Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen

ABSTRACT The rice blast fungus Magnaporthe oryzae (syn., Pyricularia oryzae) is both a threat to global food security and a model for plant pathology. Molecular pathologists need an accurate understanding of the origins and line of descent of M. oryzae populations in order to identify the genetic an...

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Autores principales:	Pierre Gladieux, Sébastien Ravel, Adrien Rieux, Sandrine Cros-Arteil, Henri Adreit, Joëlle Milazzo, Maud Thierry, Elisabeth Fournier, Ryohei Terauchi, Didier Tharreau
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	clonality deleterious mutations indica rice introgression japonica rice population genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9fdfe61cbc39451ea2fe0d2741c6ef33
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spelling	oai:doaj.org-article:9fdfe61cbc39451ea2fe0d2741c6ef332021-11-15T15:53:27ZCoexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen10.1128/mBio.01806-172150-7511https://doaj.org/article/9fdfe61cbc39451ea2fe0d2741c6ef332018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01806-17https://doaj.org/toc/2150-7511ABSTRACT The rice blast fungus Magnaporthe oryzae (syn., Pyricularia oryzae) is both a threat to global food security and a model for plant pathology. Molecular pathologists need an accurate understanding of the origins and line of descent of M. oryzae populations in order to identify the genetic and functional bases of pathogen adaptation and to guide the development of more effective control strategies. We used a whole-genome sequence analysis of samples from different times and places to infer details about the genetic makeup of M. oryzae from a global collection of isolates. Analyses of population structure identified six lineages within M. oryzae, including two pandemic on japonica and indica rice, respectively, and four lineages with more restricted distributions. Tip-dating calibration indicated that M. oryzae lineages separated about a millennium ago, long after the initial domestication of rice. The major lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and evidence of DNA acquisition from multiple lineages. Tests for weak natural selection revealed that the pandemic spread of clonal lineages entailed an evolutionary “cost,” in terms of the accumulation of deleterious mutations. Our findings reveal the coexistence of multiple endemic and pandemic lineages with contrasting population and genetic characteristics within a widely distributed pathogen. IMPORTANCE The rice blast fungus Magnaporthe oryzae (syn., Pyricularia oryzae) is a textbook example of a rapidly adapting pathogen, and it is responsible for one of the most damaging diseases of rice. Improvements in our understanding of Magnaporthe oryzae’s diversity and evolution are required to guide the development of more effective control strategies. We used genome sequencing data for samples from around the world to infer the evolutionary history of M. oryzae. We found that M. oryzae diversified about 1,000 years ago, separating into six main lineages: two pandemic on japonica and indica rice, respectively, and four with more restricted distributions. We also found that a lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and the acquisition of genetic material from multiple lineages. This work provides a population-level genomic framework for defining molecular markers for the control of rice blast and investigations of the molecular basis of differences in pathogenicity between M. oryzae lineages.Pierre GladieuxSébastien RavelAdrien RieuxSandrine Cros-ArteilHenri AdreitJoëlle MilazzoMaud ThierryElisabeth FournierRyohei TerauchiDidier TharreauAmerican Society for Microbiologyarticleclonalitydeleterious mutationsindica riceintrogressionjaponica ricepopulation genomicsMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	clonality deleterious mutations indica rice introgression japonica rice population genomics Microbiology QR1-502
spellingShingle	clonality deleterious mutations indica rice introgression japonica rice population genomics Microbiology QR1-502 Pierre Gladieux Sébastien Ravel Adrien Rieux Sandrine Cros-Arteil Henri Adreit Joëlle Milazzo Maud Thierry Elisabeth Fournier Ryohei Terauchi Didier Tharreau Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
description	ABSTRACT The rice blast fungus Magnaporthe oryzae (syn., Pyricularia oryzae) is both a threat to global food security and a model for plant pathology. Molecular pathologists need an accurate understanding of the origins and line of descent of M. oryzae populations in order to identify the genetic and functional bases of pathogen adaptation and to guide the development of more effective control strategies. We used a whole-genome sequence analysis of samples from different times and places to infer details about the genetic makeup of M. oryzae from a global collection of isolates. Analyses of population structure identified six lineages within M. oryzae, including two pandemic on japonica and indica rice, respectively, and four lineages with more restricted distributions. Tip-dating calibration indicated that M. oryzae lineages separated about a millennium ago, long after the initial domestication of rice. The major lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and evidence of DNA acquisition from multiple lineages. Tests for weak natural selection revealed that the pandemic spread of clonal lineages entailed an evolutionary “cost,” in terms of the accumulation of deleterious mutations. Our findings reveal the coexistence of multiple endemic and pandemic lineages with contrasting population and genetic characteristics within a widely distributed pathogen. IMPORTANCE The rice blast fungus Magnaporthe oryzae (syn., Pyricularia oryzae) is a textbook example of a rapidly adapting pathogen, and it is responsible for one of the most damaging diseases of rice. Improvements in our understanding of Magnaporthe oryzae’s diversity and evolution are required to guide the development of more effective control strategies. We used genome sequencing data for samples from around the world to infer the evolutionary history of M. oryzae. We found that M. oryzae diversified about 1,000 years ago, separating into six main lineages: two pandemic on japonica and indica rice, respectively, and four with more restricted distributions. We also found that a lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and the acquisition of genetic material from multiple lineages. This work provides a population-level genomic framework for defining molecular markers for the control of rice blast and investigations of the molecular basis of differences in pathogenicity between M. oryzae lineages.
format	article
author	Pierre Gladieux Sébastien Ravel Adrien Rieux Sandrine Cros-Arteil Henri Adreit Joëlle Milazzo Maud Thierry Elisabeth Fournier Ryohei Terauchi Didier Tharreau
author_facet	Pierre Gladieux Sébastien Ravel Adrien Rieux Sandrine Cros-Arteil Henri Adreit Joëlle Milazzo Maud Thierry Elisabeth Fournier Ryohei Terauchi Didier Tharreau
author_sort	Pierre Gladieux
title	Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
title_short	Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
title_full	Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
title_fullStr	Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
title_full_unstemmed	Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen
title_sort	coexistence of multiple endemic and pandemic lineages of the rice blast pathogen
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/9fdfe61cbc39451ea2fe0d2741c6ef33
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Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast Pathogen

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