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Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen

The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi have evolved highly sophisticated genomic defences to reduce TE proliferation ac...

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Autores principales: Pereira, Danilo, Oggenfuss, Ursula, McDonald, Bruce A., Croll, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549362/
https://www.ncbi.nlm.nih.gov/pubmed/34424154
http://dx.doi.org/10.1099/mgen.0.000540
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author Pereira, Danilo
Oggenfuss, Ursula
McDonald, Bruce A.
Croll, Daniel
author_facet Pereira, Danilo
Oggenfuss, Ursula
McDonald, Bruce A.
Croll, Daniel
author_sort Pereira, Danilo
collection PubMed
description The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi have evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point mutation (RIP) is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIPs is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyse 366 whole-genome sequences of Parastagonospora nodorum, a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression.
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spelling pubmed-85493622021-10-27 Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen Pereira, Danilo Oggenfuss, Ursula McDonald, Bruce A. Croll, Daniel Microb Genom Research Articles The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi have evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point mutation (RIP) is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIPs is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyse 366 whole-genome sequences of Parastagonospora nodorum, a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression. Microbiology Society 2021-08-23 /pmc/articles/PMC8549362/ /pubmed/34424154 http://dx.doi.org/10.1099/mgen.0.000540 Text en © 2021 The Authors https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
spellingShingle Research Articles
Pereira, Danilo
Oggenfuss, Ursula
McDonald, Bruce A.
Croll, Daniel
Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title_full Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title_fullStr Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title_full_unstemmed Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title_short Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
title_sort population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549362/
https://www.ncbi.nlm.nih.gov/pubmed/34424154
http://dx.doi.org/10.1099/mgen.0.000540
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