IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36674-y.html
   My bibliography  Save this article

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

Author

Listed:
  • Alice Feurtey

    (University of Neuchâtel
    Plant Pathology, D-USYS, ETH Zurich
    Max Planck Institute for Evolutionary Biology)

  • Cécile Lorrain

    (Plant Pathology, D-USYS, ETH Zurich)

  • Megan C. McDonald

    (The Australian National University
    University of Birmingham)

  • Andrew Milgate

    (Wagga Wagga Agricultural Institute)

  • Peter S. Solomon

    (The Australian National University)

  • Rachael Warren

    (The New Zealand Institute for Plant and Food Research Limited)

  • Guido Puccetti

    (University of Neuchâtel
    Syngenta Crop Protection AG)

  • Gabriel Scalliet

    (Syngenta Crop Protection AG)

  • Stefano F. F. Torriani

    (Syngenta Crop Protection AG)

  • Lilian Gout

    (Université Paris Saclay, INRAE, UR BIOGER)

  • Thierry C. Marcel

    (Université Paris Saclay, INRAE, UR BIOGER)

  • Frédéric Suffert

    (Université Paris Saclay, INRAE, UR BIOGER)

  • Julien Alassimone

    (Plant Pathology, D-USYS, ETH Zurich)

  • Anna Lipzen

    (Lawrence Berkeley National Laboratory)

  • Yuko Yoshinaga

    (Lawrence Berkeley National Laboratory)

  • Christopher Daum

    (Lawrence Berkeley National Laboratory)

  • Kerrie Barry

    (Lawrence Berkeley National Laboratory)

  • Igor V. Grigoriev

    (Lawrence Berkeley National Laboratory
    University of California Berkeley)

  • Stephen B. Goodwin

    (USDA-Agricultural Research Service)

  • Anne Genissel

    (Université Paris Saclay, INRAE, UR BIOGER)

  • Michael F. Seidl

    (Laboratory of Phytopathology
    Utrecht University, Theoretical Biology and Bioinformatics)

  • Eva H. Stukenbrock

    (Max Planck Institute for Evolutionary Biology
    Christian-Albrechts University of Kiel)

  • Marc-Henri Lebrun

    (Université Paris Saclay, INRAE, UR BIOGER)

  • Gert H. J. Kema

    (Laboratory of Phytopathology)

  • Bruce A. McDonald

    (Plant Pathology, D-USYS, ETH Zurich)

  • Daniel Croll

    (University of Neuchâtel)

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.

Suggested Citation

  • Alice Feurtey & Cécile Lorrain & Megan C. McDonald & Andrew Milgate & Peter S. Solomon & Rachael Warren & Guido Puccetti & Gabriel Scalliet & Stefano F. F. Torriani & Lilian Gout & Thierry C. Marcel &, 2023. "A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36674-y
    DOI: 10.1038/s41467-023-36674-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36674-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36674-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Daniel P. Bebber & Mark A. T. Ramotowski & Sarah J. Gurr, 2013. "Crop pests and pathogens move polewards in a warming world," Nature Climate Change, Nature, vol. 3(11), pages 985-988, November.
    2. Alexandros G. Sotiropoulos & Epifanía Arango-Isaza & Tomohiro Ban & Chiara Barbieri & Salim Bourras & Christina Cowger & Paweł C. Czembor & Roi Ben-David & Amos Dinoor & Simon R. Ellwood & Johannes Gr, 2022. "Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Joseph K Pickrell & Jonathan K Pritchard, 2012. "Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data," PLOS Genetics, Public Library of Science, vol. 8(11), pages 1-17, November.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Sabina Moser Tralamazza & Emile Gluck-Thaler & Alice Feurtey & Daniel Croll, 2024. "Copy number variation introduced by a massive mobile element facilitates global thermal adaptation in a fungal wheat pathogen," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Barton, Madeleine G. & Terblanche, John S. & Sinclair, Brent J., 2019. "Incorporating temperature and precipitation extremes into process-based models of African lepidoptera changes the predicted distribution under climate change," Ecological Modelling, Elsevier, vol. 394(C), pages 53-65.
    2. Alexandros G. Sotiropoulos & Epifanía Arango-Isaza & Tomohiro Ban & Chiara Barbieri & Salim Bourras & Christina Cowger & Paweł C. Czembor & Roi Ben-David & Amos Dinoor & Simon R. Ellwood & Johannes Gr, 2022. "Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Cliff Zinyemba & Emma Archer & Hanna-Andrea Rother, 2020. "Climate Change, Pesticides and Health: Considering the Risks and Opportunities of Adaptation for Zimbabwean Smallholder Cotton Growers," IJERPH, MDPI, vol. 18(1), pages 1-11, December.
    4. Alejandro Ochoa & John D Storey, 2021. "Estimating FST and kinship for arbitrary population structures," PLOS Genetics, Public Library of Science, vol. 17(1), pages 1-36, January.
    5. Buzbas, Erkan Ozge & Verdu, Paul, 2018. "Inference on admixture fractions in a mechanistic model of recurrent admixture," Theoretical Population Biology, Elsevier, vol. 122(C), pages 149-157.
    6. Timothy M. Lenton & Chi Xu & Jesse F. Abrams & Ashish Ghadiali & Sina Loriani & Boris Sakschewski & Caroline Zimm & Kristie L. Ebi & Robert R. Dunn & Jens-Christian Svenning & Marten Scheffer, 2023. "Quantifying the human cost of global warming," Nature Sustainability, Nature, vol. 6(10), pages 1237-1247, October.
    7. Moti Jaleta & Dave Hodson & Bekele Abeyo & Chilot Yirga & Olaf Erenstein, 2019. "Smallholders’ coping mechanisms with wheat rust epidemics: Lessons from Ethiopia," PLOS ONE, Public Library of Science, vol. 14(7), pages 1-23, July.
    8. Ningbo Chen & Xiaoting Xia & Quratulain Hanif & Fengwei Zhang & Ruihua Dang & Bizhi Huang & Yang Lyu & Xiaoyu Luo & Hucai Zhang & Huixuan Yan & Shikang Wang & Fuwen Wang & Jialei Chen & Xiwen Guan & Y, 2023. "Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Soraggi, Samuele & Wiuf, Carsten, 2019. "General theory for stochastic admixture graphs and F-statistics," Theoretical Population Biology, Elsevier, vol. 125(C), pages 56-66.
    10. Justice A. Tambo & Lenis Saweda O. Liverpool‐Tasie, 2024. "Are farm input subsidies a disincentive for integrated pest management adoption? Evidence from Zambia," Journal of Agricultural Economics, Wiley Blackwell, vol. 75(2), pages 740-763, June.
    11. Crystal M. Tomlin & Sitaram Rajaraman & Jeanne Theresa Sebesta & Anne-Cathrine Scheen & Mika Bendiksby & Yee Wen Low & Jarkko Salojärvi & Todd P. Michael & Victor A. Albert & Charlotte Lindqvist, 2024. "Allopolyploid origin and diversification of the Hawaiian endemic mints," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. R. A. Mumford & R. Macarthur & N. Boonham, 2016. "The role and challenges of new diagnostic technology in plant biosecurity," Food Security: The Science, Sociology and Economics of Food Production and Access to Food, Springer;The International Society for Plant Pathology, vol. 8(1), pages 103-109, February.
    13. Adolfo Quesada-Román & Lilliam Quirós-Arias & Juan Carlos Zamora-Pereira, 2022. "Interactions between Geomorphology and Production Chain of High-Quality Coffee in Costa Rica," Sustainability, MDPI, vol. 14(9), pages 1-15, April.
    14. Humberto García-Ortiz & Francisco Barajas-Olmos & Cecilia Contreras-Cubas & Miguel Ángel Cid-Soto & Emilio J. Córdova & Federico Centeno-Cruz & Elvia Mendoza-Caamal & Isabel Cicerón-Arellano & Marlen , 2021. "The genomic landscape of Mexican Indigenous populations brings insights into the peopling of the Americas," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    15. Philippe Gambette & Leo van Iersel & Mark Jones & Manuel Lafond & Fabio Pardi & Celine Scornavacca, 2017. "Rearrangement moves on rooted phylogenetic networks," PLOS Computational Biology, Public Library of Science, vol. 13(8), pages 1-21, August.
    16. Ran Tian & Yaolei Zhang & Hui Kang & Fan Zhang & Zhihong Jin & Jiahao Wang & Peijun Zhang & Xuming Zhou & Janet M. Lanyon & Helen L. Sneath & Lucy Woolford & Guangyi Fan & Songhai Li & Inge Seim, 2024. "Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder afrotheria," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Falkner, Katharina & Schmid, Erwin & Mitter, Hermine, 2021. "Integrated modelling of cost-effective policies to regulate Western Corn Rootworm under climate scenarios in Austria," Ecological Economics, Elsevier, vol. 188(C).
    18. Elena Arciero & Sufyan A. Dogra & Daniel S. Malawsky & Massimo Mezzavilla & Theofanis Tsismentzoglou & Qin Qin Huang & Karen A. Hunt & Dan Mason & Saghira Malik Sharif & David A. Heel & Eamonn Sherida, 2021. "Fine-scale population structure and demographic history of British Pakistanis," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    19. Huagang He & Zhaozhao Chen & Renchun Fan & Jie Zhang & Shanying Zhu & Jiale Wang & Qianyuan Zhang & Anli Gao & Shuangjun Gong & Lu Zhang & Yanan Li & Yitong Zhao & Simon G. Krattinger & Qian-Hua Shen , 2024. "A kinase fusion protein from Aegilops longissima confers resistance to wheat powdery mildew," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    20. Chris J. Brauer & Jonathan Sandoval-Castillo & Katie Gates & Michael P. Hammer & Peter J. Unmack & Louis Bernatchez & Luciano B. Beheregaray, 2023. "Natural hybridization reduces vulnerability to climate change," Nature Climate Change, Nature, vol. 13(3), pages 282-289, March.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36674-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.