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.

BACKGROUND: Reliance on fungicides to manage disease creates selection pressure for the evolution of resistance in fungal and oomycete pathogens. Rust fungi (Pucciniales) are major pathogens of cereals and other crops and have been classified as low-risk for developing resistance to fungicides; no case offield failure of fungicides in a cereal rust diseasehas yet been recorded. Recently, the Asian soybean rust pathogen, Phakopsora pachyrhizi evolved resistance to several fungicide classes, prompting us to screen a large sample of the globally widespread wheat yellow rust pathogen, Puccinia striiformis f. sp. tritici (Pst), for mutations associated with fungicide resistance. RESULTS: We evaluated 363 Pst isolates from Europe, the USA, Ethiopia, Chile, China and New Zealand for mutations in the target genes of demethylase inhibitor (DMI; Cyp51) and succinate dehydrogenase inhibitor (SDHI; SdhB, SdhC and SdhD) fungicides. A high proportion of Pst isolates carrying a Y134F DMI resistance-associated substitution in the Cyp51 gene was found among those from China and New Zealand. A set of geographically diverse Pst isolates was also found to display a substitution in SdhC (I85V) that is homologous to that reported recently in P. pachyrhizi and linked to SDHI resistance. CONCLUSION:The identification of resistance-associated alleles confirms that cereal rusts are not immune to fungicide resistance and that selection for resistance evolution is operating at high levels in certain locations. It highlights the need to adopt fungicide resistance management practices and to monitor cereal rust species for development of resistance.

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.

Rust diseases are serious threats to New Zealand cereal crops. Beside the use of fungicides, resistant varieties are an important option for managing these diseases. Changes in rust pathotypes commonly occur due to mutations in existing populations or exotic incursions. Information on these changes is the basis of gene-based disease management. Rust-infected leaves were collected from cereal crops from 2012 to 2015. The pathotypes of these and some historic samples were determined in glasshouse studies, using specific differential host sets. Eight pathotypes of Puccinia triticina (Pt, causal agent of wheat leaf rust), five of P. striiformis f. sp. tritici (Pst, causal agent of wheat stripe rust) and two of P. hordei (Ph, causal agent of barley leaf rust) were identified. The Pst ‘WA’ pathotype was most frequently found. Wheat varieties ‘Empress’ and ‘Torch’, previously resistant to Pt, were found to be susceptible to leaf rust for the first time. The ‘WA’ pathotype of Pst is likely to have arrived in New Zealand from Australia, and is now widespread. The two Pt pathotypes could have overcome resistance gene Lr24 in ‘Empress’ and ‘Torch’.

Pseudomonas fluorescens are soilinhabiting plant growthpromoting rhizobacteria (PGPR) linked with suppression of takeall of wheat a soilborne disease caused by Gaeumannomyces graminis var tritici (Ggt) PGPR increase plant growth by direct stimulation producing metabolites (such as 24diacetylphloroglucinol 24DAPG) to inhibit plant pathogens or by inducing host defence mechanisms Fortythree New Zealand P fluorescens isolates collected from wheat rhizospheres of different cropping histories were characterised for secondary metabolite production using biochemical assays and PCR analysis Their ability to inhibit the growth of Ggt was determined in dual plate assays All of the bacterial isolates produced siderophores and 10 isolates produced hydrogen cyanide (HCN) However none of the isolates produced indole acetic acid and the phlD gene responsible for the production of 24DAPG was not detected Isolates that showed at least 60 inhibition of Ggt growth were found to produce either HCN or high levels of siderophore The results suggest HCN and siderophores could play a role in suppressing Ggt and managing takeall in New Zealand