Incipient speciation in the rice blast fungus

Emerging fungal diseases of plants represent a growing issue accompanying global environmental changes, and there is tremendous interest in identifying the factors controlling their appearance and spread. Our model system is the rice blast fungus Pyricularia oryzae (synonym Magnaporthe oryzae), a textbook example of widely distributed, rapidly adapting pathogen, causing a major rice disease. We previously showed that rice-infecting P. oryzae is subdivided into four main lineages, that diversified about 1,000 years ago, including pandemic clonal lineages and a sexually-recombining Southeast Asian lineage displaying signatures of admixture with multiple sources (10.1128/mBio.01806-17). The aim of our study was to clarify the geographical distribution of rice-infecting lineages and the extent of the co-existence in syntopy, and to identify the factors contributing to reduce or facilitate gene flow between them. Analyses of population structure based on Infinium-genotyping of 5300 SNPs for 970 isolates collected on rice on the five continents confirmed the existence of four major lineages (L1 to L4) within P. oryzae. The lineages displayed contrasted population structures (L1: recombinant; L2-L4: clonal) and varied in geographic range sizes (L1 and L2: global distribution; L3 widespread in the south hemisphere; L4: mostly South Asian). The recombinant lineage (L1) was the most genetically diverse, with most diversity distributed within and between regions in East and Southeast Asia. Genealogies of clonal lineages L2-L4 had roots in Asia, consistent with an Asian origin. In vitro measurements of reproductive compatibility revealed widespread intrinsic prezygotic and early postzygotic isolation between all lineage pairs with compatible mating types, with the lower levels of reproductive isolation were measured in mating experiments with lineage L1. Mycelial growth rate measurements suggested no difference in temperature optima but pathogenicity testings showed that the lineages were differentially adapted to different rice subspecies. Our work shows that the fungus has been very extensively moved, and that the success of its different lineages is linked to their reproductive isolation, which allows their maintenance in syntopy and enhances their ability to adapt to new conditions in the face of gene flow