Transposable elements create distinct genomic niches for effector evolution among Magnaporthe oryzae lineages

Draft genome assemblies: De novo draft assemblies were generated using the software SPAdes v3.15.5 (Bankevich et al., 2012) with the “careful” method and automated k-mer selection. Assemblies are identified by their NCBI SRA accession ID. Effectors gain and loss dynamics across Magnaporthe spp. Maximum likelihood phylogenomic tree of 405 Magnaporthe genomes from the most frequently sampled pathotypes based on 300 protein sequence alignments of single-copy genes. Bootstrap confidence values >80% are displayed. AVRs are organized based on hierarchical clustering of presence/absence patterns. AVRs colored in green belong to the MoO AVR pathotype and in blue belong to the MoT AVR pathotype. Abstract: Plant-pathogen interactions are characterized by evolutionary arms races. At the molecular level, fungal effectors can target important plant functions, while plants evolve to improve effector recognition. Rapid evolution in genes encoding effectors can be facilitated by transposable elements (TEs). In Magnaporthe oryzae, the causal agent of blast disease in several cereals and grasses, TEs play important roles in chromosomal evolution as well as the gain or loss of effector genes in host specialized lineages. However, a global understanding of TE dynamics driving effector evolution at population scale and across lineages is lacking. Here, we focus on 16 AVR effector loci assessed across a global sampling of 11 reference genomes and 447 newly generated draft genome assemblies across all major M. oryzae lineages and outgroups. We classified each effector based on evidence for duplication, deletion and translocation processes among M. oryzae lineages. Next, we determined AVR gain and loss dynamics across lineages allowing for a broad categorization of effector dynamics. Each AVR was integrated in a distinct genomic niche determined by the TE activity profile contributing to the diversification at the locus. We quantified TE contributions to effector niches and found that TE identity helped diversify AVR loci. We used the large genomic dataset to recapitulate the evolution of the rice blast AVR1-CO39 locus. Taken together, our work demonstrates how TE dynamics are an integral component of M. oryzae effector evolution, likely facilitating escape from host recognition. In-depth tracking of effector loci is a valuable tool to predict the durability of host resistance.