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Genomic analysis reveals multiple endemic and pandemic lineages of rice blast and gene flow into recombining populations from southeast continental Asia
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BGPI : équipe 5. International audience. Population genomic structure represents a key observable feature of pathogen lineage emergence, divergence and spread, and population genetic models fitted to genome-wide data can be used as a baseline against which to identify the genomic features and molecular mechanisms involved in pathogen adaptation or reproductive isolation. The rice blast fungus Magnaporthe oryzae is the most damaging rice pathogen, and a textbook example of widely distributed, rapidly adapting pathogen, despite limited genetic diversity. The aim of our study was to elucidate the factors and evolutionary changes underlying the emergence, diversification and spread of M. oryzae. Analyses of population structure based on single-read Illumina resequencing of 48 isolates identified four pandemic lineages of which three were highly clonal, and one recombining, as previously reported using microsatellite multilocus typing. We also found two lineages endemic to China, represented by only a few individuals in our dataset. Because recombination is limited in this system, we could use a phylogenetic approach to date the emergence and global dispersal of M. oryzae. The sequenced isolates were collected between 1973 and 2009, which allowed us to calibrate tree nodes using dated tips. Our analysis provided an estimate of ~10.000 years before present for the split between the population infecting rice from those infecting Setaria millet, corresponding to the oldest archaeological evidence for human exploitation of rice. We also found that the six lineages of M. oryzae diverged almost simultaneously ~2.000 years ago, which might correspond to the initial spread of rice cultivation outside Asia. Phylogenomic analyses revealed discordant genealogies among chromosomes, suggesting incomplete lineage sorting associated with rapid diversification. Analyses of the distribution of lineage-specific variants revealed possible exchanges of genomic fragments among clonal lineages, suggesting that hyphal fusion and genetic exchange between mycelia may play a role in increasing the genome diversity of asexual rice blast populations. Our work provides a population-level genomic framework for defining molecular markers to assist in the control of rice blast and for investigating the molecular underpinnings of phenotypic and fitness differences between divergent lineages
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