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Bremia lactucae populations on cultivated lettuce originate from prickly lettuce and are interconnected with the wild pathosystem

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Abstract

Bremia lactucae is a devastating pathogen causing heavy yield losses in lettuce production worldwide. Long time it was thought to infect various members of the Asteraceae but recent phylogenetic investigations revealed that B. lactucae is restricted to cultivated Lactuca sativa and its wild progenitor Lactuca serriola. Many resistance genes in cultivated lettuce were crossbred from L. serriola, but often a fast overcoming of the resistance in the crop by new downy mildew races was observed. Consequently, it seems important to investigate the population genetic relationships of wild prickly lettuce and cultivated lettuce, in order to determine, if the Bremia lineages infecting these hosts are distinct or intermingled. In the first case, searching for resistance in prickly lettuce is straightforward, in the second case it would rather be futile. Bremia belongs to the genera of downy mildews with pyriform haustoria, which feature highly variable ITS-repeats that can be used as high-resolution markers for population genetics studies. Here we report that Bremia lactucae on Lactuca sativa is not homogeneous but emerged from several host shifts from Lactuca serriola and that Bremia accessions from both species are not forming distinct genepools. While the pathogen population from L. serriola showed a balanced pattern, the pathogen population from L. sativa has a directional selection pattern reflecting founder effects after host shifts, resulting in a fast colonisation of susceptible lettuce cultivars. Thus, the wild population of Bremia lactucae seems to play a major role in the epidemiology of downy mildew on cultivated lettuce. This also explains, why resistance breeding using resistance genes from prickly lettuce had little success for achieving durable resistance in cultivated lettuce and calls for both more detailed research into Bremia on wild lettuce and new breeding strategies using less closely related lettuce species.

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Funding

This study was supported by a grant from the Ministry of Science, Education, and the Arts of Baden-Württemberg awarded to F. Runge and by the research funding program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts in the framework of the Centre for Translational Biodiversity Genomics (TBG) and the Cluster for Integrative Fungal Research (IPF). A. Lebeda acknowledge the support of grant MSM 6198959215 (funded by Ministry of Education, Youth and Sports of the Czech Republic), the National Programme of Genepool Conservation of Microorganisms and Small Animals of Economic Importance of the Czech Republic, and Internal Grant Agency of Palacký University in Olomouc (IGA_PrF_2018_001; IGA_PrF_2019_004; IGA_PrF_2020 003).

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  1. IDENTXX GmbH, Maybachstr. 50, D-70469, Stuttgart, Germany

    Fabian Runge

  2. Senckenberg Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, D-60325, Frankfurt am Main, Germany

    Fabian Runge & Marco Thines

  3. Department of Biology, Institute of Ecology, Evolution and Diversity, Goethe University, Campus Riedberg, Max-von-Laue-Str. 13, D-60439, Frankfurt am Main, Germany

    Fabian Runge & Marco Thines

  4. Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Stahnsdorfer Damm 81, D-14532, Kleinmachnow, Germany

    Ute Gärber

  5. Faculty of Science, Department of Botany, Palacký University in Olomouc, Šlechtitelů 27, CZ-78371, Olomouc, Czech Republic

    Aleš Lebeda

  6. Translational Biodiversity Genomics Centre (TBG), Georg-Voigt-Str. 14-16, D-60325, Frankfurt am Main, Germany

    Marco Thines

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Runge, F., Gärber, U., Lebeda, A. et al. Bremia lactucae populations on cultivated lettuce originate from prickly lettuce and are interconnected with the wild pathosystem. Eur J Plant Pathol 161, 411–426 (2021). https://doi.org/10.1007/s10658-021-02332-6

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