Gene flow between divergent cereal- and grass-specific lineages of the rice blast fungus Magnaporthe oryzae

Authors: GLADIEUX, PIERRE - Institut National De La Recherche Agronomique (INRA); CONDON, BRADFORD - University Of Kentucky; RAVEL, SEBASTIEN - Cirad, France; SOANES, DARREN - University Of Exeter; MACIEL, JOAO LEODATO - Embrapa; NHANI, ANTONIO - Embrapa; CHEN, LI - University Of Kentucky; TERAUCHI, RYOHEI - Iwate Biotechnology Research Center; LEBRUN, MARC-HENRI - Cirad, France; THARREAU, DIDIER - Cirad, France; MITCHELL, THOMAS - The Ohio State University; Pedley, Kerry; VALENT, BARBARA - Kansas State University; TALBOT, NICK - University Of Exeter; FARMAN, MARK - University Of Kentucky; FOURNIER, ELISABETH - Cirad, France

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2017
Publication Date: 2/27/2018
Citation: Gladieux, P., Condon, B., Ravel, S., Soanes, D., Maciel, J.N., Nhani, A., Chen, L., Terauchi, R., Lebrun, M., Tharreau, D., Mitchell, T., Pedley, K.F., Valent, B., Talbot, N., Farman, M., Fournier, E. 2018. Gene flow between divergent cereal- and grass-specific lineages of the rice blast fungus Magnaporthe oryzae. mBio. 9:e01219-17. https://doi.org/10.1128/mBio.01219-17.
DOI: https://doi.org/10.1128/mBio.01219-17

Interpretive Summary: Many plant pathogens are capable of infecting multiple host plants. For example, rice blast and wheat blast are plant diseases caused by the same pathogenic fungus that infects rice, wheat, and several other species of grasses. Individual strains of ‘blast’ are not capable of infecting all hosts, indicating that distinct lineages of the pathogen may have adapted to favor one or more host plant species. However, the exchange of genetic material between individual strains of different lineages may give rise to novel lineages with new host specificity. Studying the evolutionary history of such multi-host pathogens is therefore important to better understand and predict the likely spread and emergence of new diseases. In this study, we analyzed the genomes of 76 blast strains collected from different hosts. Our results document the divergence of this pathogen into numerous lineages and provide evidence that gene flow between different lineages of the pathogen has contributed to its genetic makeup. Based on our results we believe diligent plant health surveillance is warranted to safeguard against the emergence of new diseases in regions where multiple lineages of blast coexist.

Technical 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 multi-host pathogen that infects multiple grasses and cereals, is responsible for the most damaging rice disease (rice blast), and 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 eco-evolutionary factors that underlie the diversification of M. oryzae and highlight the practicality of genomic data for epidemiological surveillance in this important multi-host pathogen.