Pan-genome analyses of 226 finger millet-infecting Magnaporthe oryzae strains from eastern Africa reveal two lineages that differ in their genetic make-up, virulence and effector gene content with gene loss driven by homologous recombination between Pot2 elements

Blast disease, caused by the filamentous ascomycete Magnaporthe oryzae, is the main biotic constraint to finger millet production in eastern Africa. M. oryzae is a pathogen on many grass species, but the high host-specificity of blast isolates underscores the need to study pathogen diversity and virulence at the host level. Here, we fill a void on knowledge on finger millet-infecting strains of M. oryzae by sequencing 226 isolates pure-cultured from infected tissues, mainly peduncles and panicles, sampled from field-grown finger millet accessions across Ethiopia, Kenya, Tanzania and Uganda. Phylogenetic analysis showed that eastern African isolates are genetically distinct from Asian isolates, and differentiated into two groups potentially driven by climate variables. One group was dominated by isolates from Kenya and Uganda (KU group), and the other by isolates from Ethiopia and Tanzania (ET group). Analysis of the portfolio of 887 predicted effector genes showed that the KU group had significantly fewer effectors, concomitant with higher virulence levels on the two finger millet accessions tested. We demonstrate that homologous recombination between transposable elements, leading to genomic deletions, plays a key role in gene removal. Transcript profiling of fungal genes in compatible and incompatible interactions revealed upregulation in the incompatible interaction as a characteristic of an estimated 30% of effector genes, including seven of the eight homologs of known avirulence genes from rice-infecting M. oryzae identified in our study. Prioritization of these effectors for functional validation will pave the way for identifying cognate resistance genes and improving finger millet for resistance to blast disease.