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

Authors: FEURTEY, ALICE - NEUCHATEL UNIVERSITY - SWITZERLAND; LORRAIN, CECILE - ETH ZURICH; MCDONALD, MEGAN - THE AUSTRALIAN NATIONAL UNIVERSITY; MILGATE, ANDREW - WAGGA WAGGA AGRICULTURAL INSTITUTE; SOLOMON, PETER - CANBERRA; WARREN, RACHEL - NEW ZEALAND INSTITUTE OF PLANT & FOOD RESEARCH; PUCCETTI, GUIDO - NEUCHATEL UNIVERSITY - SWITZERLAND; SCALLIET, GABRIEL - SYNGENTA AG; GOUT, LILIAN - UNIVERSITÉ PARIS-SACLAY; MARCEL, THIERRY - UNIVERSITÉ PARIS-SACLAY; SUFERT, FREDERIC - UNIVERSITÉ PARIS-SACLAY; ALASSIMONE, JULIEN - ETH ZURICH; LIPZEN, ANNA - DEPARTMENT OF ENERGY JOINT GENOME; YOSHINAGA, YUKO - DEPARTMENT OF ENERGY JOINT GENOME; DAUM, CHRISTOPHER - DEPARTMENT OF ENERGY JOINT GENOME; BARRY, KERRIE - DEPARTMENT OF ENERGY JOINT GENOME; GRIGORIEV, IGOR - DEPARTMENT OF ENERGY JOINT GENOME; Goodwin, Stephen - Steve; GENISSEL, ANNNE - UNIVERSITÉ PARIS-SACLAY; LEBRUN, MARC-HENRI - UNIVERSITÉ PARIS-SACLAY; KEMA, GERT - WAGENINGEN UNIVERSITY AND RESEARCH CENTER; MCDONALD, BRUCE - ETH ZURICH; CROLL, DANIEL - NEUCHATEL UNIVERSITY - SWITZERLAND

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/19/2023
Publication Date: 2/24/2023
Citation: Feurtey, A., Lorrain, C., McDonald, M.C., Milgate, A., Solomon, P.S., Warren, R., Puccetti, G., Scalliet, G., Torriani, S.F.F., Gout, L., Marcel, T.C., Suffert, F., Alassimone, J., Lipzen, A., Yoshinaga, Y., Daum, C., Barry, K., Grigoriev, I.V., Goodwin, S.B., Genissel, A., Seidel, M.F., Stukenbrock, E.H., Lebrun, M.-H., Kema, G.H.J., McDonald, B.A., Croll, D. 2023. A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen. Nature Communications. 14. Article 1059. https://doi.org/10.1038/s41467-023-36674-y.
DOI: https://doi.org/10.1038/s41467-023-36674-y

Interpretive Summary: Understanding how pathogens overcome control strategies and cope with new climates is crucial to predicting their future impacts and evolution. To test for adaptation to climates during dispersal, more than 1,100 genome sequences from a worldwide collection of isolates of the fungal pathogen Zymoseptoria tritici, the cause of Septoria tritici blotch of wheat, were obtained and analyzed for variation in molecular markers. Analysis of this huge data set identified the routes of global invasion and ongoing genetic exchange among populations of the pathogen in different wheat-growing regions. The global spread of the pathogen with its host was accompanied by increased activity of movable genetic elements, weakened genome defenses, and genetic variation that facilitated adaptation to new climates encountered during its evolution. These results will be of interest to evolutionary biologists and plant pathologists trying to understand the evolution and spread of crop pathogens to new growing areas and how they are likely to be affected by changing climates in the future.

Technical 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.