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

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

Research output: Contribution to journalArticlepeer-review

89 Scopus citations

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 contrib- uted 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.

Original languageEnglish
Article numbere01219-17
JournalmBio
Volume9
Issue number1
DOIs
StatePublished - Jan 1 2018

Bibliographical note

Funding Information:
We thank Sophien Kamoun for inspiration and for providing critical input on a previous version of the manuscript, Alfredo Urshimura for collecting and supplying us with the DNA of Brazilian isolates, and the Southgreen and Migale computing facilities. We also thank A. Akhunova at the Kansas State University Integrated Genomics Facility and J. Webb, M. Heist, and R. Ellsworth at the University of Kentucky for their technical assistance. Support by the Agriculture and Food Research Initiative Competitive grant no. 2013-68004-20378 from the USDA National Institute of Food and Agriculture is acknowledged.

Funding Information:
Support by the Agriculture and Food Research Initiative Competitive grant no. 2013-68004-20378 from the USDA National Institute of Food and Agriculture is acknowledged.

Publisher Copyright:
© 2018, American Society for Microbiology. All rights reserved.

Keywords

  • Cryptic species
  • Disease emergence
  • Diversification
  • Fungal pathogen
  • Gene flow
  • Population structure
  • Rice
  • Speciation
  • Species recognition

ASJC Scopus subject areas

  • Microbiology
  • Virology

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