Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae

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 wholegenome 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-

Gene exchange between two divergent species of the fungal human pathogen,Coccidioides

“…Studies focused on recently divergent species have identified large introgressed tracts (>1 Mb), consistent with recent admixture (Gladieux et al. ; Maxwell et al. ).…”

“…; Gladieux et al. ). Therefore, to some extent, these results are expected as recently diverged species are not likely to have accumulated many hybrid incompatibilities (Matute et al.…”

“…) and Magnaporthe (Gladieux et al. ), admixture seems to be recent as the size of the inferred introgressions (>1 Mb) is large enough to cover several centimorgans. Furthermore, each of these studies examined gene flow between relatively recently (∼2 million years ago) diverged lineages or species (Desjardins et al.…”

The polyphagous plant pathogenic fungusBotrytis cinereaencompasses host‐specialized and generalist populations

“…e . poly‐specialists, such as the rice blast fungus Pyricularia oryzae ; Gladieux et al ., ; Valent et al ., ). Depending on time‐based, geographic and genetic factors (Nosil et al ., ), speciation can then unfold relatively rapidly between pathogen populations (Giraud et al ., ).…”

A nuclear contortionist: the mitotic migration ofMagnaporthe oryzaenuclei during plant infection

“…It is capable of mass destruction to valuable plant crops such as rice and wheat, as well as barley, finger millet, and foxtail millet (Gladieux et al 2018). In fact, each year M. oryzae causes an estimated $66 billion in economic damage to rice crops, destroying enough food to have fed 60 million people (Pennisi 2010).…”