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. 2023 Jul 6;21(7):e08071. doi: 10.2903/j.efsa.2023.8071
Taxonomic information

Current valid scientific name: Phytophthora ramorum

Synonyms: –

Name used in the EU legislation: Phytophthora ramorum (non‐EU isolates) Werres, De Cock & Man in 't Veld [PHYTRA]

Order: Peronosporales

Family: Peronosporaceae

Common name: Sudden Oak Death (SOD), ramorum bleeding canker, ramorum blight, ramorum leaf blight, twig and leaf blight

Name used in the Dossier: Phytophthora ramorum

Group Oomycetes
EPPO code PHYTRA
Regulated status

The pathogen is listed in Annex II of Commission Implementing Regulation (EU) 2019/2072 as Phytophthora ramorum (non‐EU isolates) Werres, De Cock & Man in 't Veld [PHYTRA]. The EU isolates of P. ramorum are listed as protected zone quarantine pest.

The pathogen is included in the EPPO A2 list (EPPO, online_a).

Phytophthora ramorum is quarantine in Canada, Israel, Mexico, Morocco and the UK. It is on A1 list of Brazil, Chile, Egypt, Kazakhstan, Türkiye and EAEU (=Eurasian Economic Union: Armenia, Belarus, Kazakhstan, Kyrgyzstan and Russia) (EPPO, online_b).

Pest status in the UK

Phytophthora ramorum is present in the UK (Brown and Brasier, 2007; Dossier Sections 2.0 and 5.0; CABI, online; EPPO, online_c).

According to the Dossier Section 5.0, European isolates of Phytophthora ramorum are present in the UK: not widely distributed and under official control. It has been found in most regions of the UK, but it is more often reported in wetter, western regions.

Pest status in the EU Phytophthora ramorum is present in the EU and it is currently reported in the following EU Member States: Belgium, Croatia, Denmark, Finland, France, Germany, Ireland, the Netherlands, Poland, Portugal and Slovenia (EPPO, online_c).
Host status on Acer

Acer pseudoplatanus is a reported host of Phytophthora ramorum (Brown and Brasier, 2007; King et al., 2015; CABI, online; EPPO, online_d; Farr and Rossman, online).

Phytophthora ramorum is a pathogen of other Acer species such as Acer circinatum, Acer davidii, Acer laevigatum and Acer macrophyllum (Hayden et al., 2004; Cave et al., 2008; DiLeo et al., 2008; King et al., 2015; CABI, online; EPPO, online_d; Farr and Rossman, online).

There is no information on whether Phytophthora ramorum can also attack Acer campestre.

PRA information Pest Risk Assessments available:
  • Risk analysis for Phytophthora ramorum Werres, de Cock & Man in't Veld, causal agent of sudden oak death, ramorum leaf blight and ramorum dieback (Cave et al., 2008);

  • Risk analysis of Phytophthora ramorum, a newly recognised pathogen threat to Europe and the cause of sudden oak death in the USA (Sansford et al., 2009);

  • Scientific opinion on the pest risk analysis on Phytophthora ramorum prepared by the FP6 project RAPRA (EFSA PLH Panel, 2011);

  • Pest risk management for Phytophthora kernoviae and Phytophthora ramorum (EPPO, 2013);

  • UK Risk Register Details for Phytophthora ramorum (DEFRA, online).

Other relevant information for the assessment
Biology

Phytophthora ramorum is most probably native to East Asia (Poimala and Lilja, 2013; Jung et al., 2021). The pathogen is present in Asia (Japan, Vietnam), Europe (Belgium, Croatia, Denmark, Finland, France, Germany, Guernsey, Ireland, Luxembourg, the Netherlands, Norway, Poland, Portugal, Slovenia, the UK), North America (Canada, the US) and South America (Argentina) (EPPO, online_c). So far there are 12 known lineages of P. ramorum: NA1 and NA2 from North American, EU1 from Europe (including the UK) and North America (Grünwald et al., 2009), EU2 from Northern Ireland and western Scotland (Van Poucke et al., 2012), IC1 to IC5 from Vietnam and NP1 to NP3 from Japan (Jung et al., 2021).

Phytophthora ramorum is heterothallic oomycete species belonging to clade 8c (Blair et al., 2008) with two mating types: A1 and A2 (Boutet et al., 2010).

Phytophthora species generally reproduce through a) dormant (resting) spores which can be either sexual (oospores) or asexual (chlamydospores); and b) fruiting structures (sporangia) which contain zoospores (Erwin and Ribeiro, 1996).

Phytophthora ramorum produces sporangia on the surfaces of infected leaves and twigs of host plants. These sporangia can be splash‐dispersed to other close or carried by wind and rain to longer distances. The sporangia germinate to produce zoospores that penetrate and initiate an infection on new hosts. In infected plant material the chlamydospores are produced and can serve as resting structures (Davidson et al., 2005; Grünwald et al., 2008). Trunk cankers (e.g. on Quercus) are not known to support sporulation and therefore do not transmit the pathogen (DEFRA, 2008). The pathogen is also able to survive in soil (Shishkoff, 2007). In the west of Scotland, it persisted in soil for at least 2 years after its hosts were removed (Elliot et al., 2013). Oospores were only observed in pairing tests under controlled laboratory conditions (Brasier and Kirk, 2004). Optimal temperatures under laboratory conditions were 16–26°C for growth, 14–26°C for chlamydospore production and 16–22°C for sporangia production (Englander et al., 2006).

Phytophthora ramorum is mainly a foliar pathogen, however it was also reported to infect shoots, stems and occasionally roots of various host plants (Grünwald et al, 2008, Parke and Lewis, 2007). According to Brown and Brasier (2007), P. ramorum commonly occupies xylem beneath phloem lesions and may spread within xylem and possibly recolonise the phloem from the xylem. Phytophthora ramorum can remain viable within xylem for two or more years after the overlying phloem had been excised.

Phytophthora ramorum can disperse by aerial dissemination, water, movement of infested plant material and soil containing propagules on footwear, tires of trucks and mountain bikes or the feet of animals (Davidson et al., 2002; Brasier, 2008).

Infected foliar hosts can be a major source of inoculum, which can lead to secondary infections on nearby host plants. Important foliar hosts in Europe are Rhododendron spp. and Larix kaempferi (Brasier and Webber, 2010, Grünwald et al., 2008).

Possible pathways of entry for Phytophthora ramorum are plants for planting (excluding seed and fruit) of known susceptible hosts; plants for planting (excluding seed and fruit) of non‐host plant species accompanied by contaminated attached growing media; soil/growing medium (with organic matter) as a commodity; soil as a contaminant; foliage or cut branches; seed and fruits; susceptible (isolated) bark and susceptible wood (EFSA PLH Panel, 2011).

Phytophthora ramorum caused rapid decline of Lithocarpus densiflorus and Quercus agrifolia in forests of California and Oregon (Rizzo et al., 2005) and Larix kaempferi in plantations of southwest England (Brasier and Webber, 2010).

Symptoms Main type of symptoms

Phytophthora ramorum causes different types of symptoms depending on the host species and the plant tissue infected.

According to DEFRA (2008) P. ramorum causes three different types of disease:
  1. ‘Ramorum bleeding canker’ – cankers on trunks of trees, which emit a dark ooze. As they increase in size they can lead to tree death.
  2. ‘Ramorum leaf blight’ – infection of the foliage, leading to discoloured lesions on the leaves.
  3. ‘Ramorum dieback’ – shoot and bud infections which result in wilting, discolouration and dying back of affected parts.

Symptoms on Quercus species are cankers of red, brown or black color on trunk, browning of the crown, gradual leaf loss and death of trees (Davidson et al., 2003).

Leaf lesions and shoot dieback can be observed on foliar hosts such as Rhododendron, Viburnum, Pieris and Camellia. (Davidson et al., 2003, EPPO, online_e). On Larix kaempferi, P. ramorum causes foliage and bark infection that are visible as wilted shoot tips with blackened needles and stem lesions with resin bleeding (Braiser and Webber, 2010).

Symptoms on Lithocarpus densiflorus are lesions on leaves, cankers on trunk, branches and twigs; shoot tip dieback, leaf flagging and formation of a Shepard's crook. The trees can die within 1 year (Davidson et al., 2003).

Acer macrophyllum is affected by discoloration of leaves ranging from orange to brown color, which normally starts from the leaf edges (Davidson et al., 2003).

On Acer pseudoplatanus, P. ramorum has been isolated from bleeding bark lesions (Brown and Brasier, 2007). In an inoculation experiment with P. ramorum, low levels of necrosis on leaves were observed on this host species (Denman et al., 2005).

Presence of asymptomatic plants

If roots are infected by P. ramorum, the plants can be without aboveground symptoms for months until developmental or environmental factors trigger disease expression (Roubtsova and Bostock, 2009; Thompson et al., 2021).

Application of some fungicides may reduce symptoms and therefore mask infection, making it more difficult to determine whether the plant is pathogen‐free (DEFRA, 2008).

Confusion with other pests

Various symptoms caused by P. ramorum can be confused with other pathogens, such as: canker and foliar symptoms caused by other Phytophthora species (P. cinnamomi, P. citricola and P. cactorum); leaf lesions caused by rust in early stages; leafspots caused by sunburn; dieback of twigs and leaves caused by Botryosphaeria dothidea (Davidson et al., 2003).

Symptoms in Acer macrophyllum can be confused with drought stress, Xylella leaf scorch and anthracnose (Davidson et al., 2003).

Phytophthora ramorum can be easily distinguished from other Phytophthora species based on morphology (Grünwald et al., 2008) and molecular tests.

Host plant range

Phytophthora ramorum has a very wide host range, which is expanding.

Main host plants include Camellia spp., Larix decidua, L. kaempferi, Pieris spp., Rhododendron spp., Syringa vulgaris, Viburnum spp. and the North American trees species, Lithocarpus densiflorus and Quercus agrifolia (EPPO online_d).

Further proven hosts confirmed by Koch's postulates are Abies grandis, A. magnifica, Acer circinatum, A. macrophyllum, A. pseudoplatanus, Adiantum aleuticum, A. jordanii, Aesculus californica, A. hippocastanum, Arbutus menziesii, A. unedo, Arctostaphylos columbiana, A. glauca, A. hooveri, A. manzanita, A. montereyensis, A. morroensis, A. pilosula, A. pumila, A. silvicola, A. viridissima, Calluna vulgaris, Castanea sativa, Ceanothus thyrsiflorus, Chamaecyparis lawsoniana, Chrysolepis chrysophylla, Cinnamomum camphora, Corylus cornuta, Fagus sylvatica, Frangula californica, Frangula purshiana, Fraxinus excelsior, Gaultheria procumbens, G. shallon, Griselinia littoralis, Hamamelis virginiana, Heteromeles arbutifolia, Kalmia spp., Larix × eurolepis, Laurus nobilis, Lonicera hispidula, Lophostemon confertus, Loropetalum chinense, Magnolia × loebneri, M. oltsopa, M. stellata, Mahonia aquifolium, Maianthemum racemosum, Parrotia persica, Photinia fraseri, Phoradendron serotinum subsp. macrophyllum, Photinia × fraseri, Prunus laurocerasus, Pseudotsuga menziesii var. menziesii, Quercuscerris, Q. chrysolepis, Q. falcata Q. ilex, Q. kelloggii, Q. parvula var. shrevei, Rosa gymnocarpa, Salix caprea, Sequoia sempervirens, Taxus baccata, Trientalis latifolia, Umbellularia californica, Vaccinium myrtillus, V. ovatum, V. parvifolium and Vinca minor (Cave et al., 2008; APHIS USDA, 2022).

Reported evidence of impact Phytophthora ramorum is an EU quarantine pest.
Evidence that the commodity is a pathway Phytophthora ramorum is continuously intercepted in the EU on different plant species intended for planting (EUROPHYT/TRACES‐NT, online) and according to EFSA PLH Panel (2011), P. ramorum can travel with plants for planting. Therefore, plants for planting are possible pathway of entry for P. ramorum.
Surveillance information

Phytophthora ramorum at growing sites: infested plants are destroyed and potentially infested plants are ‘held’ (prohibited from moving). The UK has a containment policy in the wider environment with official action taken to remove infected trees (Dossier Section 3.0).

As part of an annual survey at ornamental retail and production sites (frequency of visits determined by a decision matrix) Phytophthora ramorum is inspected on common host plants. An additional inspection, during the growing period, is carried out at plant passport production sites. Inspections are carried out at a survey to 300 non‐woodland wider environment sites annually (Dossier Sections 3.0 and 5.0).