Phylogenetic investigations in the genus Pseudoperonospora reveal overlooked species and cryptic diversity in the P. cubensis species cluster

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Pseudoperonospora cubensis is one of the most devastating diseases of cucurbitaceous crops. The pathogen has a worldwide distribution and occurs in all major cucurbit growing areas. It had been noticed for the first time at the end of the 19th century, but it became a globally severe disease as recently as 1984 in Europe and 2004 in North America. Despite its economic importance, species concepts in Pseudoperonospora are debated. Here, we report that the genus Pseudoperonospora contains cryptic species distinct from the currently accepted ones. Pseudoperonospora on Celtis is split into two phylogenetic lineages and Pseudoperonospora humuli is confirmed as a species distinct from the Cucurbitaceae-infecting lineages. A cryptic species occupying a basal position within the Pseudoperonospora cubensis complex is revealed to be present on Humulus japonicus, thus providing evidence that the host jump that gave rise to Pseudoperonospora cubensis likely occurred from hops. Notably, Cucurbitaceae infecting pathogens are present in two cryptic sister species or subspecies. Clade 1 contains primarily specimens from North America and likely represents Pseudoperonospora cubensis s.str.. Pre-epidemic isolates in clade 2 originate from Japan and Korea, suggesting this cryptic species or subspecies is indigenous to East Asia. Recent samples of this lineage from epidemics in Europe and the United States cluster together with clade 2. It thus seems possible that this lineage is associated with the recent severe epidemics of cucurbit downy mildew and is now naturalised in North America and Europe.