Genome-Wide Detection of Genes Under Positive Selection in Worldwide Populations of the Barley Scald Pathogen

Abstract

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 specific host genotypes. Hence, spatial heterogeneity in host genotypes coupled with abiotic factors could lead to locally adapted pathogen populations. However, the genetic basis of local adaptation is poorly understood. Rhynchosporium commune, the pathogen causing barley scald disease, interacts at least partially in a gene-for-gene manner with its host. We analyzed global field populations of 125 R. commune isolates to identify candidate genes for local adaptation. Whole genome sequencing data 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 protein functions related to biotic and abiotic stress responses. 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.

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses

“…Karyotypic polymorphism within populations may be both a cause and a consequence of reduced sexual reproduction. Interestingly, R. commune shows reduced levels of sexual reproduction in most populations except Ethiopia, which is the most homogenous in genome size estimates (Mohd‐Assaad et al, ).…”

“…For this, NIP1 was used as a fixed effect with eight levels consisting of all identified combinations of NIP1A and NIP1B genotypes. In all analyses, we controlled for population structure by using the genetic cluster assigned by an unsupervised Bayesian clustering analysis (Pritchard et al, 2000) from Mohd-Assaad et al (2018) as a random effect (Supporting Information Table S5). We also excluded haplotypes with pseudogenized NIP1 variants as well as genotypes showing an admixture of more than 10% from all association tests.…”

“…We tested for evidence of selection acting on NIP1A and NIP1B among species, as well as within and among genetic clusters of R. commune. We calculated Tajima's D based on the site frequency spectra (Tajima, 1989) independently within each R. commune cluster (Mohd-Assaad et al, 2018). Admixed genotypes were excluded from the analyses as described above.…”

“…Rrs1 (Rohe et al, 1995;Schürch et al, 2004;van't Slot et al, 2007;Kirsten et al, 2012). Genome-wide scans of R. commune populations identified a series of loci under recent selection, however, none of these loci encoded putative effector genes (Mohd-Assaad et al, 2018).…”

Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States

“…Additionally, candidate genes potentially involved in pathogenicity and host adaptation, as well as genes upregulated in planta were identified within selective sweep regions. Analysis of a global collection of the barley pathogen Rhynchosporium commune identified three major genetic clusters that exhibited unique and generally non-overlapping selective sweep regions hypothesized to stem from ecological variations [23]. Interestingly, genes potentially implicated in response to abiotic stress and not host adaptation were found to be enriched under selective sweep regions.…”