Genome-wide detection of genes under positive selection in worldwide populations of the barley scald pathogen

Abstract

The coevolution between hosts and pathogens generates strong selection pressures to maintain resistance and infectivity, respectively. Genomes of plant pathogens often encode major effect loci for the ability to successfully infect a specific host. Hence, heterogeneity in the host genotypes and abiotic factors leads to locally adapted pathogen populations. However, the genetic basis of local adaptation is poorly understood. We analyzed global field populations of Rhynchosporium commune, the pathogen causing barley scald disease, to identify candidate genes for local adaptation. Whole genome sequencing data generated for 125 isolates showed that the pathogen is subdivided into three genetic clusters associated with distinct geographic and climatic regions. Using haplotype-based selection scans applied independently to each genetic cluster, we found strong evidence for selective sweeps throughout the genome. Comparisons of loci under selection among clusters revealed little overlap, suggesting that ecological differences associated with each cluster led to variable selection regimes. The strongest signals of selection were found predominantly in the two clusters composed of isolates from Central Europe and Ethiopia. The strongest selective sweep regions encoded proteins with functions related to both biotic and abiotic stresses. We found that selective sweep regions were enriched in genes encoding functions in cellular localization, protein transport activity, and DNA damage responses. In contrast to the prevailing view that a small number of gene-for-gene interactions govern plant pathogen evolution, our analyses suggest that the evolutionary trajectory is largely determined by spatially heterogeneous biotic and abiotic selection pressures.