EPPO Datasheet: Phytophthora ramorum
Authority: Werres, De Cock & Man in 't Veld
Taxonomic position: Chromista: Pseudofungi: Oomycetes: Peronosporales: Peronosporaceae
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Notes on taxonomy and nomenclature
Phylogenetically Phytophthora ramorum is placed within the genus in clade 8c and is closely related to Phytophthora lateralis and P. foliorum (Grünwald et al., 2019). The species epithet ‘ramorum’ refers to branch (Latin: ramus) and the pathogenicity of P. ramorum to twigs and branches (Werres et al., 2001).
EU Categorization: Emergency measures, A1 Quarantine pest (Annex II A), PZ Quarantine pest (Annex III)
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EPPO Code: PHYTRA
Phytophthora ramorum has caused severe damage in the 1990s and 2000s, e.g. on oak and tanoak (Quercus spp., Lithocarpus densiflorus) in the USA, on larch (Larix spp.) in the United Kingdom and on ornamental plants in Central Europe. The disease is most commonly known as ‘sudden oak death’ or ‘ramorum blight’ (Rizzo et al., 2002; Grünwald et al., 2008, 2019). The pathogen is generally characterized by a broad host range with more than 170 species currently known to be hosts. These include many important shrubs and trees of ornamental or environmental significance and some herbaceous plants. Camellia, Kalmia latifolia, Larix, Lithocarpus densiflorus, Quercus agrifolia, Pieris, Rhododendron, Syringa vulgaris, Vaccinium and Viburnum are counted among the most important host plants (Garbelotto et al., 2001; Werres et al., 2001; Davidson et al., 2005; EPPO, 2013; Grünwald et al., 2019).Host list: Abies alba, Abies concolor, Abies grandis, Abies magnifica, Abies procera, Acer circinatum, Acer davidii, Acer laevigatum, Acer macrophyllum, Acer pseudoplatanus, Adiantum aleuticum, Adiantum jordanii, Aesculus californica, Aesculus hippocastanum, Alnus cordata, Arbutus menziesii, Arbutus unedo, Arctostaphylos canescens, Arctostaphylos columbiana, Arctostaphylos glauca, Arctostaphylos manzanita, Arctostaphylos sensitiva, Arctostaphylos uva-ursi, Arctostaphylos virgata, Arctostaphylos viridissima, Arctostaphylos, Ardisia japonica, Berberis aquifolium, Betula pendula, Calluna vulgaris, Calycanthus occidentalis, Camellia japonica, Camellia sasanqua, Camellia, Castanea sativa, Castanopsis orthacantha, Ceanothus thyrsiflorus, Cercis chinensis, Chamaecyparis lawsoniana, Chamerion angustifolium, Choisya ternata, Choisya, Chrysolepis chrysophylla, Cinnamomum camphora, Clintonia andrewsiana, Cornus capitata, Cornus hybrids, Cornus kousa, Corylopsis spicata, Corylus cornuta, Cryptomeria, Daphniphyllum glaucescens, Distylium myricoides, Drimys winteri, Dryopteris arguta, Epilobium ciliatum, Eucalyptus haemastoma, Euonymus kiautschovicus, Fagus sylvatica, Frangula californica, Frangula purshiana, Fraxinus excelsior, Fraxinus latifolia, Garrya elliptica, Gaultheria procumbens, Gaultheria shallon, Griselinia littoralis, Hamamelis mollis, Hamamelis virginiana, Hamamelis x intermedia, Heteromeles arbutifolia, Ilex aquifolium, Ilex chinensis, Ilex latifolia, Kalmia angustifolia, Kalmia latifolia, Kalmia, Larix decidua, Larix kaempferi, Laurus nobilis, Leucothoe axillaris, Leucothoe fontanesiana, Lithocarpus glaber, Lonicera hispidula, Loropetalum chinense, Magnolia acuminata, Magnolia cavaleriei, Magnolia delavayi, Magnolia denudata, Magnolia doltsopa, Magnolia figo, Magnolia foveolata, Magnolia grandiflora, Magnolia insignis, Magnolia kobus, Magnolia liliiflora, Magnolia lotungensis, Magnolia maudiae, Magnolia salicifolia, Magnolia stellata, Magnolia wilsonii, Magnolia x loebneri, Magnolia x soulangeana, Magnolia x thompsoniana, Magnolia, Maianthemum racemosum, Nerium oleander, Nothofagus obliqua, Notholithocarpus densiflorus, Osmanthus decorus, Osmanthus delavayi, Osmanthus fragrans, Osmanthus heterophyllus, Osmanthus, Osmorhiza berteroi, Parrotia persica, Photinia x fraseri, Physocarpus opulifolius, Picea sitchensis, Pickeringia montana, Pieris formosa, Pieris hybrids, Pieris japonica, Pieris, Pittosporum undulatum, Prunus laurocerasus, Prunus lusitanica, Pseudotsuga menziesii, Pteris cretica, Pyracantha koidzumii, Quercus acuta, Quercus agrifolia, Quercus cerris, Quercus chrysolepis, Quercus falcata, Quercus ilex, Quercus kelloggii, Quercus parvula var. shrevei, Quercus petraea, Quercus phillyreoides, Quercus robur, Quercus rubra, Quercus, Rhododendron arboreum, Rhododendron catawbiense, Rhododendron macrophyllum, Rhododendron ponticum, Rhododendron yakushimanum, Rhododendron, Ribes laurifolium, Rosa gymnocarpa, Rosa rugosa, Rosa, Rubus spectabilis, Salix caprea, Sarcococca, Schima argentea, Schima wallichii, Sequoia sempervirens, Syringa vulgaris, Taxus baccata, Taxus brevifolia, Taxus x media, Torreya californica, Toxicodendron diversilobum, Trientalis latifolia, Tsuga heterophylla, Umbellularia californica, Vaccinium intermedium, Vaccinium myrtillus, Vaccinium ovatum, Vaccinium vitis-idaea, Vaccinium, Vancouveria planipetala, Viburnum davidii, Viburnum hillieri, Viburnum plicatum var. tomentosum, Viburnum tinus, Viburnum x bodnantense, Viburnum, Viscum
GEOGRAPHICAL DISTRIBUTION 2020-11-18
The diversity of P. ramorum has recently been studied in Vietnam and it was hypothesized that Vietnam could be the centre of origin of this species. The pathogen was also found in Vietnam on Rhododendron, thus suggesting that Rhododendron may be part of its natural host range (Jung et al., 2020). The species was introduced to Europe and North America where it was first discovered in the 1990s (Werres et al., 2001; Rizzo et al., 2002). In particular, oak trees in western North America and larch plantations in the United Kingdom were severely affected in the 1990s and 2000s by the pathogen, while in other areas of North America and Europe mainly ornamental plants were affected (Grünwald et al., 2019). So far, P. ramorum is known to occur in Europe, North America and parts of Asia.
Four clonal lineages have been characterized and named after the continent where they were first found (NA = North America, EU = Europe): NA1, NA2, EU1 and EU2. Only EU1 was found in Europe as well as in North America (Grünwald et al., 2009, 2012, 2019; Van Poucke et al., 2012). The Vietnamese lineage appears to be most closely related to NA2 with only one base pair difference on the genetic marker cox1 (Jung et al., 2020).EPPO Region: Belgium, Croatia, Denmark, Finland, France (mainland), Germany, Greece (mainland), Ireland, Italy (mainland), Lithuania, Luxembourg, Netherlands, Norway, Poland, Portugal (mainland), Serbia, Slovakia, Slovenia, Spain (mainland, Islas Baleares), Switzerland, United Kingdom (Channel Islands, England, Scotland, Wales)
North America: Canada (British Columbia), United States of America (Alabama, Arizona, Arkansas, California, Colorado, Connecticut, Florida, Georgia, Illinois, Indiana, Iowa, Kansas, Louisiana, Maryland, Mississippi, Missouri, Nebraska, New Jersey, New Mexico, New York, North Carolina, Oklahoma, Oregon, Pennsylvania, South Carolina, Tennessee, Texas, Virginia, Washington)
For the dispersal of P. ramorum, the mycelium can form three different types of spores based on a sexual or asexual reproduction.
Sporangia containing flagellated zoospores (asexual reproduction) can be formed on the surfaces of infected leaves or twigs of some hosts. After being released, zoospores can colonize neighbouring plants by swimming through thin water films (e.g. via water splash) towards the plants. It is thought that the zoospores then penetrate the new host to initiate a new infection. When inoculating twigs of Rhododendron with P. ramorum, it has been observed that the first symptoms (twig discoloration) appeared three to seven days after inoculation (Werres et al., 2001). Another mode of dispersal of P. ramorum can take place within the soil (or growing media), leading to root infection that is followed by a colonization of the vascular tissues and spread into the stem (Parke & Lewis, 2007; Grünwald et al., 2008).
In the plant, chlamydospores (asexual reproduction) are often produced to survive adverse conditions, and may also play a special role in the dispersal within the soil (or growing media) (Shikoff, 2007; Tooley et al., 2008).
Sexual reproduction via the production of gametangia has not yet been observed in plants, but only under laboratory conditions on culture media (Garbelotto et al., 2001; Werres et al., 2001, Brasier & Kirk, 2004). The known lineages of P. ramorum belong to different mating types (A1 or A2): NA1 and NA2 belong to mating type A2, EU1 predominantly belongs to mating type A1 and rarely to A2, EU2 belongs to A1 and the Vietnamese lineage comprises both mating types A1 and A2 (Grünwald et al., 2009; Van Poucke et al., 2012; Jung et al., 2020).
DETECTION AND IDENTIFICATION 2020-11-18
Two different disease syndromes can be distinguished, based on a foliar phase or on a bole canker phase: ‘sudden oak death’ and ‘ramorum blight’ (Grünwald et al., 2008), but in general, symptoms are host specific and vary according to the host (Kliejunas, 2010).
‘Sudden oak death’ (including ‘sudden larch death’) is characterized by lethal cankers. The trunk of affected trees shows bleeding cankers or tarry spots, mostly in the lower part, but in some cases up to a height of 20 m. Sometimes sunken or flattened cankers can be observed nearby. After removing the outer bark, mottled areas and necrotic discoloration of the inner bark tissues can be seen, showing similarities with the normal oxidative reddening of phloem tissues. Dark zones are often present at the edges of these necrotic areas. In particular, young or thinner trees show a distinct edge between healthy and necrotic tissues. Vessel blockage caused by P. ramorum often results in a wilt of leaves or needles (without premature leaf fall or needle cast) and eventually in tree mortality (Hansen et al., 2002; EPPO 2006; Parke et al., 2007; Webber et al., 2010).
‘Ramorum blight’ occurs in twigs in the form of brown or black lesions. On Rhododendron, the development of twig lesions begins at the tips and moves towards the base. In addition, cankers can form on shoots or stems, which can lead to a rapid wilting of the leaves, depending on the position of the canker. The wilted leaves remain attached. After removing the bark of a diseased twig, discoloration of the cambial tissue can be seen. The main characteristic leaf symptom is a blackening of the petiole that spreads into the leaf base. Further spread along the midrib can also occur. In other host plant species, not all the above described symptoms may appear. Another manifestation of ‘ramorum blight’ is the development of diffuse brown to dark-brown spots on the leaves. These spots are usually found at the leaf tips, but may appear elsewhere. The whole leaf area may turn brown to black, and leaves may fall prematurely (Werres et al., 2001; Hansen et al., 2002; EPPO 2006).
P. ramorum is a heterothallic species with two mating types. Cultivated individuals can produce gametangia by pairing with opposite Phytophthora mating types of few strains or species, e.g. P. ramorum A1 with P. cryptogea A2.
Oogonia are produced terminally or laterally. They are subglobose and smooth with a size of 24-40 µm (average 29.8-33 µm). Oospores are plerotic and 20-36 µm in size (average 27.2-31.4 µm). Antheridia are amphigynous and mainly rounded to barrel-shaped with a size of 12-22 x 15-18 µm. Two-celled antheridia are very seldom.
Chlamydospores are produced intercalarily or terminally, occasionally laterally. They are globose and thin-walled with a size of 20-91 µm (average 46.4-60.1 µm).
Sporangia are ellipsoid, spindle-shaped or elongated-ovoid with a length x width range of 25-97 x 14-34 µm and an average (length x width) of 45.6-65 x 21.2-28.3 µm. The average length: width ratio is 1.8-2.4. Generally, they have a rounded base; a tapered base is seldom. The caducous sporangia retain a short pedicel, or none, and are semipapillate with one narrow papilla.
Isolates of P. ramorum grow between 2 and 30 °C. The optimal temperature is 20 °C for most isolates, but in exceptional cases, it can vary between 17 and 25 °C. Isolates grow 2.5-3.5 mm in 24 h at the optimal temperature (Werres et al., 2001).
Detection and inspection methods
The presence of P. ramorum can be detected in different types of samples, e.g. plant material, water, soil or growing media. Visual inspections alone are not sufficient, because symptoms can vary between different plant species (Kliejunas, 2010), they can be visually undetectable (e.g. root infections), or they can be suppressed by the use of fungicides (EPPO, 2006).
Isolation from water or soil (or growing media) is possible by using a bait test with rhododendron leaves (Themann et al., 2002; Junker et al., 2018).
Isolation from plant material (selected plant parts or leaves previously used in a bait test) is possible after a surface disinfection followed by plating the plant material onto a suitable culture medium.
The identification of the pathogen is possible by using morphological methods combined with growth characteristics on culture media or DNA-based methods.
The typical morphological structures of Phytophthora (e.g. chlamydospores, sporangia, gametangia) in culture and the growth characteristics have to be checked and measured for an identification. An identification key (e.g. Gallegly & Hong, 2008) should be used together with a comparison with the original species description (Werres et al., 2001). A comparison with closely related or similar species (e.g. P. palmivora) needs to be considered (EPPO, 2006).
DNA barcoding is another option for an identification and can serve as support for a morphological identification of P. ramorum (EPPO, 2016). Different DNA-based methods and primer combinations are possible (EPPO, 2006; Hughes et al., 2006; Bilodeau et al., 2007, 2009; Tomlinson et al., 2007; Martin et al., 2009, Vettraino et al., 2010; Martin, 2013, Feau et al., 2019; Wong et al., 2020). The presence of inhibitors in some wood (e.g. larch) can cause difficulties to DNA-based testing (EPPO, 2006).
The EPPO diagnostic protocol for P. ramorum provides further information and recommendations on how to detect and identify the pathogen (EPPO Standard PM 7/66, 2006 – under revision).
PATHWAYS FOR MOVEMENT 2020-11-18
By releasing zoospores, P. ramorum can colonize neighbouring plants via water splash (see Biology), but it can also colonize new hosts over greater distances via wind, rain, rivers or streams (Davidson et al., 2005; Grünwald et al., 2008). Transportation by humans, for example on their shoes or car tyres, is also possible (Davidson et al., 2005; Frankel, 2008; Grünwald et al., 2008). In nurseries, P. ramorum was found in field soil, various substrates, water sediments (e.g. in puddles, sediment runoff, water retention reservoirs), wind carried leaves, plants and plant debris (Junker et al., 2016). Nevertheless, an important pathway for the movement of the pathogen is the trade of infected plants or plant parts, especially on its main hosts (Běhalová, 2006; Kliejunas, 2010; Grünwald et al., 2019).
PEST SIGNIFICANCE 2020-11-18
The main economic impacts of the disease affect forests and nurseries.
In the 1990s and 2000s, forests in the United States and the United Kingdom have been severely affected (Rizzo et al., 2002; Brasier & Webber, 2010). Around 2240 km2 were affected in the US and 200 km2 in the United Kingdom with millions of trees being felled (Webber, 2017; Grünwald et al., 2019). The broad host range of the pathogen aggravates the situation, because species of the understory vegetation (e.g. Laurus nobilis) are also hosts of P. ramorum and facilitate its establishment and survival (Grünwald et al., 2019). Due to cascading effects, the ecological impact could be very high if some species are completely removed from ecosystems by P. ramorum. It is considered that P. ramorum has the potential to disrupt native ecosystems, to increase the need for chemical or biological control programs, and to threaten already endangered plant species (Cave et al., 2008).
Nurseries in Europe and North America have also been strongly affected. In most cases, when samples from a nursery test positive for P. ramorum, quarantine measures are implemented and host plants are destroyed. This leads to significant extra costs or a change in the plant production (Grünwald et al., 2019).
Preventive fungicidal treatments can be useful for valuable plants in urban green areas. In a forest environment, the use of fungicides is usually not practical (Kliejunas, 2010). As in other Phytophthora species, metalaxyl, phosetyl-aluminium, copper sulfate or phosphonate are effective against P. ramorum (Garbelotto & Rizzo, 2001; Garbelotto et al., 2002). In particular, phosphonate compounds are helpful in controlling the pathogen. The treatment of a tree prior to infection is significantly more effective than after infection (Garbelotto et al., 2003b). Disinfection of contaminated water is possible with hydrogen peroxide, sodium hypochlorite and copper-based active ingredients (Sansford & Woodhall 2007, Colburn & Jeffers, 2010). Metalaxyl also eliminates the pathogen in the soil (Turner et al., 2006), but some isolates are resistant to it (Wagner et al., 2006, 2008; Turner et al., 2008). Moreover, metam sodium, chloropicrin or iodomethane may also eliminate P. ramorum in soils (Kliejunas, 2010). A number of other substances have also shown positive effects against P. ramorum, these include: chitosan, chloropicrin, dazomet, dichloropropene with chloropicrin, film-forming polymers, iodomethane, metam sodium, phytosterols, strobilurins, surfactants and tannin (Orlikowski, 2004; Yakabe & MacDonald, 2008; Stong et al., 2013; Elliott et al., 2015; Peterson et al., 2019).
Different biocontrol agents have also been tested against P. ramorum. Positive effects have been obtained when using the following bacteria: Bacillus brevis, Bacillus subtilis, Paenibacillus subtimyxa, Pseudomonas fluorescens and Streptomyces lydicus (Cohen et al., 2006; Linderman & Davis 2006, Elliott & Shamoun 2008). Several isolates of Trichoderma can parasitize P. ramorum, and the incorporation of Trichoderma asperellum into potting media has shown promising results (Elliott & Shamoun, 2008; Widmer, 2008, 2014).
Essential oils of Chamaecyparis lawsoniana, C. nootkatensis or Juniperus occidentalis have shown positive effects against P. ramorum under laboratory conditions (Manter et al., 2006), as well as caffeic acid, grapefruit or rice bran extract (Orlikowski, 2004; Widmer, 2008).
Sanitation is necessary to maintain pathogen-free plant material. This includes removing and testing symptomatic stock, sterilizing potting media and disinfecting tools, benches, worker’s gloves, shoes and other equipment (Erwin & Ribeiro, 1996).
Research on resistance to P. ramorum shows some promising results. Various studies are being carried out and concern different plant species or hybrids within the broad host range of the pathogen (e.g. Parke et al., 2002; Garbelotto et al., 2003a; Dodd et al., 2005; De Dobbelaere et al., 2006; Grünwald et al., 2006; Meshriy et al., 2006; Hayden et al., 2010).
In the EPPO region, P. ramorum presents a risk to many different environmental and ornamental shrubs and trees, in numerous habitats such as woodland, heathland, maquis, shrubland, as well as in managed gardens, parks or public greens, and nurseries (Sansford et al., 2008). Camellia, Kalmia latifolia, Larix, Lithocarpus densiflorus, Quercus agrifolia, Pieris, Rhododendron, Syringa vulgaris, Vaccinium and Viburnum are counted among the most important host plants that are particularly at risk (Garbelotto et al., 2001; Werres et al., 2001; Davidson et al., 2005; EPPO, 2013; Grünwald et al., 2019). The woodlands in North America, where the pathogen is established (i.e. California), have a Mediterranean type of climate similar to some EPPO countries. These countries are also particularly at risk, and include parts of Albania, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, France, Germany, Greece, Ireland, Italy, Montenegro, Netherlands, Portugal, Slovenia, Spain, Turkey and the United Kingdom (Sansford et al., 2008).
PHYTOSANITARY MEASURES 2020-11-18
In order to prevent entry or spread of P. ramorum, introduced plants should originate from a pest-free area or the areas must be found free from the pathogen after inspections, at least twice during the growing season at an appropriate time. Introduced host plants must comply with the relevant legislation and certification, such as requirements for phytosanitary certificates, a plant passport in EU countries or a scientific license if a phytosanitary certificate cannot be issued. For plants and plant products moving in trade of Betula, Coniferae, Castanea, Fagus and Quercus, guidance can be found in the EPPO Standards on commodity-specific phytosanitary measures (EPPO, 2017abc, 2018ab).
To guarantee the absence of symptoms, plants from nurseries should be inspected at appropriate times. For some host genera (Abies, Pseudotsuga), the import of plants for planting from countries outside the EPPO region is usually prohibited; for other host genera (Castanea, Photinia, Prunus, Rosa, Quercus) imports may only be allowed for plants that are in a dormant and/or leaf-less state. For imports of plants for planting from the USA, it is usually required that all deciduous trees and shrubs have to be dormant or free from leaves, except seeds and tissue cultures. Additional phytosanitary measures are required if the place of plant production is in the buffer zone of sporulating hosts. The buffer zone has a 10 m radius around host shrubs and 100 m around host trees (EPPO, 2013).
Countries should also apply appropriate measures if P. ramorum is detected in areas other than places of production, e.g. parks, gardens, forests. Eradication of the pathogen should be attempted, but if this is not possible, at least measures should be taken to contain the pest, by removing as much infected plant material as possible to reduce the pressure of infection. In each situation, the following elements of risk should be taken into account: scale of the outbreak, risk of further spread, conservation value of the habitat, heritage value in the case of parks or gardens and the local situation (e.g. topography, gradient). It is recommended to apply the following measures, depending on the decision for eradication or containment: (1) Prohibition of movement of susceptible plants, plant parts (including trees) and soil/growing media; (2) Phytosanitary measures to prevent spread of the pest; (3) Control measures; (4) Surveillance. The phytosanitary measures include the removing of plant debris, disposing of susceptible plants or plant material by burning or deep burying them, repairing and maintaining footpaths, restricting access to contaminated areas, hygienic measures such as cleaning and disinfecting shoes or machines, keeping dogs on short leashes and erecting of signs to inform the public about the measures mentioned (EPPO, 2013).
Běhalová M (2006) Surveys for Phytophthora ramorum in the Czech Republic. EPPO Bulletin 36(2), 393-395.
Bilodeau GJ, Lévesque CA, de Cock AWAM, Duchaine C, Brière S, Uribe P, Martin FN & Hamelin RC (2007) Molecular detection of Phytophthora ramorum by real-time polymerase chain reaction using TaqMan, SYBR Green, and molecular beacons. Phytopathology 97(5), 632-642.
Bilodeau G, Pelletier G, Pelletier F, Hamelin RC & Lévesque CA (2009) Multiplex real-time polymerase chain reaction (PCR) for detection of Phytophthora ramorum, the causal agent of sudden oak death. Canadian Journal of Plant Pathology 31(2), 195-210.
Brasier C & Kirk S (2004) Production of gametangia by Phytophthora ramorum in vitro. Mycological Research 108, 823-827.
Brasier C & Webber J (2010) Sudden larch death: plant pathology. Nature 466(7308), 824-825.
Cave GL, Randall-Schadel B & Redlin SC (2008) Risk analysis for Phytophthora ramorum Werres, de Cock & Man in’t Veld, causal agent of sudden oak death, ramorum leaf blight, and ramorum dieback. US Department of Agriculture, Animal and Plant Health Inspection Service, Raleigh, NC.
Cohen M, Condenso E, Anacker B, Rank N & Mazzola M (2006) Biologically based means for control of oomycete phytopathogens. 6th California oak symposium: today’s challenges, tomorrow’s opportunities, Berkeley, University of California. https://www.fs.fed.us/psw/publications/documents/psw_gtr217 (last accessed 31/Jul/2020).
Colburn GC & Jeffers SN (2010) Efficacy of commercial algaecides to manage species of Phytophthora in suburban waterways. In: Frankel SJ, Kliejunas JT & Palmieri KM (2010) Proceedings of the Sudden Oak Death Fourth Science Symposium. General Technical Report PSW-GTR-229, US Department of Agriculture, Forest Service, Pacific Southwest Research Station 229: 223-224.
Davidson JM, Wickland AC, Patterson HA, Falk KR & Rizzo DM (2005) Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95, 587-596.
De Dobbelaere I, Heungens K & Maeas M (2006) Susceptibility levels of Rhododendron species and hybrids to Phytophthora ramorum. In: The Proceedings of the Sudden Oak Death Second Science Symposium, USDA, 79-81.
Dodd RS, Hüberli D, Douhovnikoff V, Harnik TY, Afzal-Rafii Z & Garbelotto M (2005) Is variation in susceptibility to Phytophthora ramorum correlated with population genetic structure in coast live oak (Quercus agrifolia)? New Phytologist 165, 203-214.
Elliott M & Shamoun S (2008) In vitro testing of biological control agents on A1 and A2 isolates of Phytophthora ramorum. In: Frankel SJ, Kliejunas JT & Palmieri KM (2008) Proceedings of the Sudden Oak Death Third Science Symposium, General Technical Report PSW-GTR-214. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 214, 351-354.
Elliott M, Shamoun SF & Sumampong G (2015) Effects of systematic and contact fungicides on life stages and symptom expression of Phytophthora ramorum in vitro and in planta. Crop Protection 67, 136-144.
EPPO (2006) EPPO Standards PM 7/66 Diagnostics. Phytophthora ramorum. EPPO Bulletin 36, 145-155.
EPPO (2013) Pest risk management for Phytophthora kernoviae and Phytophthora ramorum. EPPO, Paris. https://gd.eppo.int/taxon/PHYTRA/documents (last accessed 07/Aug/2020).
EPPO (2016) EPPO Standards. Diagnostics. PM 7/ 129 DNA barcoding as an identification tool for a number of regulated pests. EPPO Bulletin 46(3), 501-537.
EPPO (2017a) EPPO Standards PM 8/4. Commodity-specific phytosanitary measures. Betula. EPPO Bulletin 47(3), 461-469.
EPPO (2017b) EPPO Standards PM 8/4. Commodity-specific phytosanitary measures. Castanea. EPPO Bulletin 47(3), 445-451.
EPPO (2017c) EPPO Standards PM 8/4. Commodity-specific phytosanitary measures. Quercus. EPPO Bulletin 47(3), 452-460.
EPPO (2018a) EPPO Standards PM 8/2. Commodity-specific phytosanitary measures. Coniferae. EPPO Bulletin 48(3), 463-494.
EPPO (2018b) EPPO Standards PM 8/2. Commodity-specific phytosanitary measures. Fagus. EPPO Bulletin 48(3), 495-500.
Erwin DC & Ribeiro OK (1996) Phytophthora diseases worldwide. APS Press, The American Phytopathological Society, St. Paul, MN.
Feau N, Ojeda DI, Beauseigle S, Bilodeau GJ, Brar A, Cervantes-Arango S, Dale AL, Dhillon B, Hammett C, Herath P, Shamoun SF, Tsui CKM, Tanguay P & Hamelin RC (2019) Improved detection and identification of the sudden oak death pathogen Phytophthora ramorum and the Port Orford cedar root pathogen Phytophthora lateralis. Plant Pathology 68(5), 878-888.
Frankel SJ (2008) Sudden oak death and Phytophthora ramorum in the USA: a management challenge. Plant Pathology 37, 19-25.
Gallegly ME & Hong C (2008) Phytophthora: Identifying species by morphology and DNA fingerprints. American Phytopathological Society (APS Press).
Garbelotto M, Davidson JM, Ivors K, Maloney PE, Hüberli D & Rizzo DM (2003a) Non-oak native plants are the main hosts for the sudden oak death pathogen in California. California Agriculture 57(1), 18-23.
Garbelotto M & Rizzo DM (2001) Preliminary studies on chemical and cultural control of Phytophthora associated with sudden oak death. Phytopathology 91(S30),
Garbelotto M, Rizzo DM & Marais L (2002) Phytophthora ramorum and sudden oak death in California: IV: Preliminary studies on chemical control. In: Standiford RB et al. (2002) Proceedings of the Fifth Symposium on Oak Woodlands: Oaks in California’s Challenging Landscape, General Technical Report PSW-GTR-184. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 184, 811-818.
Garbelotto M, Schmidt DJ, Tjosvold S & Harnik TY (2003b) Chemical treatment strategies for control sudden oak death in oaks and tanoaks. Phytopathology 93, S28.
Garbelotto M, Svihra P & Rizzo D (2001) New pests and diseases: sudden oak death syndrome fells 3 oak species. California Agriculture 55(1), 9-19.
Grünwald NJ, Davis EA & Linderman RG (2006) Variation in phenotype for resistance to Phytophthora ramorum, in a range of species and cultivars of the genus Viburnum. In: Sudden Oak Death Second Science Symposium: The State of our Knowledge. US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 83-85.
Grünwald NJ, Goss EM, Ivors K, Garbelotto M, Martin FN, Prospero S, Hansen E, Bonants PJM, Hamelin RC, Chastagner G, Werres S, Rizzo DM, Abad G, Beales P, Bilodeau GJ, Blomquist CL, Brasier C, Brière SC, Chandelier A, Davidson JM, Denman S, Elliott M, Frankel SJ, Goheen EM, de Gruyter H, Heungens K, James D, Kanaskie A, McWilliams MG, Man in’t Veld W, Moralejo E, Osterbauer NK, Palm ME, Parke JL, Perez Sierra AM, Shamoun SF, Shishkoff N, Tooley PW, Vettraino AM, Webber J & Widmer TL (2009) Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen Emergence of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology 99(7), 792-795.
Grünwald NJ, Goss EM & Press CM (2008) Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Molecular Plant Pathology 9(6), 729-740.
Grünwald NJ, LeBoldus JM & Hamelin RC (2019) Ecology and evolution of the sudden oak death pathogen Phytophthora ramorum. Annual Review of Phytopathology 57, 301-321.
Hansen E, Sutton W, Parke J & Linderman R (2002) Phytophthora ramorum and Oregon forest trees – one pathogen, three diseases. In: Sudden Oak Death Science Symposium, University of California, Monterey, USA, 78.
Hayden KJ, Lundquist A, Schmidt DJ, Sniezko RA, Frankel S & Garbelotto M (2010) Tanoak resistance: Can it be used to sustain populations? In: Frankel SJ, Kliejunas JT & Palmieri KM (2010) Proceedings of the Sudden Oak Death Fourth Science Symposium, General Technical Report PSW-GTR-229. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 229, 183-188.
Hughes KJ, Tomlinson JA. Griffin RL, Boonham N, Inman AJ & Lane CR (2006) Development of a one-step real-time polymerase chain reaction assay for diagnosis of Phytophthora ramorum. Phytopathology 96(9), 975-981.
Jung T, Scanu B, Brasier CM, Webber J, Milenković I, Corcobado T, Tomšovský M, Pánek M, Bakonyi J, Maia C, Bačová A, Raco M, Rees H, Pérez-Sierra A & Jung MH (2020) A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests 11, 93.
Junker C, Goff P, Wagner S & Werres S (2016) Occurrence of Phytophthora species in commercial nursery production. Plant Health Research 17(2), 64-75.
Junker C, Pfaff A & Werres S (2018) Validation of the bait test with rhododendron leaves for Phytophthora ramorum. EPPO Bulletin 48(3), 595-609.
Kliejunas JT (2010) Sudden oak death and Phytophthora ramorum: a summary of the literature. General Technical Report PSW-GTR-234. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 234, 181 pp.
Linderman RG & Davis EA (2006) Evaluation of chemical and biological agents for control of Phytophthora species on intact plants or detached leaves of rhododendron and lilac. In: Proceedings of Sudden Oak Death Second Science Symposium, US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 265-268.
Manter DK, Karchesy JJ & Kelsey RJ (2006) The sporicidal activity of yellow-cedar heartwood, essential oil and wood constituents towards Phytophthora ramorum in culture. Forest Pathology 36, 297-308.
Martin FN (2013) Molecular identification of Phytophthora. In: Lamour K (Ed.) (2013) Phytophthora: A Global Perspective. Vol. 2, CABI.
Martin FN, Coffey MD, Zeller K, Hamelin RC, Tooley P, Garbelotto M, Hughes KJD, Kubisiak T, Bilodeau BJ, Levy L, Blomquist C & Berger PH (2009) Evaluation of molecular markers for Phytophthora ramorum detection and identification: testing for specificity using a standardized library of isolates. Phytopathology 99(4), 390-403.
Meshriy M, Hüberli D, Harnik T, Miles L, Reuther K & Garbelotto M (2006) Variation in susceptibility of Umbellularia californica (bay laurel) to Phytophthora ramorum. In: Proceedings of Sudden Oak Death Second Science Symposium, General Technical Report PSW-GTR-196. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 196, 87-89.
Orlikowski LB (2004) Biological control of Phytophthora ramorum on rhododendron. Communications in Agricultural and Applied Biological Sciences 69, 687-692.
Parke JL & Lewis C (2007) Root and stem infection of Rhododendron from potting medium infested with Phytophthora ramorum. Plant Disease 91,
Parke JL, Linderman RJ & Hansen EM (2002) Susceptibility of Vaccinium to Phytophthora ramorum, cause of sudden oak death. Phytopathology 92, S63.
Parke JL, Oh E, Voelker S, Hansen EM, Buckles G & Lachenbruch B (2007) Phytophthora ramorum colonizes tanoak xylem and is associated with reduced stem water transport. Phytopathology 97(12),
Peterson EK, Larson ER & Parke JL (2019) Film-forming polymers and surfactants reduce infection and sporulation of Phytophthora ramorum on rhododendron. Plant Disease 103(6),
Rizzo DM, Garbelotto M, Davidson JM, Slaughter GW & Koike ST (2002) Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease 86(3), 205-214.
Sansford CE, Inman AJ, Baker R, Frankel S, de Gruyter J, Husson C, Kehlenbeck H, Kessel G, Moralejo E, Steeghs M, Webber J & Werres S (2008) Report on the risk of entry, establishment, spread and socio-economic loss and environmental impact and the appropriate level of management for Phytophthora ramorum for the EU. Deliverable Report 28, EU Sixth Framework Project RAPRA. http://rapra.csl.gov.uk/
Sansford CE & Woodhall JW (2007) Datasheet for Phytophthora ramorum. PPP 11824. Sand Hutton, York: Central Science Laboratory, Department of Environment, Forestry, and Rural Affairs. 43 pp. http://www.suddenoakdeath.org/pdf/pram_PRA_UK.pdf (last accessed 31/Jul/2020).
Shikoff N (2007) Persistence of Phytophthora ramorum in soil mix and roots of nursery ornamentals. Plant Disease 91,
Stong RA, Kolodny E, Kelsey RG, González-Hernández MP, Vivanco JM & Manter DK (2013) Effect of plant sterols tannins on Phytophthora ramorum growth and sporulation. Journal of Chemical Ecology 39(6), 733-743.
Themann K, Werres S, Diener HA & Lüttmann R (2002) Comparison of different methods of detecting Phytophthora spp. in recycling water from nurseries. Journal of Plant Pathology 84, 41-50.
Tomlinson JA, Barker I & Boonham N (2007) Faster, simpler, more-specific methods for improved molecular detection of Phytophthora ramorum in the field. Applied and Environmental Microbiology 73(12),
Tooley PW, Browning M & Berner D (2008) Recovery of Phytophthora ramorum following exposure to temperate extremes. Plant Disease 92, 431-437.
Turner J, Jennings P, McDonough S, Liddell D & Stonehouse J (2006) Chemical control of Phytophthora ramorum causing foliar disease in hardy nursery stock in the United Kingdom. In: Proceedings of the Sudden Oak Death Second Science Symposium, US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 273-274.
Turner J, Jennings P, Werres S & Wagner S (2008) Report on response of isolates of P. ramorum exposed to fungicides commonly used to control Phytophthora disease in nurseries. Deliverable Report 5, Sand Hutton, York, UK, Forest Research, Central Sciences Laboratory. EU Sixth Framework Project, RAPRA.
Van Poucke K, Franceschini S, Webber JF, Vercauteren A, Turner JA, McCracken AR, Heungens K & Brasier CM (2012) Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biology 116(11),
Vettraino AM, Sukno S, Vannini A & Garbelotto M (2010) Diagnostic sensitivity and specificity of different methods used by two laboratories for the detection of Phytophthora ramorum on multiple natural hosts. Plant Pathology 59(2), 289-300.
Wagner S, Kaminski K, Keitz WV & Werres S (2006) Influence of Metalaxyl-M on Phytophthora ramorum. In: Proceedings of the Third International IUFRO Working Party (S07.02.09) Meeting: Progress in Research on Phytophthora Diseases of Forest Trees, Farnham, UK.
Wagner S, Kaminski K & Werres S (2008) Evaluation of fungicides for control of Phytophthora ramorum. In: Frankel SJ, Kliejunas JT & Palmieri KM (2008) Proceedings of the Sudden Oak Death Third Science Symposium, General Technical Report PSW-GTR-214. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 214, 481-482.
Webber JF (2017) Phytophthora ramorum: update on the impact and wider consequences of the epidemic in Britain. In: Proceedings of the Sudden Oak Death Second Science Symposium, General Technical Report PSW-GTR-255. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 255, 4-6.
Webber JF, Mullet M & Brasier CM (2010) Dieback and mortality of plantation Japanese larch (Larix kaempferi) associated with infection by Phytophthora ramorum. New Disease Reports 22, 19.
Werres S, Marwitz R, Man in’t Veld WA, De Cock AWAM, Bonants PJM, De Weerdt M, Themann K, Ilieva E & Baayen RP (2001) Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycological Research 105(10),
Widmer T (2008) Investigating the potential of biological control against Phytophthora ramorum. In: Frankel SJ, Kliejunas JT & Palmieri KM (2008) Proceedings of the Sudden Oak Death Third Science Symposium, General Technical Report PSW-GTR-214. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 214, 491.
Widmer TL (2014) Screening Trichoderma species for biological control activity against Phytophthora ramorum in soil. Biological Control 79, 43-48.
Wong B, Leal I, Feau N, Dale A, Uzunovic A & Hamelin RC (2020) Molecular assays to detect the presence and viability of Phytophthora ramorum and Grosmannia clavigera. PloS one 15(2), e0221742.
Yakabe LE & MacDonald JD (2008) Soil treatments for the elimination of Phytophthora ramorum from nursery beds: current knowledge from the laboratory and the field. In: Frankel SJ, Kliejunas JT & Palmieri KM (2008) Proceedings of the Sudden Oak Death Third Science Symposium, General Technical Report PSW-GTR-214. US Department of Agriculture, Forest Service, Pacific Southwest Research Station 214, 113-114.
This datasheet was prepared in 2020 by Janett Riebesehl (Julius Kühn Institute, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Braunschweig, Germany). Her valuable contribution is gratefully acknowledged.
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Datasheet history 2020-11-18
This datasheet was first published online in 2020. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.