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Phytophthora Ramorum Sydney E University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 2014 Phytophthora ramorum Sydney E. Everhart University of Nebraska-Lincoln, [email protected] Javier F. Tabima Oregon State University Niklaus J. Grünwald USDA ARS, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/plantpathpapers Part of the Other Plant Sciences Commons, Plant Biology Commons, and the Plant Pathology Commons Everhart, Sydney E.; Tabima, Javier F.; and Grünwald, Niklaus J., "Phytophthora ramorum" (2014). Papers in Plant Pathology. 371. http://digitalcommons.unl.edu/plantpathpapers/371 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Phytophthora ramorum 8 Sydney E. Everhart, Javier F. Tabima, and Niklaus J. Gru¨nwald nonlethal and show foliar or twig blight, which 8.1 Introduction allow prolific production of aerial sporangia. In contrast, on coast live oak, tanoak, and Japanese 8.1.1 Sudden Oak Death larch (Larix kaempferi), infections can be lethal and Ramorum Blight and include bleeding bole cankers (Fig. 8.1). Sudden oak death has resulted in about 80 % Phytophthora ramorum is a recently emerged mortality of tanoaks in portions of the Los Padres plant pathogen and causal agent of one of the National Forest in California, killing 119,000 most destructive and devastating diseases cur- tanoaks across approximately 3,200 ha (Rizzo rently affecting US horticulture and forests et al. 2005). The high mortality of dominant oak (Rizzo et al. 2002, 2005). This oomycete path- species and foliar blight of understory shrubs has ogen was discovered in Marin County, Califor- permanently altered natural forest ecosystems in nia, in the mid-1990s, causing sudden oak death the western US. Until recently, tree infections in on coast live oak (Quercus agrifolia) and tanoak Europe have been comparatively rare and pri- (Notholithocarpus densiflorus) and simulta- marily affected native beech and non-native oak neously discovered in Europe causing foliar species, however an outbreak in 2009 caused blight on Rhododendron and Viburnum (Rizzo widespread mortality of Japanese larch in plan- et al. 2002; Werres et al. 2001). It is now known tations in SW England. By 2010, an outbreak in to affect more than 100 plant species, including Wales led to approximately half a million trees economically important nursery and forest host felled over 1,300 ha, and by 2013 the most recent species (Frankel 2008; Rizzo et al. 2005; Tooley surveys indicate the outbreak has expanded to an et al. 2004; Tooley and Kyde 2007). additional 1,800 ha of newly infected trees in This pathogen has two distinct disease symp- south Wales (COMTF 2013). tom classes (Grünwald et al. 2008). On some Infested nursery plants offer a very effective plant species, mostly woody ornamentals such as means of dispersing the pathogen. This has hap- Viburnum and Rhododendron, symptoms are pened twice in the United States with shipments of infected camellias from California that resulted in 1.6 million potentially infected plants detected in 175 infested sites in over 20 states (see California S. E. Everhart Á J. F. Tabima Á N. J. Grünwald (&) Department of Botany and Plant Pathology, Oregon Oak Mortality Task Force web site http://www. State University, Corvallis, OR 97331, USA suddenoakdeath.org for current status). State, e-mail: [email protected] national, and international quarantines have been N. J. Grünwald imposed on all host plant species grown in affec- Horticultural Crops Research Laboratory, USDA ted areas, including eradication of affected ARS, Corvallis, OR 97331, USA R. A. Dean et al. (eds.), Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens, 159 DOI: 10.1007/978-3-662-44056-8_8, Ó Springer-Verlag Berlin Heidelberg (outside the USA) 2014 160 S. E. Everhart et al. Fig. 8.1 a Sudden oak death epidemic on tanoak in bleeding cankers produced on tanoak in native forests Marin County, California (courtesy S. Frankel). b Sudden (courtesy S. Everhart) oak death symptoms showing necrosis found beneath nursery stock. Similarly, P. ramorum has been currently recognized Phytophthora species reported in 21 European countries, where emer- commonly known as water molds. Phytophthora gency phytosanitary measures have been imple- species are in the phylum Oomycota, which mented since 2002 for member countries of the includes several notable plant pathogens, such as European Union (Walters et al. 2009). These trade Phytophthora infestans, P. sojae, P. cinnamomi, regulations and phytosanitary measures can P. capsici, and Pythium spp. This group is a directly impact commercial nurseries and retail- member of the Stramenopiles and is most closely ers. For example, horticultural nurseries across related to the golden-brown algae and diatoms. the US have lost millions of dollars from Current phylogenetic analysis of Phytophthora destruction of infected stock and suffer further species based on seven nuclear loci places P. losses from disrupted and lost markets. Further- ramorum in clade 8c (Blair et al. 2008). The other more, combining direct loss of nursery and orna- close relatives of P. ramorum in clade 8c include mental crops, decrease in property values with P. lateralis that causes root rot of Port Orford- dead/dying trees, and the costs of disease tracking cedar (Chamaecyparis lawsoniana), P. hiber- and management, total economic losses are in the nalis that primarily causes citrus brown rot and tens of millions of dollars (Cave et al. 2005; leaf/twig blight, and P. foliorum that causes leaf Frankel 2008). Risk analysis for the US has shown spot of Rhododendron spp. (Fig. 8.2). Although that if the pathogen spreads to forests on the East the origin of P. ramorum is unknown, the dis- Coast as well as into new production systems on covery of P. lateralis in Taiwan suggests that the the West Coast, the economic impact of quaran- origin of this clade may be in Eastern Asia tine regulations on trade in conifer and hardwood (Brasier et al. 2010), but more direct evidence in products, logs, Christmas trees, and tree seedlings support of this hypothesis is needed. will be even greater (Cave et al. 2005; Frankel 2008). Rapid spread of disease since the mid-1990s and simultaneous discovery in Europe 8.1.3 Life Cycle led to intensive research efforts to characterize the pathogen, which resulted in whole-genome In nature, the life cycle of P. ramorum currently sequencing only 3 years after formal description includes only an asexual phase although a sexual of the pathogen in 2001. phase is theoretically possible, where asexual spores include sporangia and chlamydospores and the sexual phase yields oospores. Asexual 8.1.2 Taxonomy sporangia are produced from infected leaf tissue and germinate directly, producing a germ tube Formally described in 2001, P. ramorum is a and appressorium to infect the host tissue, or filamentous, diploid protozoan that is one of 117 indirectly by release of zoospores in the presence 8 Phytophthora ramorum 161 P. syringae recombination has not been detected and labora- P. austrocedrae tory pairings among different mating types only 8d P. obscura leads to occasional formation of gametangia and, where meiosis has occurred, leads to aneuploid P. trifolii progeny of reduced fitness (Boutet et al. 2010, P. medicaginis Vercauteren et al. 2011, Van Poucke et al. 2012). P. sansomea Oospores produced under controlled laboratory 8a P. drechsleri conditions appear aberrant and alleles do not P. erythroseptica segregate in a Mendelian fashion (Boutet et al. P. cryptogea 2010; Brasier and Kirk 2004; Vercauteren et al. P. porri 2011). P. primulae 8b P. brassicae 8.1.4 Genetics P. hibernalis P. lateralis 8c Like many Phytophthora species, P. ramorum is P. ramorum a diploid, clonal organism. There are four P. foliorum genetically and phenotypically distinct clonal lineages of P. ramorum (NA1, NA2, EU1, and 0.02 EU2) that were named after the continent (North America or Europe) where each was first Fig. 8.2 Maximum likelihood phylogeny for Phytoph- detected. Genetic variation that discriminates the thora clade 8 based on ITS sequence (adapted from Grünwald et al. 2012b). Phytophthora ramorum is a four clonal lineages include AFLP, SSR micro- clade 8c taxon with P. lateralis, P. hibernalis, and P. satellites, and SNPs, whereas ITS and isozyme foliorum as sister-taxa profiles are indistinct, consistent with the con- specific nature of the lineages. Phenotypic traits of free water. P. ramorum readily produces thick- associated with fitness, such as growth rate, walled chlamydospores that can serve both as aggressiveness, and colony stability have been primary inoculum and provide a means of sur- shown to vary with respect to lineage, where viving adverse conditions such as drought. When EU1 and NA2 are considered more aggressive favorable conditions return, the chlamydospore than NA1, which also showed uniform and will germinate directly to infect the host or irregular growth types that are also called non- produce sporangia. P. ramorum is readily distin- wild type (nwt) or senescent phenotypes (Braiser guished from other Phytophthora species through et al. 2006; Elliott et al. 2011). its formation of abundant, large chlamydospores In North America, three lineages are present, (Werres et al. 2001). P. ramorum is heterothallic where NA1 genotypes are by far the most fre- (out-crossing) and sexual mating in the labora- quent and diverse in the US (Goss et al. 2009a, tory, thus requires contact between individuals of b; Ivors et al. 2006; Ivors et al. 2004; Masch- compatible mating types, A1 and A2. Based on eretti et al. 2008; Prospero et al. 2007, 2009). In knowledge about other species, we expect that Europe, the pathogen exists as the EU1 clonal pheromones released by the opposite mating type lineage (Ivors et al.
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