Pathogens cause significant challenges to global food security. On annual crops, pathogens must re-infect from environmental sources in every growing season. Fungal pathogens have evolved mixed reproductive strategies to cope with the distinct challenges of colonizing growing plants. However, how pathogen diversity evolves during growing seasons remains largely unknown. Here, we performed a deep hierarchical sampling in a single experimental wheat field infected by the major fungal pathogen Zymoseptoria tritici. We analysed whole genome sequences of 177 isolates collected from 12 distinct cultivars replicated in space at three time points of the growing season to maximize capture of genetic diversity. The field population was highly diverse with 37 SNPs per kilobase, a linkage disequilibrium decay within 200–700 bp and a high effective population size. Using experimental infections, we tested a subset of the collected isolates on the dominant cultivar planted in the field. However, we found no significant difference in virulence of isolates collected from the same cultivar compared to isolates collected on other cultivars. About 20 % of the isolate genotypes were grouped into 15 clonal groups. Pairs of clones were disproportionally found at short distances (<5 m), consistent with experimental estimates for per-generation dispersal distances performed in the same field. This confirms predominant leaf-to-leaf transmission during the growing season. Surprisingly, levels of clonality did not increase over time in the field although reproduction is thought to be exclusively asexual during the growing season. Our study shows that the pathogen establishes vast and stable gene pools in single fields. Monitoring short-term evolutionary changes in crop pathogens will inform more durable strategies to contain diseases.

Transposable elements (TEs) are key drivers of adaptive evolution within species. Yet, the propagation of TEs across the genome can be highly deleterious and ultimately lead to genome expansions. Hence, TE activity is likely under complex selection regimes within species. To address this, we analyzed a large whole-genome sequencing dataset of the fungal wheat pathogen Zymoseptoria tritici harboring TE-mediated adaptations to overcome host defenses and fungicides. We built a robust map of genome-wide TE insertion and deletion loci for six populations and 284 fungal individuals across the world. We identified a total of 2’456 unfixed TE loci within the species and a significant excess of rare insertions indicating strong purifying selection. A subset of TEs recently swept to near complete fixation with at least one locus likely contributing to higher levels of fungicide resistance. TE-driven adaptation was also supported by evidence for selective sweeps. In parallel, we identified a substantial genome-wide expansion of TE families from the pathogen’s center of origin to more recently founded populations, suggesting that population bottlenecks played a major role in shaping TE content of the genome. The most dramatic expansion occurred among a pair of North American populations collected in the same field at an interval of 25 years. We show that both the activation of specific TEs and relaxed purifying selection likely underpin the expansion. Our study disentangles the effects of selection and TE bursts leading to intra-specific genome expansions, providing a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

Genome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations, but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogen’s center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

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Plant-soil feedbacks refer to effects on plants that are mediated by soil modifications caused by the previous plant generation. Maize conditions the surrounding soil by secretion of root exudates including benzoxazinoids (BXs), a class of bioactive secondary metabolites. Previous work found that a BX-conditioned soil microbiota enhances insect resistance while reducing biomass in the next generation of maize plants. Whether these BX-mediated and microbially driven feedbacks are conserved across different soils and response species is unknown. We found the BX-feedbacks on maize growth and insect resistance conserved between two arable soils, but absent in a more fertile grassland soil, suggesting a soil-type dependence of BX feedbacks. We demonstrated that wheat also responded to BX-feedbacks. While the negative growth response to BX-conditioning was conserved in both cereals, insect resistance showed opposite patterns, with an increase in maize and a decrease in wheat. Wheat pathogen resistance was not affected. Finally and consistent with maize, we found the BX-feedbacks to be cultivar-specific. Taken together, BXfeedbacks affected cereal growth and resistance in a soil and genotype-dependent manner. Cultivar-specificity of BX-feedbacks is a key finding, as it hides the potential to optimize crops that avoid negative plant-soil feedbacks in rotations.

AbstractPathogens can rapidly surmount crop resistance challenging global food security. On annual crops, pathogens must re-infect from environmental sources at the beginning of every growing season. Fungal pathogens evolved mixed reproductive strategies to cope with the distinct life cycle challenges of colonizing plants, spreading within fields and ultimately producing propagules for survival in winter. However, how genotypic diversity evolves over this period remains largely unknown. Here, we performed a deep hierarchical sampling in a single experimental wheat field infected by the major fungal pathogen Zymoseptoria tritici. We analyzed whole genome sequences of 177 isolates collected from twelve distinct cultivars replicated in space at three time points of the growing season. The field population was highly diverse with 37 SNPs per kilobase and a linkage disequilibrium decay within 200-700 bp. We found that ~20% of the individual isolates were grouping into 15 clonal groups. Pairs of clones were disproportionally found at short distance (<5m) but a low degree of dispersal occurred also at the scale of the entire field consistent with a predominant leaf-to-leaf dispersal. We found no association of wheat cultivars and clonal genotypes with the exception of one cultivar. Surprisingly, levels of clonality did not increase over time in the field although reproduction is thought to be exclusively asexual during the growing season. Our study shows that the pathogen establishes vast and stable gene pools in single fields over the growing season. Monitoring short-term evolutionary changes in crop pathogens will inform more durable strategies to contain diseases.Data summaryAll Illumina sequencing datasets are available from the NCBI Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra). The Supplementary Tables S1-S3 list the exact strain names, collection location, genotype and genetic diversity indices.

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Our data revealed a high incidence of Gram-positive cocci causing PPI. Every hospital should formulate their antibiotic policy based on the pattern of the hospital flora and their drug sensitivity.