Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus
Magnaporthe oryzae
Authors: 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 , Fournier Elisabeth 
Published: February 2018

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 contributed 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.