Population diversity and structure of Podosphaera macularis in the Pacific Northwestern U.S. and other populations

Authors: Gent, David - Dave; CLAASSEN, BRIANA - Oregon State University; GADOURY, DAVID - Cornell University; Grunwald, Niklaus - Nik; KNAUS, BRIAN - Oregon State University; RADISEK, SEBASTJAN - Slovenian Institute Of Hop Research And Brewing; WELDON, WILLIAM - Cornell University; WISEMAN, MICHELE - Oregon State University; WOLFENBARGER, SIERRA - Oregon State University

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2020
Publication Date: 4/6/2020
Citation: Gent, D.H., Claassen, B.J., Gadoury, D.M., Grunwald, N.J., Knaus, B.J., Radisek, S., Weldon, W., Wiseman, M.S., Wolfenbarger, S.N. 2020. Population diversity and structure of Podosphaera macularis in the Pacific Northwestern U.S. and other populations. Phytopathology. 110(5):1106-1116. https://doi.org/10.1094/PHYTO-12-19-0448-R.
DOI: https://doi.org/10.1094/PHYTO-12-19-0448-R

Interpretive Summary: Powdery mildew is an important disease of hop in the primary production regions in the Pacific Northwestern U.S. Powdery mildew has been present in this region in the mid-1990s, but the origin of the disease is unknown. We conducted research that characterized the genetic diversity of the powdery mildew organism and variability in traits associated with potential to mate. We found that the fungus likely was introduced into the western U.S. from Europe, and likely spread from the western U.S. to re-emerging production regions in the eastern U.S. The sum of this research points to the need for greater emphasis on sanitation measures during propagation and quarantine policies to limit further spread of novel strains of the pathogen, both between and within production areas nationally and internationally.

Technical Abstract: Powdery mildew of hop was first reported in the Pacific Northwestern U.S. in the mid-1990s. More recently, the disease has reemerged in newly planted hop yards of the eastern U.S., as production has expanded to meet local demand. The spread of strains adapted to extant sources of host resistance, available fungicides, and the MAT1-2 mating type to the western U.S. where this mating type presently is absent all threaten the sustainability of hop production. We sequenced the transcriptome of 104 isolates of P. macularis collected throughout the western U.S., eastern U.S., and Europe to quantify genetic diversity of pathogen populations and elucidate the possible origins of pathogen populations in the western U.S. Discriminant analysis of principal components grouped isolates within 3 to 5 geographic populations, dependent on stringency of grouping criteria. Isolates from the western U.S. were phenotyped and categorized into one of three pathogenic races based on disease symptoms generated on differential cultivars. Western U.S. populations were clonal, irrespective of pathogenic race, and grouped with isolates originating from Europe. Isolates originating from wild hop plants in the eastern U.S. were genetically differentiated from all other populations, whereas isolates from cultivated hop plants in the eastern U.S. mostly grouped with isolates originating from the west, consistent with origins from nursery sources. Mating types of isolates originating from cultivated western and eastern U.S. hop plants were entirely MAT1-1. In contrast, a 1:1 ratio of MAT1-1 and MAT1-2 was observed with isolates sampled from wild plants or Europe. Within the western U.S. a set of highly differentiated loci were identified in P. macularis isolates associated with virulence to the powdery mildew R-gene R6. The weight of genetic and phenotypic evidence suggest a European origin of the P. macularis populations in the western U.S., followed by spread of the pathogen from the western U.S. to re-emergent production regions in the eastern U.S.