Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>

ABSTRACT Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal biodiversity and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multihost pathogen that i...

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Autores principales:	Pierre Gladieux, Bradford Condon, Sebastien Ravel, Darren Soanes, Joao Leodato Nunes Maciel, Antonio Nhani, Li Chen, Ryohei Terauchi, Marc-Henri Lebrun, Didier Tharreau, Thomas Mitchell, Kerry F. Pedley, Barbara Valent, Nicholas J. Talbot, Mark Farman, Elisabeth Fournier
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	cryptic species disease emergence diversification fungal pathogen gene flow population structure Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/015378b8448940198a809435624b1dde
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spelling	oai:doaj.org-article:015378b8448940198a809435624b1dde2021-11-15T15:53:25ZGene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>10.1128/mBio.01219-172150-7511https://doaj.org/article/015378b8448940198a809435624b1dde2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01219-17https://doaj.org/toc/2150-7511ABSTRACT Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal biodiversity and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multihost pathogen that infects multiple grasses and cereals, is responsible for the most damaging rice disease (rice blast), and is of growing concern due to the recent introduction of wheat blast to Bangladesh from South America. However, the genetic structure and evolutionary history of M. oryzae, including the possible existence of cryptic phylogenetic species, remain poorly defined. Here, we use whole-genome sequence information for 76 M. oryzae isolates sampled from 12 grass and cereal genera to infer the population structure of M. oryzae and to reassess the species status of wheat-infecting populations of the fungus. Species recognition based on genealogical concordance, using published data or extracting previously used loci from genome assemblies, failed to confirm a prior assignment of wheat blast isolates to a new species (Pyricularia graminis-tritici). Inference of population subdivisions revealed multiple divergent lineages within M. oryzae, each preferentially associated with one host genus, suggesting incipient speciation following host shift or host range expansion. Analyses of gene flow, taking into account the possibility of incomplete lineage sorting, revealed that genetic exchanges have contributed to the makeup of multiple lineages within M. oryzae. These findings provide greater understanding of the ecoevolutionary factors that underlie the diversification of M. oryzae and highlight the practicality of genomic data for epidemiological surveillance in this important multihost pathogen. IMPORTANCE Infection of novel hosts is a major route for disease emergence by pathogenic microorganisms. Understanding the evolutionary history of multihost pathogens is therefore important to better predict the likely spread and emergence of new diseases. Magnaporthe oryzae is a multihost fungus that causes serious cereal diseases, including the devastating rice blast disease and wheat blast, a cause of growing concern due to its recent spread from South America to Asia. Using whole-genome analysis of 76 fungal strains from different hosts, we have documented the divergence of M. oryzae into numerous lineages, each infecting a limited number of host species. Our analyses provide evidence that interlineage gene flow has contributed to the genetic makeup of multiple M. oryzae lineages within the same species. Plant health surveillance is therefore warranted to safeguard against disease emergence in regions where multiple lineages of the fungus are in contact with one another.Pierre GladieuxBradford CondonSebastien RavelDarren SoanesJoao Leodato Nunes MacielAntonio NhaniLi ChenRyohei TerauchiMarc-Henri LebrunDidier TharreauThomas MitchellKerry F. PedleyBarbara ValentNicholas J. TalbotMark FarmanElisabeth FournierAmerican Society for Microbiologyarticlecryptic speciesdisease emergencediversificationfungal pathogengene flowpopulation structureMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	cryptic species disease emergence diversification fungal pathogen gene flow population structure Microbiology QR1-502
spellingShingle	cryptic species disease emergence diversification fungal pathogen gene flow population structure Microbiology QR1-502 Pierre Gladieux Bradford Condon Sebastien Ravel Darren Soanes Joao Leodato Nunes Maciel Antonio Nhani Li Chen Ryohei Terauchi Marc-Henri Lebrun Didier Tharreau Thomas Mitchell Kerry F. Pedley Barbara Valent Nicholas J. Talbot Mark Farman Elisabeth Fournier Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
description	ABSTRACT Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal biodiversity and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multihost pathogen that infects multiple grasses and cereals, is responsible for the most damaging rice disease (rice blast), and is of growing concern due to the recent introduction of wheat blast to Bangladesh from South America. However, the genetic structure and evolutionary history of M. oryzae, including the possible existence of cryptic phylogenetic species, remain poorly defined. Here, we use whole-genome sequence information for 76 M. oryzae isolates sampled from 12 grass and cereal genera to infer the population structure of M. oryzae and to reassess the species status of wheat-infecting populations of the fungus. Species recognition based on genealogical concordance, using published data or extracting previously used loci from genome assemblies, failed to confirm a prior assignment of wheat blast isolates to a new species (Pyricularia graminis-tritici). Inference of population subdivisions revealed multiple divergent lineages within M. oryzae, each preferentially associated with one host genus, suggesting incipient speciation following host shift or host range expansion. Analyses of gene flow, taking into account the possibility of incomplete lineage sorting, revealed that genetic exchanges have contributed to the makeup of multiple lineages within M. oryzae. These findings provide greater understanding of the ecoevolutionary factors that underlie the diversification of M. oryzae and highlight the practicality of genomic data for epidemiological surveillance in this important multihost pathogen. IMPORTANCE Infection of novel hosts is a major route for disease emergence by pathogenic microorganisms. Understanding the evolutionary history of multihost pathogens is therefore important to better predict the likely spread and emergence of new diseases. Magnaporthe oryzae is a multihost fungus that causes serious cereal diseases, including the devastating rice blast disease and wheat blast, a cause of growing concern due to its recent spread from South America to Asia. Using whole-genome analysis of 76 fungal strains from different hosts, we have documented the divergence of M. oryzae into numerous lineages, each infecting a limited number of host species. Our analyses provide evidence that interlineage gene flow has contributed to the genetic makeup of multiple M. oryzae lineages within the same species. Plant health surveillance is therefore warranted to safeguard against disease emergence in regions where multiple lineages of the fungus are in contact with one another.
format	article
author	Pierre Gladieux Bradford Condon Sebastien Ravel Darren Soanes Joao Leodato Nunes Maciel Antonio Nhani Li Chen Ryohei Terauchi Marc-Henri Lebrun Didier Tharreau Thomas Mitchell Kerry F. Pedley Barbara Valent Nicholas J. Talbot Mark Farman Elisabeth Fournier
author_facet	Pierre Gladieux Bradford Condon Sebastien Ravel Darren Soanes Joao Leodato Nunes Maciel Antonio Nhani Li Chen Ryohei Terauchi Marc-Henri Lebrun Didier Tharreau Thomas Mitchell Kerry F. Pedley Barbara Valent Nicholas J. Talbot Mark Farman Elisabeth Fournier
author_sort	Pierre Gladieux
title	Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
title_short	Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
title_full	Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
title_fullStr	Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
title_full_unstemmed	Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>
title_sort	gene flow between divergent cereal- and grass-specific lineages of the rice blast fungus <italic toggle="yes">magnaporthe oryzae</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/015378b8448940198a809435624b1dde
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Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus <italic toggle="yes">Magnaporthe oryzae</italic>

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