Sexual reproduction in the fungal foliar pathogen Zymoseptoria tritici is driven by antagonistic density-dependence mechanisms

This study provides empirical evidence for antagonistic density-dependence mechanisms driving sexual reproduction in the wheat fungal pathogen Zymoseptoria tritici. Biparental crosses with 12 increasing inoculum concentrations, in controlled conditions, showed that sexual reproduction in Z. tritici was impacted by an Allee effect due to mate limitation and a competition with asexual multiplication for resource allocation. The highest number of ascospores discharged was reached at intermediate inoculum concentrations (from 5.104 conidia.mL−1 to 106 conidia.mL−1). Consistent with these results for controlled co-inoculation, we found that the intensity of sexual reproduction varied with both cropping period and the vertical position of the host tissues in the field, with a maximum between 25 and 35 cm above the ground. An optimal lesion density (disease severity of 30 to 45%) maximizing offspring (ascospores) number was established, and its eco-evolutionary consequences are considered here. Two ecological mechanisms may be involved: competition for resources between the two modes of reproduction (decrease in the host resources available for sexual reproduction due to their prior use in asexual multiplication), and competitive disequilibrium between the two parental isolates, due to differential interaction dynamics with the host, for example, leading to an imbalance between mating types. A conceptual model based on these results suggest that sexual reproduction plays a key role in the evolution of pathogenicity traits, including virulence and aggressiveness. Ecological knowledge about the determinants of sexual reproduction in Z. tritici may, therefore, open up new perspectives for the management of other fungal foliar pathogens with dual modes of reproduction. We thank Nathalie Retout (INRA BIOGER, France) for technical assistance, Dr. Frédéric Hamelin (Agrocampus Ouest, France) for preliminary discussions on ecological modeling aspects, and Anne-Lise Boixel (INRA BIOGER, France) for her help in statistical analyses. We thank Julie Sappa for her help correcting our English. We thank Dr. Alexey Mikaberidze and Prof. Bruce McDonald (ETH Zürich, Switzerland) for providing the ST99CH-3D7 and ST99CH-1A5 strains of Z. tritici and seeds of the wheat cv. Runal. We thank the two anonymous reviewers for their constructive comments, which helped us to improve the manuscript. This study was supported by a grant from the European Union Horizon Framework 2020 Program (Grant Agreement no. 634179, EMPHASIS project) covering the 2015-2019 period.