One Clonal Lineage of Calonectria pseudonaviculata Is Primarily Responsible for the Boxwood Blight Epidemic in the United States

Abstract

Boxwood blight caused by Calonectria pseudonaviculata (Cps) and C. henricotiae (Che) is destroying cultivated and native boxwood worldwide, with profound negative economic impacts on the horticulture industry. First documented in the U.S. in 2011, the disease has now occurred in 28 states. Previous research showed that global Cps populations prior to 2014 had a clonal structure, and only the MAT1-2 idiomorph was observed. In this study, we examined the Cps genetic diversity and population structure in the U.S. after 2014, following the expansion of the disease across the country over the past five years. Two hundred eighteen isolates from 21 states were genotyped by sequencing 11 simple sequence repeat (SSR) loci and by MAT1 idiomorph typing. All isolates presented Cps-specific alleles, indicating that Che is still absent in the U.S. states sampled. The presence of only the MAT1-2 idiomorph and gametic linkage disequilibrium suggests the prevalence of asexual reproduction. The contemporary Cps population is characterized by a clonal structure and composed of 13 multilocus genotypes (SSR-MLGs) unevenly distributed across the U.S. These SSR-MLGs grouped into two clonal lineages (CL). The predominant lineage CL2 (93% of isolates) is the primary contributor to U.S. disease expansion. The contemporary U.S. Cps population is not geographically subdivided and not genetically differentiated from the U.S. population prior to 2014, but is significantly differentiated from the main European population, which is largely composed of CL1. Our findings provide insights into the boxwood blight epidemic that are critical for disease management and breeding of resistant boxwood cultivars.

Potential distribution of invasive boxwood blight pathogen (Calonectria pseudonaviculata) as predicted by process-based and correlative models

“…In developing species distribution models for Cps and evaluating the role of climatic factors in shaping its known range limits, we have provided some of the first insights into the potential invasive distribution and geographic origin of the most widespread and damaging pathogens of boxwood. Understanding where the pathogen could establish is particularly important in light of evidence for intercontinental dispersal and multiple introductions of Cps in the United States, which suggests that introductions of the pathogen are common and will likely continue to occur (Castroagudín et al 2020a, LeBlanc et al 2021. The CLIMEX and ensemble correlative model are consistent in predicting the potential for further spread in Europe (southern and eastern Europe), and in North America (southern, midwestern, and Pacific coast region).…”

“…For example, most of the Buxus species native to tropical America are endemic to single islands in the Caribbean (Köhler and Brückner 1989), 37 of which occur in Cuba alone (Gutiérrez 2014, Köhler 2014. None of the Buxaceae species tested to date are completely immune to boxwood blight infections, although severity of disease varies widely across Buxus species and cultivars (Henricot et al 2008, Shishkoff et al 2015, LaMondia and Shishkoff 2017, and it appears to be low in pachysandra Our global climatic suitability models for Cps provide some of the first insights into the potential geographic origin of the pathogen, which is still unknown (Castroagudín et al 2020a, LeBlanc et al 2021. The CLIMEX and ensemble correlative model both included a large part of southeastern China and Japan in the potential distribution, a finding which supports the hypothesis that the pathogen may have arrived to Europe on boxwood plants from East Asia (Daughtrey 2019).…”

“…A possible origin of Cps from China is consistent with reports that most non-European imports of Buxus species to Europe come from this country (EPPO 2012), and with a leading hypothesis for the likely origin of invasive box tree moth in Europe (Van der Straten and Muus 2010, CABI 2021). Nonetheless, we cannot rule out the possibility that Cps is native to another host center of diversity for Buxus or other Buxaceae species such as in the Caribbean or Madagascar (Castroagudín et al 2020a), particularly given that at least one of the modeling approaches included parts of these regions in the potential distribution.…”

“…Both pathogen species can infect and blight boxwood foliage, resulting in rapid plant death. Calonectria henricotiae is only known to occur in Europe, whereas Cps has a wider distribution that presently spans 24 countries primarily in Europe, Asia, and North America (Gehesquière et al 2016, Daughtrey 2019, Castroagudín et al 2020a, EPPO 2020. Cps typically disperses long distances through human-mediated transport of diseased liners (young plants) and nursery stock (Gehesquière 2014, Daughtrey 2019, often going undetected because plants can be asymptomatic until exposed to weather patterns favoring infection and subsequent symptom development (Gehesquière et al 2013, LeBlanc et al 2018.…”

Metagenomic sequencing for detection and identification of the boxwood blight pathogen Calonectria pseudonaviculata

“…Besides distinguishing between species, metagenomics was shown to almost reach strain/lineage-level precision for plant pathogenic bacteria 23 . Cps has diversified into multiple lineages with several of them being present in the US 43 , 45 . Neither MetaMaps nor Kraken 2 can easily distinguish between lineages since they rely on NCBI taxIDs and only a single taxID is associated with each fungal species.…”