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Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities

Many species of fungal plant pathogens coexist as multiple lineages on the same host, but the factors underlying the origin and maintenance of population structure remain largely unknown. The rice blast fungus Pyricularia oryzae is a widespread model plant pathogen displaying population subdivision....

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Autores principales: Thierry, Maud, Charriat, Florian, Milazzo, Joëlle, Adreit, Henri, Ravel, Sébastien, Cros-Arteil, Sandrine, borron, Sonia, Sella, Violaine, Kroj, Thomas, Ioos, Renaud, Fournier, Elisabeth, Tharreau, Didier, Gladieux, Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352207/
https://www.ncbi.nlm.nih.gov/pubmed/35877779
http://dx.doi.org/10.1371/journal.ppat.1010687
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author Thierry, Maud
Charriat, Florian
Milazzo, Joëlle
Adreit, Henri
Ravel, Sébastien
Cros-Arteil, Sandrine
borron, Sonia
Sella, Violaine
Kroj, Thomas
Ioos, Renaud
Fournier, Elisabeth
Tharreau, Didier
Gladieux, Pierre
author_facet Thierry, Maud
Charriat, Florian
Milazzo, Joëlle
Adreit, Henri
Ravel, Sébastien
Cros-Arteil, Sandrine
borron, Sonia
Sella, Violaine
Kroj, Thomas
Ioos, Renaud
Fournier, Elisabeth
Tharreau, Didier
Gladieux, Pierre
author_sort Thierry, Maud
collection PubMed
description Many species of fungal plant pathogens coexist as multiple lineages on the same host, but the factors underlying the origin and maintenance of population structure remain largely unknown. The rice blast fungus Pyricularia oryzae is a widespread model plant pathogen displaying population subdivision. However, most studies of natural variation in P. oryzae have been limited in genomic or geographic resolution, and host adaptation is the only factor that has been investigated extensively as a contributor to population subdivision. In an effort to complement previous studies, we analyzed genetic and phenotypic diversity in isolates of the rice blast fungus covering a broad geographical range. Using single-nucleotide polymorphism genotyping data for 886 isolates sampled from 152 sites in 51 countries, we showed that population subdivision of P. oryzae in one recombining and three clonal lineages with broad distributions persisted with deeper sampling. We also extended previous findings by showing further population subdivision of the recombining lineage into one international and three Asian clusters, and by providing evidence that the three clonal lineages of P. oryzae were found in areas with different prevailing environmental conditions, indicating niche separation. Pathogenicity tests and bioinformatic analyses using an extended set of isolates and rice varieties indicated that partial specialization to rice subgroups contributed to niche separation between lineages, and differences in repertoires of putative virulence effectors were consistent with differences in host range. Experimental crosses revealed that female sterility and early post-mating genetic incompatibilities acted as strong additional barriers to gene flow between clonal lineages. Our results demonstrate that the spread of a fungal pathogen across heterogeneous habitats and divergent populations of a crop species can lead to niche separation and reproductive isolation between distinct, widely distributed, lineages.
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spelling pubmed-93522072022-08-05 Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities Thierry, Maud Charriat, Florian Milazzo, Joëlle Adreit, Henri Ravel, Sébastien Cros-Arteil, Sandrine borron, Sonia Sella, Violaine Kroj, Thomas Ioos, Renaud Fournier, Elisabeth Tharreau, Didier Gladieux, Pierre PLoS Pathog Research Article Many species of fungal plant pathogens coexist as multiple lineages on the same host, but the factors underlying the origin and maintenance of population structure remain largely unknown. The rice blast fungus Pyricularia oryzae is a widespread model plant pathogen displaying population subdivision. However, most studies of natural variation in P. oryzae have been limited in genomic or geographic resolution, and host adaptation is the only factor that has been investigated extensively as a contributor to population subdivision. In an effort to complement previous studies, we analyzed genetic and phenotypic diversity in isolates of the rice blast fungus covering a broad geographical range. Using single-nucleotide polymorphism genotyping data for 886 isolates sampled from 152 sites in 51 countries, we showed that population subdivision of P. oryzae in one recombining and three clonal lineages with broad distributions persisted with deeper sampling. We also extended previous findings by showing further population subdivision of the recombining lineage into one international and three Asian clusters, and by providing evidence that the three clonal lineages of P. oryzae were found in areas with different prevailing environmental conditions, indicating niche separation. Pathogenicity tests and bioinformatic analyses using an extended set of isolates and rice varieties indicated that partial specialization to rice subgroups contributed to niche separation between lineages, and differences in repertoires of putative virulence effectors were consistent with differences in host range. Experimental crosses revealed that female sterility and early post-mating genetic incompatibilities acted as strong additional barriers to gene flow between clonal lineages. Our results demonstrate that the spread of a fungal pathogen across heterogeneous habitats and divergent populations of a crop species can lead to niche separation and reproductive isolation between distinct, widely distributed, lineages. Public Library of Science 2022-07-25 /pmc/articles/PMC9352207/ /pubmed/35877779 http://dx.doi.org/10.1371/journal.ppat.1010687 Text en © 2022 Thierry et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Thierry, Maud
Charriat, Florian
Milazzo, Joëlle
Adreit, Henri
Ravel, Sébastien
Cros-Arteil, Sandrine
borron, Sonia
Sella, Violaine
Kroj, Thomas
Ioos, Renaud
Fournier, Elisabeth
Tharreau, Didier
Gladieux, Pierre
Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title_full Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title_fullStr Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title_full_unstemmed Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title_short Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
title_sort maintenance of divergent lineages of the rice blast fungus pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352207/
https://www.ncbi.nlm.nih.gov/pubmed/35877779
http://dx.doi.org/10.1371/journal.ppat.1010687
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