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Hybridization and introgression drive genome evolution of Dutch elm disease pathogens

Nature Ecology & Evolution volume 4, pages 626–638 (2020)Cite this article

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Abstract

Hybridization and the resulting introgression can drive the success of invasive species via the rapid acquisition of adaptive traits. The Dutch elm disease pandemics in the past 100 years were caused by three fungal lineages with permeable reproductive barriers: Ophiostoma ulmi, Ophiostoma novo-ulmi subspecies novo-ulmi and Ophiostoma novo-ulmi subspecies americana. Using whole-genome sequences and growth phenotyping of a worldwide collection of isolates, we show that introgression has been the main driver of genomic diversity and that it impacted fitness-related traits. Introgressions contain genes involved in host–pathogen interactions and reproduction. Introgressed isolates have enhanced growth rate at high temperature and produce different necrosis sizes on an in vivo model for pathogenicity. In addition, lineages diverge in many pathogenicity-associated genes and exhibit differential mycelial growth in the presence of a proxy of a host defence compound, implying an important role of host trees in the molecular and functional differentiation of these pathogens.

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Fig. 1: Clustering analyses based on genomic variation of worldwide Ophiostoma species samples show among-lineage admixture.
Fig. 2: Introgression between DED-causing Ophiostoma lineages is frequent.
Fig. 3: The most diverse genomic regions in ONU derive from recent introgression from OU.
Fig. 4: Hybridization and introgression have a strong impact on growth rate and virulence.

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Data availability

Read sequence data that support the findings of this study have been deposited in the Sequence Read Archive repository under BioProject number PRJNA566197. Genome sequence variant file (VCF) and phenotyping data are available on Figshare (https://doi.org/10.6084/m9.figshare.11663811).

Code availability

All custom codes, as well as descriptions, versions and URLs of all open-source software used in this study are provided at https://github.com/Landrylab/Ophiostoma_Hybridization_2019.

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Acknowledgements

This work was funded by Genome Canada, Genome British Columbia and Génome Québec within the framework of project bioSAFE (Biosurveillance of Alien Forest Enemies; project number 10106). Additional funding was provided by the Canadian Food Inspection Agency, Natural Resources Canada and FPInnovations and by the NSERC Discovery Grant of C.R.L. We thank A. Dubé, A. Gagné, I. Giguère and A. Potvin for help with the experiments, W. Babik and the Landry laboratory for comments and discussions, the McGill University and the Centre d’Expertise et de Services Génome Québec and the Institut de Biologie Intégrative et des Systèmes bioinformatics platform for technical support.

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Author notes

  1. Julien Prunier

    Present address: Centre de Recherche du CHU de Québec, Département de Médecine Moléculaire, Faculté de Médecine, Université Laval, Québec, Québec, Canada

  2. These authors contributed equally: Pauline Hessenauer, Anna Fijarczyk.

Authors and Affiliations

  1. Département des Sciences du Bois et de la Forêt, Faculté de Foresterie, de Géographie et de Géomatique, Université Laval, Québec, Québec, Canada

    Pauline Hessenauer, Julien Prunier, Jérôme Chapuis, Louis Bernier & Richard C. Hamelin

  2. Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Québec, Canada

    Pauline Hessenauer, Anna Fijarczyk, Hélène Martin, Julien Prunier, Guillaume Charron, Jérôme Chapuis, Louis Bernier, Richard C. Hamelin & Christian R. Landry

  3. Département de Biologie, Faculté des Sciences et de Génie, Université Laval, Québec, Québec, Canada

    Anna Fijarczyk, Hélène Martin, Guillaume Charron & Christian R. Landry

  4. Le Réseau Québécois de Recherche sur la Fonction, la Structure et l’Ingénierie des Protéines (PROTEO), Université Laval, Québec, Québec, Canada

    Anna Fijarczyk, Hélène Martin, Guillaume Charron & Christian R. Landry

  5. Centre de Recherche en Données Massives (CRDM), Université Laval, Québec, Québec, Canada

    Anna Fijarczyk, Hélène Martin, Guillaume Charron & Christian R. Landry

  6. Centre d’Étude de la Forêt, Université Laval, Québec, Québec, Canada

    Louis Bernier

  7. Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, Québec, Canada

    Philippe Tanguay

  8. Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, British Columbia, Canada

    Richard C. Hamelin

  9. Département de Biochimie, Microbiologie et Bio-informatique, Faculté des Sciences et de Génie, Université Laval, Québec, Québec, Canada

    Christian R. Landry

Authors
  1. Pauline Hessenauer
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  2. Anna Fijarczyk
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  3. Hélène Martin
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  4. Julien Prunier
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  5. Guillaume Charron
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  6. Jérôme Chapuis
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  8. Philippe Tanguay
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  9. Richard C. Hamelin
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Contributions

P.H., A.F., H.M., P.T., R.C.H. and C.R.L. designed the study. L.B. provided the isolates. P.H. and J.P. selected the isolates from the collection of L.B. P.H. performed the DNA extractions. P.H., G.C. and J.C. performed the phenotyping experiments. P.H., A.F. and H.M. performed the genome analyses. P.H. and A.F. wrote the manuscript. All authors contributed to manuscript editing. R.C.H. and C.R.L. supervised the research. C.R.L. overviewed the analyses and writing.

Corresponding authors

Correspondence to Richard C. Hamelin or Christian R. Landry.

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Supplementary information

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Supplementary Figs. 1–18.

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Hessenauer, P., Fijarczyk, A., Martin, H. et al. Hybridization and introgression drive genome evolution of Dutch elm disease pathogens. Nat Ecol Evol 4, 626–638 (2020). https://doi.org/10.1038/s41559-020-1133-6

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  • DOI: https://doi.org/10.1038/s41559-020-1133-6

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