REVIEW ARTICLE Soil- and waterborne species linked to recent outbreaks in Northern California restoration sites A review identifies several Phytophthora species found in California wildlands and discusses approaches for preventing and diagnosing the spread of these plant pathogens.

by Matteo Garbelotto, Susan J. Frankel and Bruno Scanu

istorically, the release of Phytophthora species Abstract in the wild has resulted in massive die-offs of Himportant native plant species, with cascading Many studies around the globe have identified plant production facilities consequences on the health and productivity of affected as major sources of plant pathogens that may be released in the wild, ecosystems (Brasier et al. 2004; Hansen 2000; Jung with significant consequences for the health and integrity of natural 2009; Lowe 2000; Rizzo and Garbelotto 2003; Swiecki ecosystems. Recently, a large number of soilborne and waterborne et al. 2003; Weste and Marks 1987). Once introduced, species belonging to the plant pathogenic genus Phytophthora have plant pathogens in general cannot be eradicated (Cun- been identified for the first time in California native plant production niffe et al. 2016; Garbelotto 2008), and costs associated facilities, including those focused on the production of plant stock used with the spread and control of exotic pathogens and in ecological restoration efforts. Additionally, the same Phytophthora pests have been estimated to surpass $100 billion per species present in production facilities have often been identified in failing year for the United States alone (Pimentel et al. 2005). restoration projects, further endangering plant species already threatened Thus, preventing the introduction of pathogens by us- or endangered. To our knowledge, the identification of Phytophthora ing pathogen-free plant stock is the most cost-effective species in restoration areas and in plant production facilities that produce and responsible approach (Parnell et al. 2017). plant stock for restoration projects is a novel discovery that finds many In their extensive meta-analysis, Santini et al. land managers unprepared, due to a lack of previous experience with (2013) identify the trade of live plants as the main these pathogens. This review summarizes some of the key knowledge pathway for the introduction of invasive forest dis- about the genus Phytophthora in general and lists some of the many eases in Europe. Similarly, Jung et al. (2016) identi- soilborne and waterborne species recently recovered from some California fied plant production facilities as a major source of restoration sites and plant production facilities.

Online: https://doi.org/10.3733/ca.2018a0033

Phytophthora diseases are increasingly being found in California wildlands and parks, where they have caused large die-offs of native plant species. Shown here is Ione manzanita (Arctostaphylos myrtifolia) in Ione, California, killed by P. cinnamomi.

Matteo Garbelotto Matteo 208 CALIFORNIA AGRICULTURE • VOLUME 72, NUMBER 4 Phytophthora inoculum that may be released in the genus Phytophthora is part of the order : wild. The best-known example of a Phytophthora spe- this order contains genera that are notable for having cies released in California natural environments from co-evolved with plant hosts mostly as plant pathogens, commercially produced plants is that of Phytophthora although some are pathogens of animals (Spies et al. ramorum (Grünwald et al. 2012), but an equally im- 2016; Thines 2014). The four best-known genera are portant prior introduction associated with infested Peronospora, Plasmopara, Pythium and Phytophthora. plant nurseries is that of Phytophthora lateralis, which Each has evolved distinct epidemiological strategies. affected Port Orford cedar in California and Oregon While Peronospora and Plasmopara species (causal (Hansen et al. 2000). agents of plant diseases known as “downy mildews”) Recently, Rooney-Latham and colleagues (Rooney- mostly spread aerially, Pythium species are almost ex- Latham and Blomquist 2014; Rooney-Latham et al. clusively soilborne and waterborne. The genus Phytoph- 2015) identified at least two soilborne Phytophthora thora stands between the two, and includes species that species, including one reported for the first time ever are soilborne and waterborne, or airborne, and some in the United States, as the cause of extensive mortality species with a mixed epidemiological strategy (Bourret of two plant species recently employed in an extensive et al. 2018; Oßwald et al. 2014). restoration project. Both species were also found in the Phytophthora propagules responsible for much of production facilities that had supplied the plant stock, the known host-to-host spread are normally ovoid or and both species have been shown, through greenhouse pyriform in shape and are called sporangia (fig. 1A). inoculation studies, to be aggressive pathogens on three Sporangia can be extremely variable in form and size important hosts present in the restoration areas (Sims and are normally produced alone or in clusters at the et al. 2018). This discovery triggered multiple surveys of end of stalks. If sporangia can be easily detached from failed restoration projects and of the facilities that pro- the stalks that bear them, the species may be aerially vided plants employed in such projects (Frankel et al. dispersed rather than just being soilborne and/or wa- 2018). While soilborne and waterborne Phytophthoras terborne (Erwin and Ribeiro 1996). have been found in commercial production of orchard Sporangia of all Phytophthora species, when mature, and landscaping plants, to our knowledge this is the contain a variable number of motile, biflagellate zoo- first reported case of Phytophthora species found in spores (fig. 1B). Sporangia sometimes can germinate plants bound for native landscapes (Frankel et al. directly and infect a plant, or plants can be infected 2018; M. Garbelotto, unpublished results). Although directly by hyphae growing in the soil. However, it is Phytophthora species are known to be plentiful in com- the zoospores that are mostly responsible for infec- mercial plant production facilities, their discovery in tion of plant tissue. Zoospores are normally attracted native plant production facilities is novel, and finds by chemical or electrical signals generated by the many land managers unprepared, due to a lack of pre- plant host (Carlile 1983) and require a film of water to vious experience with these pathogens. “swim” and initiate the infection process. If there is no Given that the research community has been film of water or water dries out, zoospores can encyst focused on aerial Phytophthora species such as P. and become dormant without losing viability. Infection ramorum recently, this review summarizes some basic by zoospores or by germinating sporangia can occur knowledge for soilborne and waterborne Phytophthora through stomatal openings, or an infection peg can species, such as those recently recovered from restora- rupture the plant and directly infect plant tis- tion and disturbed sites in the San Francisco Bay Area sue (Erwin and Ribeiro 1996). The need for a film of in California. Even if we acknowledge that infected water for zoospore-mediated infection to occur largely plants can often be asymptomatic (Bienapfl and Balci explains the direct relationship between increasing dis- 2014; Jung et al. 2016; Migliorini et al. 2015), we hope ease levels and increasing rainfall values. this article may increase the awareness about this Phytophthora species also produce spherical sur- group of pathogens, possibly leading to their early vival structures called (fig. 1C). The detection in plant production facilities (Parke et al. size of chlamydospores, the pattern and the abundance 2014; Patel et al. 2016), before infected plants are out- in which they are produced, and the thickness of their planted in the wild. outer wall can often be diagnostic traits differentiating Phytophthora species. Chlamydospores can survive Introduction to the genus up to several years in adverse environmental condi- Phytophthora tions; they can also contaminate soil and water and be responsible for dispersal of the pathogen. In favorable For decades, Phytophthora species have been errone- conditions, chlamydospores can germinate directly ously lumped with the Fungi, but in order to fully or they can produce a . Like sporangia, understand their biology and ecology it is important chlamydospores are clonally produced and do not to understand their correct taxonomic position. The require mating. genus Phytophthora belongs to the kingdom Stramini- Sexual structures produced by Phytophthora spe- pila (formerly Chromista), which also includes aquatic cies after mating are called oospores and are produced organisms such as diatoms and kelp (Dick 2001). The by a single individual in homothallic species, or when

http://calag.ucanr.edu • OCTOBER – DECEMBER 2018 209 two individuals bearing different mating types come chlamydospores (fig. 1D). Note that oospores of ho- into contact in heterothallic species. Exposure of het- mothallic species will be genetically identical to the erothallic species to certain fungi or chemicals can individual that produced them, because recombination also trigger the formation of oospores in the absence between homologous chromosomes cannot generate of mating (Pratt et al. 1972; Uchida and Aragaki variation, while oospores of heterothallic species will 1980). Oospores are particularly thick walled and can be genetically different from the two parents. Sexually also be regarded as long-term survival structures, generated variation may help the pathogen to adapt to often even more resilient to adverse conditions than novel environments or hosts.

(A) (B) Doug Schmidt, UC Berkeley Doug Schmidt, UC Berkeley Sims, Lee Laura

(C) (D) Doug Schmidt, UC Berkeley Doug Schmidt, UC Berkeley Sims, Lee Laura

FIG. 1. Micrographs (300× magnification) of (A) sporangia of Phytophthora ramorum, (B) a zoospore exiting a sporangium of Phytophthora bilorbang, (C) chlamydospores of Phytophthora ramorum and (D) an oospore of Phytophthora alni subspecies uniformis.

210 CALIFORNIA AGRICULTURE • VOLUME 72, NUMBER 4 In addition to variation in morphological traits among differ- (A) ent species, Phytophthora species have been differentiated based on the traits listed below. Some of these traits may have important implications for disease management and modeling (Erwin and Ribeiro 1996). For instance, one may assume that the release of a “cold-weather” Phytophthora species in a warm region may be rela- tively unsuccessful: (1) Temperature preferences: that is, adaptation to warm, cool or cold environments (Cooke et al. 2000). (2) Ability to infect a large number of unrelated hosts (generalists) versus ability to infect only closely related or a limited number of hosts (specialists) (Oßwald et al. 2014). (3) Mode of reproduction. Individuals belonging to homothallic spe-

cies can complete the sexual stage and produce oospores without UC Berkeley Sims, Lee Laura mating. Two individuals carrying opposite mating types (namely A1 and A2) are needed instead by outcrossing, heterothallic spe- (B) cies. It should be pointed out that sporangia are produced asexu- ally both in homothallic and heterothallic species, so normally lack of sex does not interfere with spread of a species. Also, it seems plausible that homothallic species may survive in harsher climates (M. Garbelotto, unpublished data), thanks to the fact they can often easily produce oospores without the need for mating with a compatible strain. (4) Range of soil pH preferred for growth (Kong et al. 2009). (5) Evolutionary relationship or relatedness. Species belonging to the same clade (a clade is a group of closely related species that evolved from the same ancestor; based on Jung et al. [2017] there are at least 12 clades in the Phytophthora genus) often have similar biology and can hybridize (Brasier et al. 2004; Husson et al. 2015). Laura Lee Sims, UC Berkeley Sims, Lee Laura Hybrids, however, may differ in host range and virulence from the UC Berkeley Sims, Lee Laura parental species. (C) (6) Virulence. Some Phytophthora species may be defined as oppor- tunistic, requiring a weakened host for infection or colonization, while other species are aggressive primary pathogens, leading to severe symptoms, impairment or mortality independent of host health status (Jung et al. 2011). This distinction is key in predicting the impact of emergent Phytophthora species; however, it is vari- able and the virulence of a species may change due to variation in the host or in the environment. (7) Aerially spreading, or spreading through infested soil or water (Scanu and Webber 2016). Soilborne and waterborne versus aerial species

The part of the plant that a Phytophthora species infects (, foliage or stem) drives many aspects of disease epidemiology. It is unclear what makes a Phytophthora species well adapted to be either airborne Laura Lee Sims, UC Berkeley Sims, Lee Laura UC Berkeley Sims, Lee Laura and primarily infect aerial parts of plants, or to be soilborne or water- borne with infections primarily limited to the roots and collars. FIG. 2. Visible symptoms caused by root and root collar infection by soilborne and waterborne Phytophthora species. (A) Coffeeberry (Frangula In the second case, aboveground symptoms are not caused directly by californica) in San Mateo County infected by Phytophthora multivora; infection but are a consequence of root mortality and of girdling of (B) coffeeberry outplanted in Marin County infected by Phytophthora the root collar (fig. 2). It should be noted that the distinction between megasperma on the left, and healthy coffeeberry on the right; and airborne and soilborne or waterborne species is not always clear-cut. (C) healthy sticky monkey flower (Diplacus aurantiacus) on the left, and In general, we define as airborne those species that spread through plants infected by Phytophthora megasperma on the right.

http://calag.ucanr.edu • OCTOBER – DECEMBER 2018 211 airborne propagules, while the soilborne and water- less abundant in sandy, well-drained soils (Cook and borne category includes species that mostly spread Papendick 1972); their frequency increases as rainfall through soil and water contaminated by propagules. To and temperature increase (Thompson et al. 2014); and be more precise, some species within the soilborne and high levels of soil infestation are associated with soils waterborne group appear to be better adapted to live that are poor in organic matter (Weste and Marks in water (e.g., lakes, streams, ponds), while others may 1987), as in the case of serpentine soils (Shearer and preferentially be found in matrical soil water. However, Crane 2011). Furthermore, disease development ap- we believe this difference to be often debatable and have pears to be more marked in those climates that alter- decided to group together soilborne and waterborne nate between wet and dry periods, for example, regions species in the same group. Table 1 compares a few im- characterized by a Mediterranean climate (Burgess et portant traits between soilborne and waterborne and al. 2016). The reasons behind marked disease severity airborne species. in areas with Mediterranean climate may be twofold. First, wet-dry cycles maximize the frequency and the TABLE 1. A quick comparison of a few traits of soilborne/waterborne and airborne duration of periods in which soil is wet but not satu- Phytophthora species rated at field capacity; in fact, anaerobiosis in saturated soils actually depresses sporulation by Phytophthoras Soilborne and waterborne Airborne (Nesbitt et al. 1979). Second, plants infected dur- ing wet periods may then become more susceptible They infest soil and water, and mostly infect They can be found in soil and water, so to colonization by Phytophthoras due to the stress roots and root collar. They can also infect infested soil and water can be responsible for induced by prolonged periods of drought (Desprez- aerial portions of plants through infested their spread. Infections occur mostly on aerial tools or splash of soil or water particles plant parts, but occasional root infections are Loustau et al. 2006). (Madden et al. 1992; Scanu and Webber 2016; possible (Rizzo et al. 2005). Trione and Roth 1957). Establishment and spread of exotic They can survive for relatively long periods They can survive in soil but are not extremely species in soil or potting media. Survival may be long-lived (Fichtner et al. 2007) and are less independent of plant debris present in the competitive than soilborne and waterborne Major pathways for the initial primary introduction soil (Vettraino et al. 2010), while sporulation species (Eyre et al. 2013). Conversely, survival of exotic soilborne and waterborne Phytophthora spe- appears to be linked to the presence of roots in inert potting media can be extensive cies in a new region include the use of infected plant or root fragments embedded in the soil (Jung (Shishkoff 2007). et al. 2013). material or of infested soil (Liebhold et al. 2012; Parke et al. 2014). Phytophthora inoculum (e.g., infectious Production of chlamydospores, or oospores Production of chlamydospores, or oospores propagules) may be present either in infected plant tis- or stromata-like hyphal aggregations (masses or stromata-like hyphal aggregations (masses sue, in the soil plants have been grown in, or in both of vegetative structures) may be necessary for of vegetative structures) may be necessary for long-term survival in soil (Crone et al. 2013). long-term survival in soil (Crone et al. 2013). (Jung et al. 2016). Once introduced in a new site, sec- ondary spread up to a few meters per year can be the Sporangia can be caducous or not caducous Sporangia are almost always caducous (i.e., result of root-to-root infection or of infection of roots (Erwin and Ribeiro 1996). deciduous) (Erwin and Ribeiro 1996). by hyphae, and of movement of infectious or survival structures (sporangia, chlamydospores and oospores) through splash (Ristaino and Gumpertz 2000), or of A consequence of being soilborne or waterborne is the movement of insects or small animals that may an extremely patchy distribution at the landscape level. carry Phytophthora propagules on their bodies. Longer- However, the distribution of soilborne or waterborne range spread, up to tens or even hundreds of kilometers Phytophthora species can be further expanded through per year, can occur through soil movement due to ve- various human-related mechanisms, including planting hicular traffic or to animal movement, and through the of infected plants and movement of soil along roads or movement of infested water. paths (Krull et al. 2013; Ristaino and Gumpertz 2000). Spread through infested water may occur at dif- Additionally, once introduced in a site, propagules of ferent spatial scales: a few meters when dealing with these pathogens will move on their own following grav- matrical water (i.e., water present among soil particles), ity and movement of water in waterways and in under- tens or hundreds of meters for runoff water, hundreds ground water tables (Maurel et al. 2001). When humans or even thousands of meters for infested underground are not directly involved in their spread, these patho- water tables (Hayden et al. 2013), and even longer dis- gens often appear to move more easily downhill than tances for infested water carried in streams and rivers uphill. Downhill spread can be significant because it as evidenced for the spread of P. lateralis in southern occurs via both root contacts and downward movement Oregon and Northern California (Hansen et al. 2000). of infested water or contaminated soil. Uphill move- Infested water can also be moved by helicopter or ment, by contrast, is usually more limited, because it trucks used for firefighting or for road dust abatement. relies almost exclusively on root contacts. Spread at the landscape level is thus affected by abun- There are some commonalities among all soil- dance of roads and streams, by intensity of human borne and waterborne species: They tend to be more activities, by topography (with draws and depressions abundant in soils with a loamy to clay structure and being more conducive to spread), by abundance of

212 CALIFORNIA AGRICULTURE • VOLUME 72, NUMBER 4 favorable sites (clay soils, lower organic content) and be equally effective when trying to detect different by densities of animals and, especially, of susceptible Phytophthora species (Erwin and Ribeiro 1996). In hosts. Abundance of snails and ants may also contrib- some cases, drying the soil before baiting is recom- ute to increase disease severity in a site (El-Hamalawi mended (Erwin and Ribeiro 1996). One advantage of and Menge 1996). baiting is that precise knowledge of the exact portion Increasing host diversity in a site may have diamet- of the plant or the specific soil particles that may con- rically different effects on disease spread rate and dis- tain viable Phytophthora infection is not needed; for ease severity. When the percentage of infectious hosts this reason, baiting is one of the preferred diagnostic increases (note that some hosts may be susceptible but approaches when surveying large facilities, soil and not infectious), so do disease spread rate and disease wildland waterways. However, for unknown reasons, severity. This is, for instance, the case of some Lupinus some species are difficult to detect by baiting and thus species present in woodlands infested by P. cinnamomi negative baiting results can represent false negatives. in Spain (Serrano et al. 2010). Conversely, when in- Furthermore, baiting requires experience, particu- creased host diversity leads to a decrease of percentage larly in the identification of the agent causing the of the more infectious hosts, an effect called “inoculum symptoms on the bait, which can be done by direct dilution” leads to decreased spread rates and disease culturing or by the use of molecular approaches on severity (Haas et al. 2011). symptomatic tissue (see 2 and 3 below). (2) Direct isolation from symptomatic (or asymp- Prevention and diagnostics tomatic) plant tissue using Phytophthora selective me- of Phytophthora species dia (Jeffers and Martin 1986; Scanu et al. 2014). There are a few drawbacks of direct isolation: (a) one needs The most effective control of soilborne or waterborne to sample a portion of the plant where the pathogen is Phytophthoras relies either on the prevention of their viable and viability may be dependent on season and/or introduction or on slowing their further spread, once phenological state of the host plant; and (b) some spe- introduced. Prevention of primary introductions can cies may have almost identical morphology and there- be achieved by properly testing plant material to be fore are difficult to identify correctly without molecular outplanted and by using stock produced in facilities testing. The most significant drawback of this approach that observe best management practices (BMPs) aimed is that sampling requires destructively excising a por- at limiting establishment of these soilborne patho- tion of the plant, and often that requires destructively gens in soil, pots and water systems as well as plants manipulating plants to identify symptomatic portions (Parke and Grünwald 2012). Recently, BMPs aimed to be plated. False negatives for both direct isolation at reducing risk of infestation have become avail- and baiting techniques can occur in the case of species able (see Sims et al. 2018 or www.suddenoakdeath. that are not easily culturable, or due to the presence of org/wp-content/uploads/2016/04/Restoration.Nsy_. secondary microorganisms preventing Phytophthoras Guidelines.final_.092216.pdf and http://ucanr.edu/ from growing axenically. phytophthorabmps). (3) Molecular identification techniques are based Notwithstanding the use of material produced in on the detection of specific sequences of nucleic acids facilities adhering to such BMPs, it has been repeatedly (DNA, RNA) (Martin et al. 2012; Prigigallo et al. 2015). advised to place all new plant material in a quaran- Molecular approaches are not dependent on the vi- tined area for several weeks and to observe it for the ability of the pathogen but do require that the correct onset of symptoms (Alexander and Lee 2010). In the portion of an infected plant be processed. Additionally, absence of a certificate indicating the production fa- there are risks of false positives due to either lab cility is free of Phytophthora species (Brasier 2008), a contamination or to a lack of specificity of the assay direct inspection of plants to be purchased needs to be detection probes, caused either by the existence of performed, including observations of the health status undiscovered closely related species or by poor probe of root systems. design. False negatives are commonly caused by poor Four different approaches may be utilized for direct processing or by the presence of inhibitors, whose con- testing of these substrates: centration in tissues or substrate may vary depending (1) Baiting. Plant material (symptomatic and on time of year and material sampled. asymptomatic), root and soil samples can be baited The high sensitivity of molecular approaches thus by submerging the sample in water and floating can be regarded both as a benefit and a drawback. A baits comprised of susceptible plant parts such as benefit because it allows the detection of relatively leaves and fruits. Baiting must be done under aerobic young incipient infections or infections in remission conditions assured by mixing the correct amounts characterized by a low amount of pathogen DNA of plant material or soil and water (see Erwin and (Hayden et al. 2004). A drawback because results with Ribeiro 1996), but protocols vary greatly with regards such approaches may not be informative as to the vi- to specific baiting protocols (Jung et al. 1996; Scanu ability of the pathogen, due to the fact that unviable et al. 2013). Different baits (e.g., consisting of differ- dead cells of the target organism may also be detected ent plant species or of different plant parts) may not (Chimento et al. 2011).

http://calag.ucanr.edu • OCTOBER – DECEMBER 2018 213 Molecular identification assays normally are based can be used outside the laboratory (Lane et al. 2010). on one of two approaches: (a) Results may be positive A general limitation of these techniques is that the or negative and based on the success or failure of as- antibodies used for ELISA and LFD rarely are species- says specifically designed to target one or a few species. specific and often cross-react with several Pythium spe- Or (b) Results may be based on the homology (e.g., cies (Timmer et al. 1993). similarity) of DNA sequences of so-called barcode Control or mitigation of extant Phytophthora infes- genetic loci. The two most common barcode loci for tations deserves its own review, but an excellent syn- Phytophthora species identification are the nuclear in- thesis of approaches has been provided by Hayden et al. ternal transcribed spacer (ITS) and the mitochondrial (2013), and we refer the reader to such a review. cytochrome oxidase (COX) (Cooke et al. 2000; Martin et al. 2014). In general, homology has to be 98% or Phytophthora species possibly higher between a published sequence and the sequence detected in restoration sites of an unknown sample to identify the unknown. Most conspecific genotypes have a DNA homology of 99% to As of the summer of 2017, at least 25 soilborne Phy- 100%. Sequences are published in several databases, but tophthora species have been recovered in restoration the most commonly used one remains GenBank (www. sites near natural ecosystems or in parks in the greater ncbi.nlm.nih.gov/genbank/). One caveat: The robust- San Francisco Bay Area in California. Eight species ness of species identification based on DNA homology are well known, eight are closely related and belong to depends on ensuring the published sequence is associ- Clade 6, and nine represent new putative hybrid spe- ated with a correctly identified species. cies (see supporting table S1 online, http://ucanr.edu/u. (4) Immunological techniques are based on the cfm?id=215, for a partial list). All identifications were detection of specific antibodies to proteins or other done both on cultures in vitro, and were based in part molecules produced by a pathogen species. These tech- on morphology and in part on the homology of DNA niques, including the enzyme-linked immunosorbent sequences between published sequences and sequences assay (ELISA) and lateral flow device (LFD), showed of newly obtained isolates at the species-specific loci higher diagnostic sensitivities than that of culture- ITS and/or COX (Martin et al. 2012). Identification of based morphological identification, which can be influ- novel Phytophthora species, their hosts or substrates enced by environmental conditions (Lane et al. 2010). and the California counties in which these species ELISA tests are generally inexpensive and relatively were found is still being completed, and, as a result, the The undersides of these petri dishes filled with easy to perform, which makes them suitable for large- information provided in table S1 should be taken as Phytophthora-selective scale prescreening. On the contrary, LFD tests are more provisional and subject to change. Contributors of un- growth medium show expensive and are not suitable for large-scale testing. published data are acknowledged in the acknowledge- Phytophthora colonies Their strength is that they are rapid and robust, and ments section at the end of this review. growing out of baits. Please note that as this review is being written, more Phytophthora species are being discovered in California wildlands and parks; however, these spe- cies are not included here because they have not been shared yet by their identifiers. Also, note that the distri- bution information in this review is simply limited to the few areas that have already been surveyed. Hence, the actual distribution of the Phytophthora species included in this paper may be much larger than that reported here and may increase as more surveys are completed. Additionally, the of these spe- cies is in flux, and thus their species designation may change in the future. A provisional and partial list of soilborne species isolated in sites in Northern California as of the sum- mer of 2017 includes, in alphabetical order, P. bilor- bang, P. cactorum, P. chlamydospora, P. cinnamomi, P. citricola, P. crassamura, P. cryptogea, P. erythroseptica, P. gonapodyides, P. inundata, P. ‘kelmania’, P. lacustris, P. megasperma, P. plurivora, P. quercetorum, P. riparia and P. tentaculata. Nine hybrid species were also iden- tified, but their precise diagnosis is yet to be completed, so we prefer to omit them. Table S1 provides a com- parative analysis of the species listed in this review, for a range of important traits. Laura Lee Sims, UC Berkeley Sims, Lee Laura

214 CALIFORNIA AGRICULTURE • VOLUME 72, NUMBER 4 Phytophthora diseases are no longer limited to the ornamental plant production industry or to agriculture, but are also emerging as a complex issue in wildlands.

In conclusion, Phytophthora diseases are no longer key tools for mitigating and preventing further infesta- limited to the ornamental plant production industry tions. This will require that the scientific community or to agriculture but are also emerging as a complex is- continue raising awareness about this emerging prob- sue in native plant production and deployment. These lem and familiarizing stakeholders with details of some diseases are emerging not only in association with of the Phytophthora species that are increasingly being inadvertent casual introductions, or due to the proxim- found in California wildlands. c ity of wildlands to agricultural settings, but also, unex- pectedly, in association with infested plant production facilities providing stock for restoration projects and thus with restoration projects themselves. The problem M. Garbelotto is UC Cooperative Extension Specialist and Adjunct Professor, Department of Environmental Science, Policy and is compounded by several issues, including (1) our in- Management, University of California, Berkeley; S.J. Frankel is ability to properly sample plant stock and the need for Forest Pathologist, U.S. Forest Service, Pacific Southwest Research new sampling approaches (see Swiecki et al. 2018, page Station, Albany, CA; and B. Scanu is Research Scientist and 217 in this issue), (2) the realization that Phytophthora Lecturer, Dipartimento di Agraria, Sezione di Patologia Vegetale ed species are in a continuum ranging from impossible to Entomologia (SPaVE), Università degli Studi di Sassari, Sassari, Italy. culture to easily culturable, (3) the fact that geographic Funding for this review was provided by the San Francisco distribution and the host ranges of Phytophthora spe- Public Utilities Commission and the assistance of Mia Ingolia, Jessica Appel and Greg Lyman is appreciated. Data on cies are not clearly known and are constantly changing, Phytophthora species identified in California were kindly provided (4) the discovery of novel species at a faster pace than by Tedmund Swiecki and Elizabeth Bernhardt, Phytosphere ever before and, finally, (5) reports that species forced Research; Laura Lee Sims and Matteo Garbelotto, UC Berkeley; to comingle in production facilities and in infested Tyler Bourret and David M. Rizzo, UC Davis; and Suzanne Rooney- wildlands may generate new hybrid entities. Latham and Cheryl Blomquist, California Department of Food Early detection and understanding that there is a and Agriculture. Phytophthora problem in Northern California remain

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