Genetic variation bias towards noncoding regions and secreted proteins in the rice blast fungus Magnaporthe oryzae

The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the number of studies that have examined the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, we applied experimental evolution and high-throughput pool sequencing on Magnaporthe oryzae, a fungal pathogen that causes massive losses in rice production, to observe the evolution of genome variation. We found that mutations, including single nucleotide polymorphisms (SNPs), insertions and deletions (InDels) and transposable element (TE) insertions, accumulated very rapidly throughout the genome of M. oryzae during sequential plant inoculation and preferentially in noncoding regions, while such mutations were limited in coding regions. However, we also observed that new TE insertions accumulated with time and preferentially accumulated at the proximal region of secreted protein (SP)-coding genes in M. oryzae populations. Taken together, these results revealed a bias in genetic variation towards noncoding regions and SP genes in M. oryzae, which is consistent with the two-speed genome theory and may contribute to the fast adaptative evolution of the blast fungal effectors under host selection.