Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen

Singh, Navreet; Badet, Thomas; Croll, Daniel

doi:10.21203/rs.3.rs-244755/v1

Cited by 4 publications

(14 citation statements)

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“…We analysed pathogenicity profiles for a subset of 120 isolates out of the total number of isolates analysed in this study. The pathogenicity assay dataset was generated to perform genome-wide association studies [45]. In summary, seedlings of the cultivar Claro were grown under controlled conditions as follows: 16/8 h day/night periods at 18 °C throughout the experiment.…”

Section: Culture Preparation and Seedling Infection Assaymentioning

confidence: 99%

“…Using greenhouse assays we tested whether isolates sampled from different time points or cultivars showed differences in virulence on the most frequent cultivar (CH Claro) planted in the field. For this, we analysed data generated for a genome-wide association study from a subset (n=120) of the isolates [45] (Table S5). We found that isolates from the third collection produced significantly more pycnidia (a proxy for pathogen reproduction) compared to earlier collection (one-way ANOVA, P=0.002) (Fig.…”

Section: Experimental Analyses Of Virulence On Cultivar Claromentioning

confidence: 99%

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Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici

2021

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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.

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Section: Culture Preparation and Seedling Infection Assaymentioning

confidence: 99%

Section: Experimental Analyses Of Virulence On Cultivar Claromentioning

confidence: 99%

Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici

2021

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“…tritici (strain 3D7). The second fully unrolled leaf of 3-week-old plants were spray-infected with 10 ml of blastospores following a standard infection protocol (Singh et al, 2021). The inoculated plants were kept at 100% relative humidity and 21 0 C for 2 days, before going back to initial growth conditions (see above).…”

Section: Pathogen Assaymentioning

confidence: 99%

Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

Cadot

Gfeller

et al. 2021

Preprint

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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, BX-feedbacks 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.

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“…We tested using greenhouse assays whether isolates sampled from different time points or cultivars showed differences in virulence on the most frequent cultivar (CH Claro) planted in the field. For this, we analyzed data generated for a genome-wide association study from a subset (n = 120) of the isolates (Singh et al 2021, DOI pending; Supplementary Table S5). We found that isolates from the third collection to produce significantly more pycnidia (a proxy for pathogen reproduction) compared to earlier collection (one-way ANOVA, p-value = 0.002) (Figure 6A-B).…”

Section: Experimental Analyses Of Virulence On Cultivar Claromentioning

confidence: 99%

“…Z.tritici satisfies all these conditions, and a recent study has shown the successful application of GWAS to identify a candidate effector gene related to the pathogen's virulence (Plissonneau et al 2017;Singh, Badet, et al 2021;.…”

Section: General Introductionmentioning

confidence: 99%

Population genomics of lifestyle and virulence evolution in the fungal wheat pathogen "Zymoseptoria tritici"

Singh¹

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Plant pathogens cause significant reductions in agricultural productivity worldwide, and control strategies remain ineffective for many pathogens. Fungal plant pathogens often rapidly overcome resistance gene mediated immunity defeating expensive breeding efforts. Similarly, the deployment of synthetic chemicals is often followed by the rise of resistant pathogen populations. However, we still lack basic understanding how different evolutionary forces shape the genetic composition of pathogen populations. Additionally, how virulence evolves over time and its genetic basis remains largely unknown. In this PhD thesis was to study the lifestyle and virulence evolution in the fungal wheat pathogen Zymoseptoria tritici using population genomics, association mapping and metabolite analysis. We deep sequenced a large set of isolates of Zymoseptoria tritici sampled from multiple genetically distinct wheat cultivars replicated in space at three time points of the growing season. Population genomic analysis revealed an astonishing level of genetic diversity in a single field exceeding global diversity levels for many other pathogens. The study establishes the role of sexual and asexual reproduction in short-term adaptation, as recombination enables the reshuffling of allelic variation. In the second chapter, I used genome-wide association mapping to investigate genetic basis of fungal virulence of Z. triticion a commonly used wheat cultivar. The strongest association was intergenic and flanked by genes encoding a predicted effector and a serinetype protease. The virulence loci was highly dynamic, consisting of multiple families of transposable elements and strong signatures of repeat-induced point mutation (RIP), contributing to the locus's rapid diversification. In the third chapter investigated the genetic basis of metabolites production variation in a single field Z. tritici population. Using untargeted metabolic profile and GWAS we found strong associations in proximity genes encoding functions related to endosomal functions and transporters. Overall this PhD thesis highlights the potential of whole genome sequencing of a single field population in understanding the lifestyle and evolution of virulence for an important plant pathogen. Establishing a complete picture of the genomic basis of adaptation in a pathogen population will help in efficient designing of plant disease management strategies

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Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen

Cited by 4 publications

References 87 publications

Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici

Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici

Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

Population genomics of lifestyle and virulence evolution in the fungal wheat pathogen "Zymoseptoria tritici"

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