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

Thierry Maud, Charriat Florian, Milazzo Joëlle, Adreit Henri, Ravel Sébastien, Cros-Arteil Sandrine, Borron Sonia, Sella Violaine, Kroj Thomas, Loos Renaud, Fournier Elisabeth, Tharreau Didier, Gladieux Pierre. 2022. Maintenance of divergent lineages of the Rice Blast Fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities. PLoS Pathogens, 18 (7):e1010687, 33 p.

Résumé : Many 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 polymor- phism 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 sep- aration. 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.

Mots-clés Agrovoc : Pyricularia oryzae

Classification Agris : H20 - Maladies des plantes
F30 - Génétique et amélioration des plantes
H50 - Troubles divers des plantes

Champ stratégique Cirad : CTS 4 (2019-) - Santé des plantes, des animaux et des écosystèmes

Auteurs et affiliations

• Thierry Maud
• Charriat Florian, CIRAD-BIOS-UMR ASTRE (FRA)
• Milazzo Joëlle
• Adreit Henri, CIRAD-BIOS-UMR PHIM (FRA)
• Ravel Sébastien, IRD (FRA) ORCID: 0000-0001-6663-782X
• Cros-Arteil Sandrine, INRAE (FRA)
• Borron Sonia, INRAE (FRA)
• Sella Violaine, ANSES (FRA)
• Kroj Thomas, INRAE (FRA)
• Loos Renaud, ANSES (FRA)
• Fournier Elisabeth, INRAE (FRA)
• Tharreau Didier, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0003-3961-6120 - auteur correspondant
• Gladieux Pierre, INRAE (FRA) - auteur correspondant

Source : Cirad-Agritrop (https://agritrop.cirad.fr/601790/)

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