Complex Adaptive Architecture Underlies Adaptation to Quantitative Host Resistance in a Fungal Plant Pathogen

Plant pathogens often adapt to plant genetic resistance so characterization of the architecture under-lying such an adaptation is required to understand the adaptive potential of pathogen populations. Erosion of banana quantitative resistance to a major leaf disease caused by polygenic adaptation of the causal agent, the fungus Pseudocercospora fijiensis, was recently identified in the northern Caribbean region. Genome scan and quantitative genetics approaches were combined to investigate the adaptive architecture underlying this adaptation. Thirty-two genomic regions showing host se-lection footprints were identified by pool sequencing of isolates collected from seven plantation pairs of two cultivars with different levels of quantitative resistance. Individual sequencing and phenotyping of isolates from one pair revealed significant and variable levels of correlation be-tween haplotypes in 17 of these regions with a quantitative trait of pathogenicity (the diseased leaf area). The multilocus pattern of haplotypes detected in the 17 regions was found to be highly varia-ble across all the population pairs studied. These results suggest complex adaptive architecture un-derlying plant pathogen adaptation to quantitative resistance with a polygenic basis, redundancy, and a low level of parallel evolution between pathogen populations. Candidate genes involved in quantitative pathogenicity and host adaptation of P. fijiensis were highlighted in genomic regions combining annotation analysis with available biological data.