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Puccetti, G.

Publications and source records attributed to Puccetti, G..

4 recordsLinked to original sources

A pangenomics-enabled platform for the high-throughput discovery of antifungal resistance factors in crop pathogens

The rise of antifungal resistance is a global challenge for both human health and food security, because resistance emergence easily outpaces the antifungal development pipeline. Furthermore, resistance arises often in parallel and through alternative mechanisms creating challenges to predict emergence. In agriculture, where vast areas are sprayed by diverse cocktails, antifungal resistance gains are particularly complex. Despite broad efforts, knowledge of resistance mechanisms is often limited to model genotypes and empirical evidence from the field is lacking. Here, we define and validate a high- throughput pipeline for antifungal resistance discovery informed by emerging resistance gains at continental scale. We analyzed a thousand-genome European diversity panel of the major wheat pathogen Zymoseptoria tritici and assessed resistance levels against over 29 fungicides covering all major classes. We optimized high-throughput phenotyping assays to comprehensively capture emerging resistance phenotypes. Pangenome-informed genotyping techniques revealed a total of 2192 genes associated with antifungal resistance. This expands by an order of magnitude the current knowledge and establishes a refined atlas of resistance mutations. We generated mutants to recapitulate several of the discovered resistance factors. Hence, our approach captures in-field resistance gains across Europe for all major fungicide classes and can define exact molecular targets. Broad knowledge of resistance gains will guide more sustainable fungicide development pipelines.

microbiology↗

Historic transposon mobilisation waves create distinct pools of adaptive variants in a major crop pathogen

Transposable elements (TEs) can drive the evolution of host-pathogen interactions and gains in antimicrobial resistance. However, how adaptive TEs arise in populations and historical contingencies affect TE dynamics remains unknown. Fungal pathogens in agriculture provide unique frameworks to address such questions due to the availability of spatially explicit sampling and well- characterized niche conditions. We characterised TE evolutionary dynamics using an extensive intraspecies sampling of 1,953 genomes across the global distribution range of the major fungal wheat pathogen Zymoseptoria tritici. Employing a pangenomic approach, we characterise genomic diversity and benchmark methods to robustly infer TE insertion polymorphism, before systematically assessing TEs as a source of adaptive variation. We annotated [~]3.2 million TE loci among genomes, finding substantial variation in TE content within and among populations. TE activity surged during the pathogens expansion from its centre of origin in the Middle East, with unique TE activity profiles arising in derived populations. TE-mediated adaptation emerged from distinct waves of TE mobilization. The highest rates of TE activity were observed over timescales as short as 25 years. 45 TE loci showing local adaptation signatures within 1kb of 49 host genes were identified, with adaptive TE insertions likely related to adaptation to antifungals and the plant host environment. This work highlights the power of vast genomic datasets to unravel intraspecies TE invasion histories and pinpoint factors likely driving recent adaptation. This argues for a shift in focus to incorporate deep population-level TE activity surveys in our pursuit to uncover the molecular drivers of adaptive evolution.

genomics↗

A large European diversity panel reveals complex azole fungicide resistance gains of a major wheat pathogen

Fungicide resistance in crop pathogens poses severe challenges to sustainable agriculture. Demethylation inhibitors (DMIs) are critical for controlling crop diseases but face rapid resistance gains in the field. Even though the main molecular basis of resistance is well established, field surveys have repeatedly revealed alternative resistance mechanisms. The European continent in particular has seen rapid and heterogeneous gains in azole resistance in the past decades. Here, we establish a large genome panel to dissect the genetic architecture of emerging resistance in the major wheat pathogen Zymoseptoria tritici. The European diversity panel spans 15 sampling years and 27 countries for a total of 1394 sequenced and phenotyped strains. Using two complementary assays to quantify resistance levels of each strain, we captured fine-grained shifts in DMI resistance over space and time. We conducted genome-wide association studies based on a comprehensive set of genotyping approaches for six DMIs. We mapped a total of 21,220 genetic variants and 158 genes linked to resistance. The substantial scope in genetic mechanisms underpinning DMI resistance significantly expands our mechanistic understanding how continent-wide resistance arises in fungal pathogens over time. Diversification of the Cyp51 coding sequence was particularly striking with new resistant haplotypes emerging with complex configurations and geographic patterns. This study provides expansive new insights into fungicide resistance gains of crop pathogens relevant for future resistance management strategies.

microbiology↗

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

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.

genomics↗