The impatiens downy mildew epidemic in the U.S. is caused by new, introgressed lineages of Plasmopara destructor with prominent genotypic heterogenicity and high evolutionary potential

Authors: Salgado-Salazar, Catalina; CATSTROAGUDIN, VANINA - Oak Ridge Institute For Science And Education (ORISE); Leblanc, Nicholas; DAUGHTREY, MARGERY - Cornell University; HAUSBECK, MARY - Michigan State University; PALMER, CRISTI - Rutgers University; Shishkoff, Nina; Warfield, Colleen; Crouch, Jo Anne

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/23/2022
Publication Date: 6/29/2023
Citation: Salgado-Salazar, C., Catstroagudin, V., Leblanc, N.R., Daughtrey, M., Hausbeck, M., Palmer, C., Shishkoff, N., Warfield, C.Y., Crouch, J. 2023. The impatiens downy mildew epidemic in the U.S. is caused by new, introgressed lineages of Plasmopara destructor with prominent genotypic heterogenicity and high evolutionary potential. Plant Disease. https://doi.org/10.1094/PDIS-08-22-1872-RE.
DOI: https://doi.org/10.1094/PDIS-08-22-1872-RE

Interpretive Summary: Impatiens are a popular annual bedding plant, prized for their brilliant colors and ease of care in the landscape. Downy mildew is a disease that causes impatiens to loose their leaves and die, due to an infection by a plant pathogenic mildew. The disease first showed up in the U.S. in 2004 and has been a problem ever since. The genetic composition of the impatiens pathogen as it caused disease outbreaks across the U.S. is unknown. Therefore, a nationwide collection of more than 600 new samples of the pathogen were fingerprinted using custom DNA markers called SSRs. Seven unique genetic lineages (genotypes) were determined to be responsible for the impatiens downy mildew outbreaks and shared genotypes were found in samples from different countries. This indicates that the pathogen has moved internationally and that the global epidemic may have originated from a common point of origin. It also indicates that the pathogen may be able to overcome host disease resistance and develop tolerance to fungicides. This research is important because it shows how spread of impatiens downy mildew has occurred and suggests how it will continue to move in the U.S. This research will be used by plant pathologists, plant breeders extension personnel and quarantine officials to minimize the transmission and impact of impatiens downy mildew.

Technical Abstract: Impatiens downy mildew (IDM) caused by Plasmopara destructor is the primary constraint on the production and use of impatiens bedding plants (Impatiens walleriana) worldwide. Downy mildew has been documented since the 1880s from wild-grown Impatiens spp., but epidemic outbreaks of the disease affecting the commercially grown, ornamental I. walleriana were only reported for the first time in 2004. Here we assess the genetic diversity, level of differentiation, and population structure from 623 samples associated with current and pre-epidemic IDM outbreaks and genotyped with SSR markers. Plasmopara destructor population structure following the emergence of IDM in the U.S. is subdivided into seven genetic lineages characterized by high genetic heterogeneity, mixed reproduction mode, inbreeding, and excess of heterozygosity. Plasmopara destructor genotypes are significantly differentiated from pre-epidemic IDM samples from hosts other than I. walleriana, but no geographical or temporal subdivision was evident. Plasmopara destructor from different Impatiens species show significant but very low levels of differentiation in the AMOVA test that did not hold in DAPC analyses. The same was observed between samples of P. destructor and P. velutina recovered from I. walleriana. The finding of shared genotypes in samples from different countries and lack of differentiation among U.S. and Costa Rican samples indicate the occurrence of the international movement of the pathogen and a possible common origin of the epidemic. Our study provides the first high-resolution analysis of the diversity of P. destructor populations and the IDM epidemic that may be instrumental for disease management and breeding efforts.