Population genomics trace clonal diversification and intercontinental migration of an emerging fungal pathogen of boxwood

Authors: Leblanc, Nicholas; CUBETA, MARC - North Carolina State University; Crouch, Jo Anne

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/9/2020
Publication Date: 10/13/2020
Citation: LeBlanc, N.R., Cubeta, M., Crouch, J.A. 2020. Population genomics trace clonal diversification and intercontinental migration of an emerging fungal pathogen of boxwood. Phytopathology. 111:184-193. https://doi.org/10.1094/PHYTO-06-20-0219-FI.
DOI: https://doi.org/10.1094/PHYTO-06-20-0219-FI

Interpretive Summary: Boxwood plants worldwide are threatened by a deadly fungal disease known as boxwood blight. Currently the disease is spreading rapidly across the U.S. and parts of Asia, but has been present in Europe since the late 1990s. Because the boxwood blight pathogens have such similar DNA profiles, standard approaches to track their movement and predict new disease outbreaks are not always effective. Therefore, a new strategy called population genomics was used, with the entire genome of DNA sequenced and analyzed from a large global sample of boxwood blight pathogens. From this new approach, more than 2,000 differences in the pathogen's DNA were discovered, which is a significant increase from previous methods, where less than two dozen DNA differences were known. From these new DNA data, scientists learned that four different genetic groups of the pathogen are present worldwide: two groups with limited geographic distribution and two groups found globally including in the U.S. The two DNA groups found in the U.S. came from different sources: one from Europe and the other from a still unknown source. This research is important because it shows how spread of the blight fungus has occurred and suggests how it will continue to move in the U.S. and globally. This research will be used by plant pathologists, plant breeders, extension personnel and quarantine officials to minimize the spread and impact of boxwood blight.

Technical Abstract: Boxwood blight was first documented in Europe, prior to its recent colonization of North America, where it continues to have significant negative impacts on the ornamental industry. Due to near genetic uniformity in the causal pathogens, understanding of historical disease emergence and ability to predict future outbreaks is limited. The goals of this research were to apply population genomics to understand the role of pathogen diversification and migration in disease emergence. Specifically, we tested if the primary pathogen species has remained genetically isolated from its sister species, while diversifying into clonal lineages that have migrated among continents. SNPs were identified in 67 isolates of the geographically widespread pathogen species Calonectria pseudonaviculata (Cps) from four continents and 13 isolates of the European-limited species C. henricotiae (Che). 1608 SNPs were identified in Cps and 1017 SNPs in Che. Interspecific genetic structure and an absence of shared polymorphisms indicated lack of gene flow between the sister species. Tests for intraspecific genetic structure in Cps identified four genetic clusters, three of which corresponded to monophyletic phylogenetic clades. Comparison of evolutionary divergence scenarios among the four genetic clusters using approximate Bayesian computation indicated the two Cps genetic clusters currently found in the United States were derived from different sources, one from the first genetic cluster found in Europe and the second from an unidentified population. Evidence for multiple introductions of this disease into the US and intercontinental migration indicates future introductions are likely to occur and should be considered in quarantine regulation.