Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew, Plasmopara viticola

Abstract

Europe is the historical cradle of viticulture, but grapevines (Vitis vinifera) have been increasingly threatened by pathogens of American origin. The invasive oomycete Plasmopara viticola causes downy mildew, one of the most devastating grapevine diseases worldwide. Despite major economic consequences, its invasion history remains poorly understood. We analyzed a comprehensive dataset of ∼2,000 samples, collected from the most important wine-producing countries, using nuclear and mitochondrial gene sequences and microsatellite markers. Population genetic analyses revealed very low genetic diversity in invasive downy mildew populations worldwide and little evidence of admixture. All the invasive populations originated from only one of the five native North American lineages, the one parasitizing wild summer grape (V.aestivalis). An approximate Bayesian computation-random forest approach allowed inferring the worldwide invasion scenario of P.viticola. After an initial introduction into Europe, invasive European populations served as a secondary source of introduction into vineyards worldwide, including China, South Africa, and twice independently, Australia. Only the invasion of Argentina probably represents a tertiary introduction, from Australia. Our findings provide a striking example of a global pathogen invasion resulting from secondary dispersal of a successful invasive population. Our study will also help designing quarantine regulations and efficient breeding for resistance against grapevine downy mildew.