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Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation
The tight interaction between pathogens and their hosts results in reciprocal selective forces that impact the genetic diversity of the interacting species. The footprints of this selection differ between pathosystems because of distinct life-history traits, demographic histories, or genome architec...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8120014/ https://www.ncbi.nlm.nih.gov/pubmed/33837781 http://dx.doi.org/10.1093/gbe/evab073 |
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author | Schweizer, Gabriel Haider, Muhammad Bilal Barroso, Gustavo V Rössel, Nicole Münch, Karin Kahmann, Regine Dutheil, Julien Y |
author_facet | Schweizer, Gabriel Haider, Muhammad Bilal Barroso, Gustavo V Rössel, Nicole Münch, Karin Kahmann, Regine Dutheil, Julien Y |
author_sort | Schweizer, Gabriel |
collection | PubMed |
description | The tight interaction between pathogens and their hosts results in reciprocal selective forces that impact the genetic diversity of the interacting species. The footprints of this selection differ between pathosystems because of distinct life-history traits, demographic histories, or genome architectures. Here, we studied the genome-wide patterns of genetic diversity of 22 isolates of the causative agent of the corn smut disease, Ustilago maydis, originating from five locations in Mexico, the presumed center of origin of this species. In this species, many genes encoding secreted effector proteins reside in so-called virulence clusters in the genome, an arrangement that is so far not found in other filamentous plant pathogens. Using a combination of population genomic statistical analyses, we assessed the geographical, historical, and genome-wide variation of genetic diversity in this fungal pathogen. We report evidence of two partially admixed subpopulations that are only loosely associated with geographic origin. Using the multiple sequentially Markov coalescent model, we inferred the demographic history of the two pathogen subpopulations over the last 0.5 Myr. We show that both populations experienced a recent strong bottleneck starting around 10,000 years ago, coinciding with the assumed time of maize domestication. Although the genome average genetic diversity is low compared with other fungal pathogens, we estimated that the rate of nonsynonymous adaptive substitutions is three times higher in genes located within virulence clusters compared with nonclustered genes, including nonclustered effector genes. These results highlight the role that these singular genomic regions play in the evolution of this pathogen. |
format | Online Article Text |
id | pubmed-8120014 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-81200142021-05-19 Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation Schweizer, Gabriel Haider, Muhammad Bilal Barroso, Gustavo V Rössel, Nicole Münch, Karin Kahmann, Regine Dutheil, Julien Y Genome Biol Evol Research Article The tight interaction between pathogens and their hosts results in reciprocal selective forces that impact the genetic diversity of the interacting species. The footprints of this selection differ between pathosystems because of distinct life-history traits, demographic histories, or genome architectures. Here, we studied the genome-wide patterns of genetic diversity of 22 isolates of the causative agent of the corn smut disease, Ustilago maydis, originating from five locations in Mexico, the presumed center of origin of this species. In this species, many genes encoding secreted effector proteins reside in so-called virulence clusters in the genome, an arrangement that is so far not found in other filamentous plant pathogens. Using a combination of population genomic statistical analyses, we assessed the geographical, historical, and genome-wide variation of genetic diversity in this fungal pathogen. We report evidence of two partially admixed subpopulations that are only loosely associated with geographic origin. Using the multiple sequentially Markov coalescent model, we inferred the demographic history of the two pathogen subpopulations over the last 0.5 Myr. We show that both populations experienced a recent strong bottleneck starting around 10,000 years ago, coinciding with the assumed time of maize domestication. Although the genome average genetic diversity is low compared with other fungal pathogens, we estimated that the rate of nonsynonymous adaptive substitutions is three times higher in genes located within virulence clusters compared with nonclustered genes, including nonclustered effector genes. These results highlight the role that these singular genomic regions play in the evolution of this pathogen. Oxford University Press 2021-04-10 /pmc/articles/PMC8120014/ /pubmed/33837781 http://dx.doi.org/10.1093/gbe/evab073 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Schweizer, Gabriel Haider, Muhammad Bilal Barroso, Gustavo V Rössel, Nicole Münch, Karin Kahmann, Regine Dutheil, Julien Y Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title | Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title_full | Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title_fullStr | Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title_full_unstemmed | Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title_short | Population Genomics of the Maize Pathogen Ustilago maydis: Demographic History and Role of Virulence Clusters in Adaptation |
title_sort | population genomics of the maize pathogen ustilago maydis: demographic history and role of virulence clusters in adaptation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8120014/ https://www.ncbi.nlm.nih.gov/pubmed/33837781 http://dx.doi.org/10.1093/gbe/evab073 |
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