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

Authors: RICHARDS, JONATHAN - North Dakota State University; STUKENBROCK, EVA - Max Planck Institute For Evolutionary Biology; CARPENTER, JESSICA - North Dakota State University; LIU, ZHAOHUI - North Dakota State University; Cowger, Christina; Faris, Justin; Friesen, Timothy

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/25/2019
Publication Date: 10/18/2019
Citation: Richards, J.K., Stukenbrock, E.H., Carpenter, J., Liu, Z., Cowger, C., Faris, J.D., Friesen, T.L. 2019. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PLoS Genetics. 15(10):e1008223. https://doi.org/10.1371/journal.pgen.1008223.
DOI: https://doi.org/10.1371/journal.pgen.1008223

Interpretive Summary: Plant pathogen populations evolve rapidly to overcome resistance that has been deployed by breeders and planted by growers. Without a clear understanding of pathogen diversity and the ability to change, breeders are unable to select for disease resistance that will be effective long term rather than being quickly overcome by the pathogen population. In the current work, the objective was to obtain genome sequences of 197 isolates of Parastagonospora nodorum, causal agent of septoria nodorum blotch of wheat, collected from the major wheat growing areas of the United States to investigate the gene diversity of the pathogen population. The gene diversity of the pathogen population was shown to be very different in the eastern winter wheat growing regions compared to the Midwest and Northern Great Plains. Different putative virulence genes were under selection in each population showing that the pathogen population can adapt to the local sources of resistance and that the different classes of wheat (winter and spring) harbor different resistances. This information is critical for pathologists and breeders alike to be able to intelligently manage this and other important disease of wheat.

Technical Abstract: Filamentous fungi rapidly evolve in response to environmental selection pressures, exemplified by their genomic plasticity and propensity to diversification. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of putative effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. A total of 1,026,859 quality SNPs/InDels were identified within the entire natural population. Implementation of a GWAS successfully identified novel loci, as well as SnToxA and SnTox3 as major factors in disease. Genes displaying presence/absence variation and predicted effector genes had significantly higher pN/pS ratios, indicating a greater level of diversifying selection. Population structure analyses indicated two major P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1. Additionally, 20 and 27 candidate effector genes were observed to be under diversifying selection among isolates from Population 1 and Population 2, respectively, but under purifying or neutral selection in the opposite population. Selective sweep analysis revealed 42 and 46 regions of positive selection from Population 1 and Population 2, respectively, with 191 genes underlying population specific selective sweeps. Also, genes exhibiting presence/absence variation or those located under selective sweeps were found to be significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection.