Population genomic analysis of the rice blast fungus reveals specific events associated with expansion of three main clades

Abstract

We examined the genomes of 100 isolates of Magnaporthe oryzae (Pyricularia oryzae), the causal agent of rice blast disease. We grouped current field populations of M. oryzae into three major globally distributed groups. A genetically diverse group, clade 1, which may represent a group of closely related lineages, contains isolates of both mating types. Two well-separated clades, clades 2 and 3, appear to have arisen as clonal lineages distinct from the genetically diverse clade. Examination of genes involved in mating pathways identified clade-specific diversification of several genes with orthologs involved in mating behavior in other fungi. All isolates within each clonal lineage are of the same mating type. Clade 2 is distinguished by a unique deletion allele of a gene encoding a small cysteine-rich protein that we determined to be a virulence factor. Clade 3 isolates have a small deletion within the MFA2 pheromone precursor gene, and this allele is shared with an unusual group of isolates we placed within clade 1 that contain AVR1-CO39 alleles. These markers could be used for rapid screening of isolates and suggest specific events in evolution that shaped these populations. Our findings are consistent with the view that M. oryzae populations in Asia generate diversity through recombination and may have served as the source of the clades 2 and 3 isolates that comprise a large fraction of the global population.

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

“…(N=43) [30] and Zhong et al . (N=88) [31] . The combined use of samples from these two studies increases not only the number of M. oryzae samples but also their geographical spread (Supp.…”

“…Zhong et al . [31] divided their dataset in three groups (I-III) but did not identify group IV, since their dataset only include one individual from this group. In addition to groups I-IV, Gladieux et al .…”

“…Until recently, understanding of the population genomics structure of the rice blast fungus has remained limited. In 2018, two studies reported whole genome sequences from non-overlapping sets of globally distributed rice-infecting M. oryzae isolates [30,31] . Both studies suggested the presence of a diverse Southeast Asian population and two major clonal groups.…”

“…[30] and Zhong et al . [31] to reconcile the two datasets and increase the number of examined M. oryzae individuals to 131 isolates from 21 countries. This has enabled us to assess the global genetic structure of rice-infecting M. oryzae more comprehensively than the prior separate analyses of the two datasets.…”

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

“…Records of rice blast disease in China date back to the early 17 th century and until today it is recognized as one of the most threatening and widely distributed rice diseases [39]. Recent population genetics studies revealed that the rice-infecting lineage of M. oryzae consists of both a recombining population and multiple, clonally expanded lineages [42][43][44]. In Europe, the rice blast fungus population consists of only one of three major clonal lineages and it is possible that mating type isolation led to local asexual expansions.…”