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Quantitative pathogenicity and host adaptation in a fungal plant pathogen revealed by whole-genome sequencing

Author

Listed:
  • Reda Amezrou

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Aurélie Ducasse

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Jérôme Compain

    (Université Paris-Saclay, INRAE, UR URGI)

  • Nicolas Lapalu

    (Université Paris-Saclay, INRAE, UR BIOGER
    Université Paris-Saclay, INRAE, UR URGI)

  • Anais Pitarch

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Laetitia Dupont

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Johann Confais

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Henriette Goyeau

    (Université Paris-Saclay, INRAE, UR BIOGER)

  • Gert H. J. Kema

    (Plant Research International B.V.)

  • Daniel Croll

    (Department of Ecology and Evolution, Université de Neuchâtel)

  • Joëlle Amselem

    (Université Paris-Saclay, INRAE, UR URGI)

  • Andrea Sanchez-Vallet

    (CBGP, INIA, Campus de Montegancedo UPM, Pozuelo de Alarcón)

  • Thierry C. Marcel

    (Université Paris-Saclay, INRAE, UR BIOGER)

Abstract

Knowledge of genetic determinism and evolutionary dynamics mediating host-pathogen interactions is essential to manage fungal plant diseases. Studies on the genetic architecture of fungal pathogenicity often focus on large-effect effector genes triggering strong, qualitative resistance. It is not clear how this translates to predominately quantitative interactions. Here, we use the Zymoseptoria tritici-wheat model to elucidate the genetic architecture of quantitative pathogenicity and mechanisms mediating host adaptation. With a multi-host genome-wide association study, we identify 19 high-confidence candidate genes associated with quantitative pathogenicity. Analysis of genetic diversity reveals that sequence polymorphism is the main evolutionary process mediating differences in quantitative pathogenicity, a process that is likely facilitated by genetic recombination and transposable element dynamics. Finally, we use functional approaches to confirm the role of an effector-like gene and a methyltransferase in phenotypic variation. This study highlights the complex genetic architecture of quantitative pathogenicity, extensive diversifying selection and plausible mechanisms facilitating pathogen adaptation.

Suggested Citation

  • Reda Amezrou & Aurélie Ducasse & Jérôme Compain & Nicolas Lapalu & Anais Pitarch & Laetitia Dupont & Johann Confais & Henriette Goyeau & Gert H. J. Kema & Daniel Croll & Joëlle Amselem & Andrea Sanche, 2024. "Quantitative pathogenicity and host adaptation in a fungal plant pathogen revealed by whole-genome sequencing," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46191-1
    DOI: 10.1038/s41467-024-46191-1
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    References listed on IDEAS

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    1. Thierry Rouxel & Jonathan Grandaubert & James K. Hane & Claire Hoede & Angela P. van de Wouw & Arnaud Couloux & Victoria Dominguez & Véronique Anthouard & Pascal Bally & Salim Bourras & Anton J. Cozij, 2011. "Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations," Nature Communications, Nature, vol. 2(1), pages 1-10, September.
    2. Cyrille Saintenac & Florence Cambon & Lamia Aouini & Els Verstappen & Seyed Mahmoud Tabib Ghaffary & Théo Poucet & William Marande & Hélène Berges & Steven Xu & Maëlle Jaouannet & Bruno Favery & Julie, 2021. "A wheat cysteine-rich receptor-like kinase confers broad-spectrum resistance against Septoria tritici blotch," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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