A thousand-genome panel retraces the global spread and adaptation of a major fungal 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.

Recent reactivation of a pathogenicity-associated transposable element triggers major chromosomal rearrangements in a fungal wheat pathogen

“…However, bursts in transposon activity and population bottlenecks following founder events are impacting transposon dynamics as well (47). The evolutionary history of Z. tritici is tightly linked to wheat domestication in the Fertile Crescent followed by stepwise introduction events to new continents (28). Populations outside of the Middle East and Europe have both gained in transposon content and overall reduced RIP-like mutations (28).…”

“…The evolutionary history of Z. tritici is tightly linked to wheat domestication in the Fertile Crescent followed by stepwise introduction events to new continents (28). Populations outside of the Middle East and Europe have both gained in transposon content and overall reduced RIP-like mutations (28). Colonization events over the past centuries in Australia induced population bottlenecks leading to reduced genetic diversity and likely less efficient selection.…”

“…To assess the geographic and temporal variation in Styx copy numbers in Z. tritici, we used a 923-genome panel of Illumina sequenced genomes (28) where the pathogen has been recorded. We trimmed raw Illumina reads to remove adapters and retain only high quality bases (LEADING:15 TRAILING:15 SLIDINGWINDOW:5:15 MINLEN:50) with Trimmomatic v.0.39 (62).…”

Population-level transposable element expression dynamics influence trait evolution in a fungal crop pathogen

“…Active transcription of a TE can generate new TE insertions in the genome, as well as impact the structure and function of the genome (Feschotte, 2008; Wicker et al, 2018). The heterogeneous effects of RIP against different classes of TEs is compounded by the relaxation of RIP genomic defenses within the species following the expansion from the center of origin in the Middle East (Feurtey et al, 2023; Jovan Komluski, 2022; Moller et al, 2021).…”

“…Similarly, TE insertions are linked to the adaptive deletion of a gene encoding an effector, which is likely recognized by the plant host (Hartmann et al, 2017). The activity of TEs is generally high in the pathogen and varies with geography (Badet et al, 2020; Feurtey et al, 2023; Oggenfuss et al, 2021; Oggenfuss & Croll 2023).…”