A global genetic analysis of herbarium specimens reveals the invasion dynamics of an introduced plant pathogen

Highlights

• We observed a powdery mildew epidemic on Acer macrophyllum in Seattle WA.

• We subsequently identified the powdery mildew species as Sawadaea bicornis.

• Acer macrophyllum is significantly more susceptible to S. bicornis than nine other Acer species tested.

• We identified 7 S. bicornis haplotypes from sequence data acquired from fresh and herbarium specimens collected throughout the world.

• Based on multiple lines of evidence we contend that this pathogen has a European origin.

Abstract

The introduction, spread, and impact of fungal plant pathogens is a critical concern in ecological systems. In this study, we were motivated by the rather sudden appearance of Acer macrophyllum heavily infected with powdery mildew. We used morphological and genetic analyses to confirm the pathogen causing the epidemic was Sawadaea bicornis. In subsequent field studies, this pathogen was found in several locations in western North America, and in greenhouse studies, A. macrophyllum was found to be significantly more susceptible to S. bicornis than nine other Acer species tested. A genetic analysis of 178 specimens of powdery mildew from freshly collected and old herbarium specimens from 15 countries revealed seven different haplotypes. The high diversity of haplotypes found in Europe coupled with sequence results from a specimen from 1864 provides evidence that S. bicornis has a European origin. Furthermore, sequence data from a specimen from 1938 in Canada show that the pathogen has been present in North America for at least 82 years revealing a considerable lag time between the introduction and current epidemic. This study used old herbarium specimens to genetically hypothesize the origin, the native host, and the invasion time of a detrimental fungal plant pathogen.

Introduction

Invasive plant pathogens can cause substantial damage to ecosystems throughout the world (Mack, 2000; Ellison et al., 2005; Loo, 2008; Stajich et al., 2009). Due to increases in global trade, and in particular, the importation of plants, many detrimental plant pathogens have been introduced relatively recently (Brasier, 1990; Gómez-Alpizar et al., 2007; Rellou, 2018). For example, during the 1900s, the causative agents of Dutch elm disease (Ophiostoma ulmi) (Brasier, 1990), chestnut blight (Cryphonectria parasitica) (Rellou, 2018), and white pine blister rust (Cronartium ribicola) (Maloy, 1997) were introduced to North America where they have caused major declines in their host trees and in the case of American chestnut, functional extinction (Anagnostakis, 1987). The introduction of non-native fungal pathogens can be particularly difficult to manage due to their small size and ability to arrive without detection on asymptomatic host plants (Migliorini et al., 2015; Burgess et al., 2016).

Fungi, as model organisms to study biological invasions, have often been overlooked due to their inconspicuous nature and the difficulty in identifying them to the species level. The widespread nature of fungi and their fast rate of evolution also makes them valuable study organisms for elucidating ecological and evolutionary processes involved in pathogen success in new environments (Gladieux et al., 2014; Burgess et al., 2016). Herbarium specimens of fungal plant pathogens can provide unique insights into the evolutionary history of pathogen-host interactions (Ristaino et al., 2001; Yoshida et al., 2014; Miller et al., 2016; Ristaino, 2020). For example, the evaluation of herbarium specimens of the Oomycete pathogen Phytophthora infestans lead to the discovery that the genotype present now is distinct from the genotype that caused the Irish potato famine (Martin et al., 2013, Martin et al., 2013; Yoshida et al., 2013). Among fungal pathogens, powdery mildew is an ideal model system to study invasions due to its cosmopolitan distribution (Braun and Cook, 2012), high rate of evolution (Glawe, 2008), and rapid adaptation to plant hosts (Brown and Rant, 2013).

Powdery mildews are known to infect >10,000 flowering plant species worldwide (Amano, 1986), with an estimated 873 described species (Braun and Cook, 2012). Symptoms of powdery mildew first appear on its host plants as white powdery spots that can spread over large areas of the plant, decreasing growth, and reducing flower and fruit quantity (Daughtrey and Benson, 2005). Powdery mildew conidia, an asexual spore stage, can aerially disperse and greatly facilitate its spread, resulting in severe epidemics over a relatively short time period (Ale-Agha et al., 2000, 2004; Brown et al., 1991; Kiss, 2005).

In recent years, tree mortality in western North America has increased at a higher rate than what is thought to be expected under historical conditions (van Mantgem et al., 2009; Cohen et al., 2016). In some tree species, fungal plant pathogens have been shown to contribute to mortality (Farr et al., 2005; Stone et al., 2008). In 2018, severe powdery mildew infections were observed on bigleaf maple, Acer macrophyllum, in and around the University of Washington campus in Seattle, Washington, USA (Fig. 1A); A. macrophyllum has been reported to be in decline in western North America (Washington Department of Natural Resources, 2016; Betzen, 2018, Oregon State University Extension, 2019). We were motivated by this observation, and the possibility that this fungal pathogen might be detrimentally affecting A. macrophyllum. We thus sought to (1) identify the powdery mildew species infecting A. macrophyllum from samples collected from the University of Washington campus, (2) evaluate the susceptibility of A. macrophyllum and other Acer species to this powdery mildew species, and (3) conduct a global genetic analysis on old (i.e., >150 years) herbarium and newly collected specimens of powdery mildew on Acer species. The genetic analysis allowed us to identify multiple powdery mildew haplotypes, provided evidence on the likely native range of this powdery mildew species, and provided a means to estimate the timing of its introduction to western Washington.