Natural selection drives population divergence for local adaptation in a wheat pathogen.

Evolution favors the emergence of locally-adapted optimum phenotypes that are likely to differ across a wide array of environmental conditions. The emergence of favorable adaptive characteristics is accelerated in agricultural pathogens due to the unique properties of agro-ecosystems. We performed a QST - FST comparison using 164 strains of Parastagonospora nodorum sampled from eight global field populations to disentangle the predominant evolutionary forces driving population divergence in a wheat pathogen. We used digital image analysis to obtain quantitative measurements of growth rate and melanization at different temperatures and under different fungicide concentrations in a common garden experiment. FST measures were based on complete genome sequences obtained for all 164 isolates. Our analyses indicated that all measured traits were under selection. Growth rates at 18 °C and 24 °C were under stabilizing selection (QST < FST), while diversifying selection (QST > FST) was the predominant evolutionary force affecting growth under fungicide and high temperature stress. Stabilizing selection (QST < FST) was the predominant force affecting melanization across the different environments. Melanin production increased at 30 °C but was negatively correlated with higher growth rates, consistent with a trade-off under heat stress. Our results demonstrate that global populations of P. nodorum possess significant evolutionary potential to adapt to changing local conditions, including warmer temperatures and applications of fungicides.

Pereira D ，Croll D ，Brunner PC ，McDonald BA ... -  《-》

The influence of genetic drift and selection on quantitative traits in a plant pathogenic fungus.

Stefansson TS ，McDonald BA ，Willi Y 《PLoS One》

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

Richards JK ，Stukenbrock EH ，Carpenter J ，Liu Z ，Cowger C ，Faris JD ，Friesen TL ... -  《PLoS Genetics》

The Genetic Architecture of Emerging Fungicide Resistance in Populations of a Global Wheat Pathogen.

Containing fungal diseases often depends on the application of fungicidal compounds. Fungicides can rapidly lose effectiveness due to the rise of resistant individuals in populations. However, the lack of knowledge about resistance mutations beyond known target genes challenges investigations into pathways to resistance. We used whole-genome sequencing data and association mapping to reveal the multilocus genetic architecture of fungicide resistance in a global panel of 159 isolates of Parastagonospora nodorum, an important fungal pathogen of wheat. We found significant differences in azole resistance among global field populations. The populations evolved distinctive combinations of resistance alleles which can interact when co-occurring in the same genetic background. We identified 34 significantly associated single nucleotide polymorphisms located in close proximity to genes associated with fungicide resistance in other fungi, including a major facilitator superfamily transporter. Using fungal colony growth rates and melanin production at different temperatures as fitness proxies, we found no evidence that resistance was constrained by genetic trade-offs. Our study demonstrates how genome-wide association studies of a global collection of pathogen strains can recapitulate the emergence of fungicide resistance. The distinct complement of resistance mutations found among populations illustrates how the evolutionary trajectory of fungicide adaptation can be complex and challenging to predict.

Pereira D ，McDonald BA ，Croll D 《Genome Biology and Evolution》

Evidence for local adaptation and pleiotropic effects associated with melanization in a plant pathogenic fungus.

We combined a common garden experimental design with digital image analysis to determine how melanization responds to temperature and fungicide stress in 126 strains of Rhynchosporium commune sampled from nine global field populations. We found that different temperatures and fungicide stress significantly affected the degree of melanization. The nine field populations showed similar patterns in response to the different temperatures. Significant correlations were found between the degree of melanization and the local environment, including mean annual temperature, latitude, and relative humidity, suggesting that melanization is a locally adaptive trait. We also found that melanization is positively correlated with both virulence and fungicide resistance. These findings suggest that melanization has pleiotropic effects in Rhynchosporium commune.

Zhu W ，Zhan J ，McDonald BA 《-》