A thousand-genome panel retraces the global spread and climatic adaptation of a major crop pathogen

Abstract

Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen.

A highly multiplexed assay to monitor pathogenicity, fungicide resistance and gene flow in the fungal wheat pathogen Zymoseptoria tritici

“…The integration of genome-wide markers greatly enhances the quality of pathogen monitoring by providing information about patterns of gene flow. Our study revealed only weak differentiation across Western European countries and among French regions consistent with high levels of gene flow and genetic diversity [ 55 ]. Knowledge of genetic structure can help identify recent movements of the pathogen due to natural or human-mediated dispersal.…”

“…G1-G10) constituted from a mix of pure DNA from the same three isolates in different proportions (INRA10-FS1006, INRA10-FS1022, IPO-09455; Fig 4 ; Table A in S1 File ). We used existing whole genome sequencing and SNP calling data for the three isolates to assess polymorphism across the genome [ 55 ]. Using the known dilutions of pure DNA, we established the expected frequencies of reference alleles ( i .…”

A highly multiplexed assay to monitor pathogenicity, fungicide resistance and gene flow in the fungal wheat pathogenZymoseptoria tritici

“…4; Table A in Supplementary File S1). We used existing whole genome sequencing and SNP calling data for the three isolates to assess polymorphism across the genome [55]. Using the known dilutions of pure DNA, we established the expected frequencies of reference alleles (i.e.…”

“…Additional isolates from Oceania included 75 isolates collected in New Zealand in 2013 and 2015 [55]. A total of 154 isolates were collected in Oregon, USA, in 1990 and 2015 [22].…”

Divergent outcomes of direct conspecific pathogen strain interaction and plant co-infection suggest consequences for disease dynamics

“…Under co-infection, Z. tritici strains colonize wheat leaves in a mosaic of genotypes (29). Field populations exhibit high genetic and phenotypic diversity worldwide due to frequent sexual reproduction, large populations, and significant gene flow among populations (30)(31)(32). Co-infection of wheat leaves by multiple strains of Z. tritici are frequent in the field (29).…”