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Magnaporthe Oryzae Pierre Gladieux University of Montpellier, France University of Kentucky UKnowledge Plant Pathology Faculty Publications Plant Pathology 2-27-2018 Gene Flow Between Divergent Cereal- and Grass- Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae Pierre Gladieux University of Montpellier, France Bradford Condon University of Kentucky Sebastien Ravel University of Montpellier, France Darren Soanes University of Exeter, UK Joao Leodato Nunes Maciel Embrapa Wheat, Brazil See next page for additional authors CFolicllokw h ethire st oa ndlet ausdd knitionow alho wwork accse asts: thott thips://uknos documewnlet bedgnee.ukfitsy. eoydu/pu. lantpath_facpub Part of the Genetics and Genomics Commons, Microbiology Commons, and the Plant Pathology Commons Repository Citation Gladieux, Pierre; Condon, Bradford; Ravel, Sebastien; Soanes, Darren; Maciel, Joao Leodato Nunes; Nhani, Antonio; Chen, Li; Terauchi, Ryohei; Lebrun, Marc-Henri; Tharreau, Didier; Mitchell, Thomas; Pedley, Kerry F; Valent, Barbara; Talbot, Nicholas J.; Farman, Mark L.; and Fournier, Elisabeth, "Gene Flow Between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae" (2018). Plant Pathology Faculty Publications. 79. https://uknowledge.uky.edu/plantpath_facpub/79 This Article is brought to you for free and open access by the Plant Pathology at UKnowledge. It has been accepted for inclusion in Plant Pathology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Authors 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 L. Farman, and Elisabeth Fournier Gene Flow Between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae Notes/Citation Information Published in mBio, v. 9, issue 1, e01219-17, p. 1-19. This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply. Digital Object Identifier (DOI) https://doi.org/10.1128/mBio.01219-17 This article is available at UKnowledge: https://uknowledge.uky.edu/plantpath_facpub/79 RESEARCH ARTICLE crossm Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae Pierre Gladieux,a Bradford Condon,b Sebastien Ravel,a Darren Soanes,c Joao Leodato Nunes Maciel,d Antonio Nhani, Jr,e Li Chen,b Ryohei Terauchi,f Marc-Henri Lebrun,g Didier Tharreau,a Thomas Mitchell,h Downloaded from Kerry F. Pedley,i Barbara Valent,j Nicholas J. Talbot,c Mark Farman,b Elisabeth Fourniera aUMR BGPI, Univ Montpellier, INRA, CIRAD, Montpellier SupAgro, Montpellier, France bDepartment of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA cCollege of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom dEmbrapa Wheat, Passo Fundo, Brazil eEmbrapa Agricultural Informatics, Campinas, Brazil fIwate Biotechnology Research Center, Kitakami, Iwate, Japan http://mbio.asm.org/ gINRA, AgroParisTech UMR BIOGER, Thiverval-Grignon, France hDepartment of Plant Pathology, Ohio State University, Columbus, Ohio, USA iUSDA, Agricultural Research Service, FDWSRU, Ft. Detrick, Maryland, USA jDepartment of Plant Pathology, Kansas State University, Manhattan, Kansas, USA ABSTRACT Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal bio- diversity and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multihost pathogen that infects multiple grasses and cere- als, is responsible for the most damaging rice disease (rice blast), and is of growing on January 28, 2019 by guest concern due to the recent introduction of wheat blast to Bangladesh from South America. However, the genetic structure and evolutionary history of M. oryzae, in- cluding the possible existence of cryptic phylogenetic species, remain poorly de- fined. 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). Received 18 July 2017 Accepted 20 Inference of population subdivisions revealed multiple divergent lineages within November 2017 Published 27 February 2018 Citation Gladieux P, Condon B, Ravel S, Soanes M. oryzae, each preferentially associated with one host genus, suggesting incipient D, Maciel JLN, Nhani A, Jr, Chen L, Terauchi R, speciation following host shift or host range expansion. Analyses of gene flow, tak- Lebrun M-H, Tharreau D, Mitchell T, Pedley KF, ing into account the possibility of incomplete lineage sorting, revealed that genetic Valent B, Talbot NJ, Farman M, Fournier E. 2018. Gene flow between divergent cereal- and exchanges have contributed to the makeup of multiple lineages within M. oryzae. grass-specific lineages of the rice blast fungus These findings provide greater understanding of the ecoevolutionary factors that un- Magnaporthe oryzae. mBio 9:e01219-17. derlie the diversification of M. oryzae and highlight the practicality of genomic data https://doi.org/10.1128/mBio.01219-17. for epidemiological surveillance in this important multihost pathogen. Editor John W. Taylor, University of California, Berkeley IMPORTANCE Infection of novel hosts is a major route for disease emergence by This is a work of the U.S. Government and is pathogenic microorganisms. Understanding the evolutionary history of multihost not subject to copyright protection in the United States. Foreign copyrights may apply. pathogens is therefore important to better predict the likely spread and emergence Address correspondence to Elisabeth Fournier, of new diseases. Magnaporthe oryzae is a multihost fungus that causes serious cereal [email protected]. diseases, including the devastating rice blast disease and wheat blast, a cause of P.G. and B.C. contributed equally to the work. growing concern due to its recent spread from South America to Asia. Using whole- This is contribution no. 18-005-J from the genome analysis of 76 fungal strains from different hosts, we have documented the Kansas Agricultural Experiment Station and contribution number 17-12-107 from the divergence of M. oryzae into numerous lineages, each infecting a limited number of Kentucky Agricultural Experiment Station. host species. Our analyses provide evidence that interlineage gene flow has contrib- ® January/February 2018 Volume 9 Issue 1 e01219-17 mbio.asm.org 1 ® Gladieux et al. uted to the genetic makeup of multiple M. oryzae lineages within the same species. Plant health surveillance is therefore warranted to safeguard against disease emer- gence in regions where multiple lineages of the fungus are in contact with one an- other. KEYWORDS cryptic species, disease emergence, diversification, fungal pathogen, gene flow, population structure, rice, speciation, species recognition nvestigating population genetic structure in relation to life history traits such as Ireproductive mode, host range, or drug resistance is particularly relevant in patho- gens (1, 2). Knowledge of species, lineages, populations, levels of genetic variability, and reproductive mode is essential to answer questions common to all infectious Downloaded from diseases, such as the tempo, origin, and proximate (i.e., molecular) and ultimate (i.e., ecoevolutionary) causes of disease emergence and spread (3). Multilocus molecular typing schemes have shown that cryptic species and lineages within species are often more numerous than estimated from phenotypic data alone. Genomic approaches are emerging as a new gold standard for detecting cryptic structure or speciation with increased resolution, allowing fine-grained epidemiological surveillance and science- based regulatory decisions. The added benefits of whole-genome approaches include identifying the genetic basis of life history traits and better understanding of both the http://mbio.asm.org/ genomic properties that influence the process of speciation and the signatures of (potentially incomplete) speciation that are observable in patterns of genomic variabil- ity (4, 5). Many plant-pathogenic ascomycete fungi are host specific, and some of their life history traits have been shown to be conducive to the emergence of novel pathogen species adapted to new hosts (6, 7). Investigating population structure within multihost ascomycetes thus offers a unique opportunity to identify the genomic features asso- ciated with recent host range expansions or host shifts. In this study, our model is Magnaporthe oryzae (synonym of Pyricularia oryzae)(8), a fungal ascomycete causing on January 28, 2019 by guest blast disease on a variety of grass hosts. Magnaporthe oryzae is well studied as the causal agent of the most important disease of rice (Oryza sativa), but it also causes blast disease on more than 50 cultivated and wild monocot plant species (9). This includes other cereal crops such as wheat (Triticum aestivum), barley (Hordeum vulgare), finger millet (Eleusine coracana), and foxtail millet (Setaria italica and Setaria viridis),
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