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

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Abstract

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.

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Acknowledgements

The curators of the herbaria BP, BRIP, DAR, FH, and NY are gratefully acknowledged for sending specimens for investigation. Aleš Lebeda, Catherine Erhard, and Peggy Marx are gratefully acknowledged for providing some of the Pseudoperonospora cubensis strains that were used in this study. The present study was financially supported by the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts and by a grant from the German Science Foundation (DFG) awarded to MT.

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  1. Institute of Botany 210, University of Hohenheim, 70593, Stuttgart, Germany

    Fabian Runge

  2. Department of Organism & Evolutionary Biology, Harvard University, 22 Divinity Ave, Cambridge, MA, 02138, USA

    Young-Joon Choi

  3. Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325, Frankfurt (Main), Germany

    Marco Thines

  4. Department of Biological Sciences, Institute of Ecology, Evolution and Diversity, Johann Wolfgang Goethe University, Siesmayerstr. 70, 60325, Frankfurt (Main), Germany

    Marco Thines

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  1. Fabian Runge
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Runge, F., Choi, YJ. & Thines, M. Phylogenetic investigations in the genus Pseudoperonospora reveal overlooked species and cryptic diversity in the P. cubensis species cluster. Eur J Plant Pathol 129, 135–146 (2011). https://doi.org/10.1007/s10658-010-9714-x

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