Phytophthora ramorum (Sudden Oak Death (SOD)).
Authors: Garbelotto Matteo , Frankel Susan J. 
Published: March 2021

Phytophthora ramorum is considered an invasive species due to its ability to spread, persist, and reproduce in new environments. Its rapid life-cycle, propensity to reproduce asexually and splash dispersal via windblown rain, plus its ability to survive through harsh climatic conditions, are elements favouring this species' potential invasiveness. Spread potential in forests has been elucidated by several studies in California and Oregon employing population genetics approaches. Results have consistently shown that scale of spread of naturalized endemic pathogen populations in natural ecosystems is limited to a few hundred metres and, occasionally, during extremely wet years, spread may reach a few (3-5) km (Mascheretti et al., 2008; Mascheretti et al., 2009; Eyre et al., 2013). Spread events at scales larger than those reported above appear to be associated either with the movement of infected plant parts, normally from large wild infestations, or with the introduction of infected plants, normally from infested ornamental nursery plant stock (Croucher et al., 2013). Spread scales from the hundreds of metres to the few kilometres apply to pathways that involve only foliar hosts, in particular California bay laurels and tanoaks, and are clearly positively correlated with rainfall (Eyre et al., 2013). However, spread from foliar hosts such as California bay laurels, tanoaks and ornamental rhododendrons to stem hosts such as oaks and tanoaks occur at the much lower scale of 10 to 20 metres and are strongly associated with the occurrence of episodic and above average rainy years (Cobb et al., 2012; Garbelotto et al., 2017). Given the limited spatial scale of dispersal of P. ramorum, its spread is strongly driven by structure and composition of individual forest stands and is projected to increase as the density of infectious foliar hosts increases (Cobb et al., 2010; Meentemeyer et al., 2015). Monocultures of Japanese larch in the UK, stands with high proportion of tanoaks in Oregon and California, and oak woodlands with an abundance of California bay laurels have all been the hardest hit systems. Presence of contiguous forests (Condeso and Meentemeyer, 2007), genetics of host populations (Dodd et al., 2005; Hayden et al., 2011), microclimate (Anacker et al., 2008; DiLeo et al., 2014) and climate (Meentemeyer et al., 2004; Venette and Cohen, 2006; Ireland et al., 2013; Meentemeyer et al., 2015) are all know to drive the spread in ecosystems invaded by P. ramorum. In spite of the theoretical tolerance of the pathogen to both high and low temperatures, models validated by extensive field sampling in regions infested by NA1 populations indicate high maximum temperatures strongly limit the spread of the pathogen (Meentemeyer et al., 2015) and may even cause significant reversion from positive to negative infection status in foliar hosts (Lione et al., 2017). High temperatures have also been shown to make water populations of the pathogen not viable (Eyre et al., 2015). In the lab, exposure of Petri dishes to 55°C for 1 hour, to 45°C for 4 hours or to 40°C for 24 hours has blocked pathogen growth (Swain et al., 2006), but survival of the pathogen has been reported up to 1 week at 55°C for infected California bay laurel leaves (Harnik et al., 2004), and in other trials the pathogen has been shown to survive in pant tissue between 40°C (2 days) and -20°C (4 days) (Tooley et al., 2008). Finally, the pathogen's broad host range on popular, nursery grown, ornamental plants, and the non-lethal, nondescript nature of the disease on most of the foliar hosts allows for long-term dispersal. Disease epidemiology in nursery settings has not been extensively studied, however it has been reported that disease cycles are strongly influenced by seasonality and year-to-year climatic variations (Tjosvold et al., 2008). Propagules have been shown to survive in potting mix for over a year but infested mix only caused infection if leaves were in contact with it (Tjosvold et al., 2009), this is in contrast with shorter survival in natural ecosystems (Fichtner et al., 2007; Eyre et al., 2013). Infection does not seem to be strongly associated with irrigation water, but sprinkler irrigation did favour disease development (Tjosvold et al., 2008). Serrano et al. (2020) have provided a first in depth analysis of an outbreak in a mock nursery setting and have identified leaf to leaf, followed by leaf to soil as the two main pathogen dispersal mechanisms in the absence of flooding. In the same study, dispersal from individual infected potted rhododendrons was always less than 2 metres in a single growing season. Anecdotal evidence suggests outbreaks in nursery settings may be associated with flooding of growing beds (see Serrano et al., 2020). Thus, both in natural ecosystems and in nurseries, foliar infections appear to be driving disease outbreaks and the microevolution (i.e. generation of novel genotypes) of the pathogen (Eyre et al., 2013; Serrano et al., 2020). Soil and water are infested but may often be dead ends, epidemiologically speaking, although water populations have been shown to foster microevolution of the pathogen which could lead to the emergence of adaptive traits (Eyre et al., 2015). Genetic analysis shows P. ramorum infection initially reported only in Europe and parts of North America is also present in northern Vietnam, at the border with China (Jung et al., 2020); three clonal lineages were originally identified: EU1 (Europe and North America, nurseries and forests), NA1 (North America, nurseries and forests) and NA2 (North American nurseries) (Ivors et al., 2006). Information to date indicates that divergence of these lineages occurred ages ago, P. ramorum originated from isolated populations and has migrated at least four times to North America and Europe (Grünwald et al., 2011). In 2012, Van Poucke et al. (2012) identified a fourth lineage, named EU2, in the UK, and additional lineages may be present in Vietnam (Jung et al., 2020). Whole genome resequencing has identified genomic differences among the lineages (Dale et al., 2019), but lineages also differ phenotypically from one another both in vitro and in planta, although estimates of their relative invasiveness may often be biased by the choice of hosts tested (Elliott et al., 2011; Eyre et al., 2014; Franceschini et al., 2014; O'Hanlon et al., 2017). One mating type only is found in each of the four widely studied lineages: EU1 and EU2 are A1 and NA1 and NA2 are A2 (Grunwald et al., 2019). Lineages with different mating types are co-mingled in some North American nurseries (Grünwald et al., 2012) and in a few forest stands of southwestern Oregon (Grünwald et al., 2016) raising the issue of potential sexual reproduction between lineages carrying different mating types. In vitro tests have indicated mating is possible (Boutet et al., 2010), however 'hybrid' progeny appears to be unstable possibly due to aberrant aneuploid genome size (Vercauteren et al., 2011). In spite of the clonal nature of populations within lineages, significant intralineage phenotypic variation has been observed; such variation is mostly due to the presence of non-wild types (nwt) that are often less virulent and are caused by genomic alterations, including locus copy number variation and chromosomal rearrangements (Kasuga et al., 2012; Kasuga et al., 2016). The emergence of nwt is strongly associated with host species (stem hosts) or habitat (plants grown in nursery settings) (Elliott et al., 2018) and may be a trait identifying pathogen populations from 'dead end' hosts.