452484980ce5e8202dff2021-11-26T11:14:45ZA population-level invasion by transposable elements triggers genome expansion in a fungal pathogen10.7554/eLife.692492050-084Xe69249https://doaj.org/article/f8a534c8ab65452484980ce5e8202dff2021-09-01T00:00:00Zhttps://elifesciences.org/articles/69249https://doaj.org/toc/2050-084XGenome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations, but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogen’s center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.Ursula OggenfussThomas BadetThomas WickerFanny E HartmannNikhil Kumar SinghLeen AbrahamPetteri KaristoTiziana VonlanthenChristopher MundtBruce A McDonaldDaniel CrolleLife Sciences Publications LtdarticleZymoseptoria triticitransposable elementsgenome evolutionpopulation genomicsfungiMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic Zymoseptoria tritici
transposable elements
genome evolution
population genomics
fungi
Medicine
R
Science
Q
Biology (General)
QH301-705.5
spellingShingle Zymoseptoria tritici
transposable elements
genome evolution
population genomics
fungi
Medicine
R
Science
Q
Biology (General)
QH301-705.5
Ursula Oggenfuss
Thomas Badet
Thomas Wicker
Fanny E Hartmann
Nikhil Kumar Singh
Leen Abraham
Petteri Karisto
Tiziana Vonlanthen
Christopher Mundt
Bruce A McDonald
Daniel Croll
A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
description Genome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations, but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogen’s center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.
format article
author Ursula Oggenfuss
Thomas Badet
Thomas Wicker
Fanny E Hartmann
Nikhil Kumar Singh
Leen Abraham
Petteri Karisto
Tiziana Vonlanthen
Christopher Mundt
Bruce A McDonald
Daniel Croll
author_facet Ursula Oggenfuss
Thomas Badet
Thomas Wicker
Fanny E Hartmann
Nikhil Kumar Singh
Leen Abraham
Petteri Karisto
Tiziana Vonlanthen
Christopher Mundt
Bruce A McDonald
Daniel Croll
author_sort Ursula Oggenfuss
title A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
title_short A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
title_full A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
title_fullStr A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
title_full_unstemmed A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
title_sort population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
publisher eLife Sciences Publications Ltd
publishDate 2021
url https://doaj.org/article/f8a534c8ab65452484980ce5e8202dff
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