Optimal strategies to protect a sub-population at risk due to an established epidemic

Epidemics can particularly threaten certain sub-populations. For example, for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the elderly are often preferentially protected. For diseases of plants and animals, certain sub-populations can drive mitigation because they are intrinsically more valuable for ecological, economic, socio-cultural or political reasons. Here, we use optimal control theory to identify strategies to optimally protect a ‘high-value’ sub-population when there is a limited budget and epidemiological uncertainty. We use protection of the Redwood National Park in California in the face of the large ongoing state-wide epidemic of sudden oak death (caused by Phytophthora ramorum ) as a case study. We concentrate on whether control should be focused entirely within the National Park itself, or whether treatment of the growing epidemic in the surrounding ‘buffer region’ can instead be more profitable. We find that, depending on rates of infection and the size of the ongoing epidemic, focusing control on the high-value region is often optimal. However, priority should sometimes switch from the buffer region to the high-value region only as the local outbreak grows. We characterize how the timing of any switch depends on epidemiological and logistic parameters, and test robustness to systematic misspecification of these factors due to imperfect prior knowledge.

Transmission of the Invasive Pathogen Phytophthora ramorum from Symptomatic to Healthy Host Plants During a Five-Year Period in California

Reliable data on the transmission of airborne plant pathogens are crucial for the development of epidemiological models and implementation of management strategies. The short-distance vertical transmission of the forest pathogen Phytophthora ramorum from a symptomatic California bay laurel (Umbellularia californica) to healthy containerized rhododendrons (Rhododendron caucasicum × R. ponticum var. album) was monitored for five winters (2016/17 to 2020/21) in a field experiment in Northern California. Transmission events were observed during four winters at a frequency of 1 to 17 per season, but not during the extremely dry winter of 2020/21, and were positively correlated to total rainfall rates. The first leaf symptoms were detected around mid-December and reached the highest numbers in January of most years. Only limited symptom development was observed in the spring, with the last detections in May. The exposure time (the time between the first rainfall after placing a bait plant under the bay laurel and development of symptoms) varied between 3 and over 150 days, with an average between 14 and 21 days. P. ramorum was detected from water samples collected from the canopy of the symptomatic California bay laurel. No horizontal pathogen spread was detected from symptomatic to healthy rhododendrons placed at a distance of 2 to 6 m.

Genomic Biosurveillance Detects A Sexual Hybrid in the Sudden Oak Death Pathogen

Invasive exotic pathogens pose a threat to trees and forest ecosystems worldwide1, hampering the provision of essential ecosystem services such as carbon sequestration and water purification2. Hybridization is a major evolutionary force that can drive the emergence of pathogens3. Phytophthora ramorum, an emergent pathogen that causes the sudden oak and larch death, spreads as reproductively isolated divergent clonal lineages. Sexual recombination has never been reported in this pathogen under natural conditions and laboratory crosses have yielded unfit progenies, suggesting postzygotic barriers to hybridization. Here we report the discovery in a plant nursery of novel variants of P. ramorum that are the result of homoploid hybridization via sexual recombination between North American and European lineages of the pathogen. We show that these hybrids are viable, can infect plants and produce spores for long-term survival and propagation. Genome sequencing revealed novel genotypic combinations, not present in the parental lineages, at 54,515 single nucleotide polymorphism loci. More than 6000 of the novel genotypes at these loci are predicted to have a functional impact in genes associated with host infection, including effectors, carbohydrate-active enzymes and proteases. We also observed post-meiotic mitotic recombination that could generate additional genotypic and phenotypic variation and contribute to homoploid hybrid speciation. Our study highlights the importance of plant pathogen biosurveillance to detect novel variants and inform management and control.

Risk of epidemic development in nurseries from soil inoculum of Phytophthora ramorum

Soilborne inoculum arising from buried, infested leaf debris may contribute to the persistence of Phytophthora ramorum at recurrently positive nurseries. To initiate new epidemics, inoculum must not only survive, but produce sporangia during times conducive to infection at the soil surface. To assess this risk, we performed two year-long experiments in a soil plot at the National Ornamentals Research Site at Dominican University of California. Inoculated rhododendron leaf disks were buried at a depth of 5 or 15 cm in the early summer of 2014 or 2015. Inoculum was baited at the soil surface with non-infested leaf disks (2014 only), then retrieved to assess pathogen viability and sporulation capacity every five weeks. Two 14-week-long trials were conducted in 2016. We were able to consistently culture P. ramorum over all time periods. Soil incubation rapidly reduced the capacity of inoculum to sporulate, especially at 5 cm; however, sporulation capacity increased with the onset of seasonally cooler temperatures. P. ramorum was baited most frequently between November and January, especially from inoculum buried at 5 cm 1-day before the baiting period; in January we also baited P. ramorum from inoculum buried at 15 cm the previous June. We validate prior observations that P. ramorum poses a greater risk after exposure to cooler temperatures and provide evidence that infested leaf debris plays a role in the perpetuation of P. ramorum in nurseries. This work provides novel insights into the survival and epidemic behavior of P. ramorum in nursery soils.

Optimal strategies to protect a sub-population at risk due to an established epidemic

Epidemics can particularly threaten certain sub-populations. For example, for SARS-CoV-2, the elderly are often preferentially protected. For diseases of plants and animals, certain sub-populations can drive mitigation because they are intrinsically more valuable for ecological, economic, socio-cultural or political reasons. Here we use optimal control theory to identify strategies to optimally protect a “high value” sub-population when there is a limited budget and epidemiological uncertainty. We use protection of the Redwood National Park in California in the face of the large ongoing state-wide epidemic of sudden oak death (caused by Phytophthora ramorum) as a case study. We concentrate on whether control should be focused entirely within the National Park itself, or whether treatment of the growing epidemic in the surrounding “buffer region” can instead be more profitable. We find that, depending on rates of infection and the size of the ongoing epidemic, focusing control on the high value region is often optimal. However, priority should sometimes switch from the buffer region to the high value region only as the local outbreak grows. We characterise how the timing of any switch depends on epidemiological and logistic parameters, and test robustness to systematic misspecification of these factors due to imperfect prior knowledge.

Three new hosts for Phytophthora ramorum confirmed in Washington State: Salal, Oregon grape, and red huckleberry

Salal (Gaultheria shallon), Oregon grape (Berberis aquifolium), and red huckleberry (Vaccinium parvifolium) are common shrubs in the understory of northwestern forests and are ecologically, culturally and economically important to the region. They are also sold in nurseries for use in ornamental landscapes and ecological restoration. These plant species were symptomatic for Phytophthora in nursery surveys in Washington State between 2011-2015. Symptoms observed on these three hosts resembled those of foliar Phytophthora infection on other woody broadleaf plants. The nursery plants were positive for P. ramorum and Koch’s postulates were completed on potted plants of the three host species, illustrating their potential as a pathway of spread from nurseries to wildlands. We recommend these three hosts be added to the USDA-APHIS regulated host list, which will aid in the effort to prevent movement of P. ramorum into new areas.

High quality, phased genomes of Phytophthora ramorum clonal lineages NA1 and EU1

Phytophthora ramorum is the causal agent of sudden oak death in West Coast forests and currently two clonal lineages, NA1 and EU1, cause epidemics in Oregon forests. Here, we report on two high-quality genomes of individuals belonging to the NA1 and EU1 clonal lineages respectively, using PacBio long-read sequencing. The NA1 strain Pr102, originally isolated from coast live oak in California, is the current reference genome and was previously sequenced independently using either Sanger (P. ramorum v1) or PacBio (P. ramorum v2) technology. The EU1 strain PR-15-019 was obtained from tanoak in Oregon. These new genomes have a total size of 57.5 Mb, with a contig N50 length of ~3.5-3.6 Mb and encode ~15,300 predicted protein-coding genes. Genomes were assembled into 27 and 28 scaffolds with 95% BUSCO scores and are considerably improved relative to the current JGI reference genome with 2,575 or the PacBio genomes with 1,512 scaffolds. These high-quality genomes provide a valuable resource for studying the genetics, evolution, and adaptation of these two clonal lineages.

Phytophthora ramorum (Sudden Oak Death (SOD)).

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.

Two new Nothophytophthora species from streams in Ireland and Northern Ireland: Nothophytophthora irlandica and N. lirii sp. nov.

Slow growing oomycete isolates with morphological resemblance to Phytophthora were obtained from forest streams during routine monitoring for the EU quarantine forest pathogen Phytophthora ramorum in Ireland and Northern Ireland. Internal Transcribed Spacer (ITS) sequence analysis indicated that they belonged to two previously unknown species of Nothophytophthora, a recently erected sister genus of Phytophthora. Morphological and temperature-growth studies were carried out to characterise both new species. In addition, Bayesian and Maximum-Likelihood analyses of nuclear 5-loci and mitochondrial 3-loci datasets were performed to resolve the phylogenetic positions of the two new species. Both species were sterile, formed chlamydospores and partially caducous nonpapillate sporangia, and showed slower growth than any of the six known Nothophytophthora species. In all phylogenetic analyses both species formed distinct, strongly supported clades, closely related to N. chlamydospora and N. valdiviana from Chile. Based on their unique combination of morphological and physiological characters and their distinct phylogenetic positions the two new species are described as Nothophytophthora irlandica sp. nov. and N. lirii sp. nov. Their potential lifestyle and geographic origin are discussed.