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...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-05-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01806-17 |
| _version_ | 1818740184847482880 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T01:36:42Z |
| format | Article |
| id | doaj.art-9fdfe61cbc39451ea2fe0d2741c6ef33 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T01:36:42Z |
| publishDate | 2018-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-9fdfe61cbc39451ea2fe0d2741c6ef332022-12-21T21:25:26ZengAmerican Society for MicrobiologymBio2150-75112018-05-019210.1128/mBio.01806-17Coexistence of Multiple Endemic and Pandemic Lineages of the Rice Blast PathogenPierre Gladieux0Sébastien Ravel1Adrien Rieux2Sandrine Cros-Arteil3Henri Adreit4Joëlle Milazzo5Maud Thierry6Elisabeth Fournier7Ryohei Terauchi8Didier Tharreau9UMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceCIRAD, UMR PVBMT, St. Pierre de la Reunion, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceIwate Biotechnology Research Center, Kitakami, Iwate, JapanUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, FranceABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.01806-17clonalitydeleterious mutationsindica riceintrogressionjaponica ricepopulation genomics |
| spellingShingle | 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 mBio clonality deleterious mutations indica rice introgression japonica rice population genomics |
| title | 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_short | 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 |
| topic | clonality deleterious mutations indica rice introgression japonica rice population genomics |
| url | https://journals.asm.org/doi/10.1128/mBio.01806-17 |
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