Population structure of Erysiphe necator on domesticated and wild vines in the Middle East sheds a new light on the origins of the grapevine powdery mildew pathogen

Authors: GUR, LIOR - University Of Haifa; REUVENI, MOSHE - University Of Haifa; COHEN, YIGAL - Bar-Ilan University; Cadle-Davidson, Lance; KISSELSTEIN, BREANNE - US Department Of Agriculture (USDA); OVADIA, SHMUEL - Carmel Winery; FRENKEL, OMER - Agricultural Research Organization, Volcani Center

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/16/2021
Publication Date: 1/18/2021
Citation: Gur, L., Reuveni, M., Cohen, Y., Cadle Davidson, L.E., Kisselstein, B., Ovadia, S., Frenkel, O. 2021. Population structure of Erysiphe necator on domesticated and wild vines in the Middle East sheds a new light on the origins of the grapevine powdery mildew pathogen. Molecular Ecology. https://doi.org/10.1111/1462-2920.15401.
DOI: https://doi.org/10.1111/1462-2920.15401

Interpretive Summary: Plant pathogens usually come from regions where hosts and pathogens co-evolve. When pathogens spread globally, their genetic fingerprints may help indicate the pathogen origin. Grape powdery mildew is a destructive fungal disease of domesticated and wild grapevines worldwide. Although Eastern USA is considered the center of origin and diversity of the fungus, previous reports on resistant Asian grapevines suggest Asia as another possible origin of the pathogen. The genetic fingerprint of the fungus in Israel identified three genetic groups: Groups A and B that are common worldwide, and a new group IL, which is genetically unlike any known group in Europe and the US. Group IL was dominant (95%) on wild and traditional vines, increased in abundance along the season, and was more aggressive than A and B. The low genetic diversity within group IL suggests that it invaded Israel from another region. Therefore, we suggest that the Israeli grape powdery mildew was founded by at least two invasions: one from the US via Europe and one from another region, possibly from Asia. This supports the theory of Eurasian co-evolution of powdery mildew in this important grape domestication center.

Technical Abstract: Plant pathogens usually originate and diversify in geographical regions where hosts and pathogens co-evolve. The genetic structure of globally invasive pathogens may help indicate the pathogen origin. Erysiphe necator, the causal agent of grape powdery mildew, is a destructive pathogen of domesticated and wild grapevines worldwide. Although Eastern USA is considered the center of origin and diversity of E. necator, previous reports on resistant native wild and domesticated Asian grapevines suggest Asia as another possible origin of the pathogen. By using multi-locus sequencing, microsatellites and a novel application of amplicon sequencing (AmpSeq), we show that the population of E. necator in Israel is composed of three genetic groups: Groups A and B that are common worldwide, and a new group IL, which is genetically differentiated from any known group in Europe and Eastern US. Group IL showed distinguished ecological characteristics: it was dominant on wild and traditional vines (95%); its abundance increased along the season; and it was more aggressive than A and B isolates on both wild and domesticated vines. The low genetic diversity within group IL suggests that it has invaded Israel from another origin. Therefore, we suggest that the Israeli E. necator population was founded by at least two invasions, of which one could be from a non-East American source, possibly from Asian origin. The discovery of the new genetic group IL provides additional important layer to the theory of a Eurasian co-evolution of E. necator in the grapevine domestication centers.