Ecological Differentiation and Incipient Speciation in the Fungal Pathogen Causing Rice Blast

Natural variation in plant pathogens has an impact on food security and ecosystem health. The rice blast fungus Pyricularia oryzae, which limits rice production in all rice-growing areas, is structured into multiple lineages. Diversification and the maintenance of multiple rice blast lineages have been proposed to be due to separation in different areas and differential adaptation to rice subspecies. However, the precise world distribution of rice blast populations, and the factors controlling their presence and maintenance in the same geographic areas, remain largely unknown. We used genotyping data for 886 isolates from more than 185 locations in 51 countries to show that P. oryzae is structured into one recombining and three clonal lineages, each with broad geographic distributions. No evidence was found for admixture in clonal lineages, and crossing experiments revealed that female sterility and early postmating genetic incompatibilities acted as strong barriers to gene flow between these lineages. An analysis of climatic and geographic data indicated that the four lineages of P. oryzae were found in areas differing in terms of the prevailing environmental conditions and types of rice grown. Pathogenicity tests with representatives of the five main rice subspecies revealed differences in host range between pathogenic lineages, highlighting a contribution of specialization to niche separation between lineages, despite co-existence on the same host species. Our results demonstrate that the spread of a pathogen across heterogeneous habitats and divergent populations of a crop species can lead to niche separation and incipient speciation in the pathogen

Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities

International audienceMany species of fungal plant pathogens coexist as multiple lineages on the same host, but the factors underlying the origin and maintenance of population structure remain largely unknown. The rice blast fungus Pyricularia oryzae is a widespread model plant pathogen displaying population subdivision. However, most studies of natural variation in P. oryzae have been limited in genomic or geographic resolution, and host adaptation is the only factor that has been investigated extensively as a contributor to population subdivision. In an effort to complement previous studies, we analyzed genetic and phenotypic diversity in isolates of the rice blast fungus covering a broad geographical range. Using single-nucleotide polymorphism genotyping data for 886 isolates sampled from 152 sites in 51 countries, we showed that population subdivision of P. oryzae in one recombining and three clonal lineages with broad distributions persisted with deeper sampling. We also extended previous findings by showing further population subdivision of the recombining lineage into one international and three Asian clusters, and by providing evidence that the three clonal lineages of P. oryzae were found in areas with different prevailing environmental conditions, indicating niche separation. Pathogenicity tests and bioinformatic analyses using an extended set of isolates and rice varieties indicated that partial specialization to rice subgroups contributed to niche separation between lineages, and differences in repertoires of putative virulence effectors were consistent with differences in host range. Experimental crosses revealed that female sterility and early post-mating genetic incompatibilities acted as strong additional barriers to gene flow between clonal lineages. Our results demonstrate that the spread of a fungal pathogen across heterogeneous habitats and divergent populations of a crop species can lead to niche separation and reproductive isolation between distinct, widely distributed, lineages

Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities

International audienceMany species of fungal plant pathogens coexist as multiple lineages on the same host, but the factors underlying the origin and maintenance of population structure remain largely unknown. The rice blast fungus Pyricularia oryzae is a widespread model plant pathogen displaying population subdivision. However, most studies of natural variation in P. oryzae have been limited in genomic or geographic resolution, and host adaptation is the only factor that has been investigated extensively as a contributor to population subdivision. In an effort to complement previous studies, we analyzed genetic and phenotypic diversity in isolates of the rice blast fungus covering a broad geographical range. Using single-nucleotide polymorphism genotyping data for 886 isolates sampled from 152 sites in 51 countries, we showed that population subdivision of P. oryzae in one recombining and three clonal lineages with broad distributions persisted with deeper sampling. We also extended previous findings by showing further population subdivision of the recombining lineage into one international and three Asian clusters, and by providing evidence that the three clonal lineages of P. oryzae were found in areas with different prevailing environmental conditions, indicating niche separation. Pathogenicity tests and bioinformatic analyses using an extended set of isolates and rice varieties indicated that partial specialization to rice subgroups contributed to niche separation between lineages, and differences in repertoires of putative virulence effectors were consistent with differences in host range. Experimental crosses revealed that female sterility and early post-mating genetic incompatibilities acted as strong additional barriers to gene flow between clonal lineages. Our results demonstrate that the spread of a fungal pathogen across heterogeneous habitats and divergent populations of a crop species can lead to niche separation and reproductive isolation between distinct, widely distributed, lineages

Sequenced isolates.

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