Rethinking grapevine downy mildew management: opportunities to disrupt the sexual cycle of the pathogen as a preventive disease control strategy.

Plant diseases caused by fungal and oomycete pathogens with mixed reproduction systems include some of the most damaging crop diseases. These pathogens reproduce asexually under low-stress conditions during the growing season in order to propagate rapidly and efficiently. They then shift to sexual reproduction when conditions become harsher, so as to survive and adapt. For those that are obligate biotroph pathogens with a deciduous host, sexual reproduction is a necessary step in their life cycle. Plasmopara viticola, the oomycete causing grapevine downy mildew (GDM), is a representative example, particularly in temperate regions in which grapevines enter dormancy in autumn. Current efforts to control GDM, including those comprising Integrated Pest Management (IPM), are typically limited to the grapevine's growing season. They target the primary contamination and the asexual propagation of P. viticola and consist most typically of repeated fungicide applications whenever contamination conditions are met. However, strategies that would target the sexual cycle of P. viticola during the offseason are often overlooked, even though related approaches are successful in other plant-pathogen systems. We discuss several novel interventions informed by plant pathogen biology, epidemiology, and ecology that would disrupt the pathogen's sexual cycle at several key points, reducing both the epidemic pressure and the ability of the pathogen to adapt from one growing season to the next. Furthermore, we identify the main scientific and technical challenges to be overcome. In line with IPM, we call for a shift toward a preventive, long-term vision of plant disease management and more sustainable agroecosystems.