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   Phytophthora lateralis (oomycete)
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    Taxonomic name: Phytophthora lateralis Tucker & Milbrath 1942
    Common names: cedar root disease, Port Orford-cedar root disease, Port-Orford cedar root rot, root rot of Chamaecyparis
    Organism type: oomycete
    Phytophthora lateralis is the causal agent of a serious root disease of Port Orford-cedar (Chamaecyparis lawsoniana), an ecologically and economically important tree. It advances quickly and can kill large trees within several years. The disease has devastated the ornamental planting and timber industry of Port Orford-cedar throughout the Pacific Northwest causing losses of millions of dollars. In natural ecosystems P. lateralis reduces populations of this important tree in riparian areas, which may have flow on effects to terrestrial and aquatic life. Control efforts are focused on reducing spread of this pathogen via roads, and the development of resistant populations.
    Phytophthora lateralis is a water mould (Oomycetes) that infects the root system of Port Orford-cedar, also known as Lawson’s cypress (Chamaecyparis lawsoniana). Young hyphae lack cross-walls (coenocytic), but may become septate in older cultures. Mycelium is usually smooth but occasionally snarled or tuberous. The sporangia are ovoid, ellipsoid or obovoid, colourless, non-papillate, 20-60 μm long, 12-20 μm wide. Sporangia are borne on simple sporangiophores and germinate to produce either zoospores or hyphae in water. Mature sporangia contain 25-40 zoospores, which are laterally biflagellate and 10-12 μm in diameter. Zoospores form cysts, which germinate to produce hyphae. Asexual chlamydospores which arise as lateral swellings on the hyphae (a distinctive feature in contrast to the clustered chlamydospores of other non-papillate species of Phytophthora, and hence the species Latin name) are 20-77 μm in diameter and often sessile. P. lateralis is homothallic and sometimes produces oogonia with paragynous antheridia in single culture. Oogonia are rare, but when observed are smooth, spherical and terminal and 33–50 μm in diameter. Oospores are 28-46 μm in diameter and pigmented (Erwin & Ribeiro, 1996 in EPPO, 2009; Tucker & Milbrath, 1942).

    The first symptoms of the disease in C. lawsoniana involve gradual colour changes in the foliage: to yellow, bronze and finally a light brown to tan colour as the foliage dries out. In cool, damp weather this colour change sequence may take two to three months, whereas in hot and dry weather it may only take two to three weeks (Tucker & Milbraith, 1942). These symptoms are uniform throughout the tree if the infection begins in the roots, but localized on individual branches in the case of aerial infection (Erwin & Ribeiro, 1996). The pathogen generally invades the roots, killing tissues as it advances, and causing a brown and water-soaked appearance. The infection eventually spreads to the root crown of the tree and causes girdling of the trunk and ensuing foliar changes described (Tucker & Milbraith, 1942). Removal of the outer bark from the infected root collar shows a sharp line of demarcation between the white healthy tissue and the dark brown dead tissue; a black resinous line can sometimes be seen on the cambium (Tucker & Milbraith, 1942). Eventually plants die; infected seedlings die rapidly but it may take several years for larger trees to die. Pacific yew (Taxus brevifolia) shows similar but less severe symptoms (EPPO, 2009).

    Occurs in:
    Habitat description
    In its invasive range in North America the main host of Phytophthora lateralis is Port Orford-cedar (Chamaecyparis lawsoniana: Cupressaceae). It was originally thought to be host specific to this species, but Pacific yew (Taxus brevifolia: Taxaceae) was reported as a host in 1991 (DeNitto & Kliejunas, 1991 in EPPO 2009). However Pacific yew is less susceptible to P. lateralis than Port Orford-cedar (Murray & Hansen, 1997). There have also been one off reports of it occurring on other Chamaecyparis species. Its native host has not been confirmed but recent evidence suggests its native range is Taiwan (Brasier et al., 2010).

    Artificial infection has also been achieved in inoculation experiments with Rhododendron species (Hoitink & Schmitthenner, 1974 in EPP0, 2009), Pseudotsuga menziesii (Pratt et al., 1976 in EPPO, 2009) and Chamaecyparis nootkatensis (Kliejunas, 1994 in EPP0, 2009). This suggests that P. lateralis may be carried latently by some plants which hare not natural hosts (EPPO, 2009).

    There are a number of published reports of this oomycete infecting other species. However reports on hosts other than cedars (Chamaecyparis spp.) and T. brevifolia are considered to be misidentifications of other Phytophthora spp. (CSL, 2006; EPPO, 2009).

    Infection can occur at temperatures of 3-25 °C, but temperatures of 15-20 °C are optimal. Growth is restricted at 25 °C and inhibited entirely at 30 °C (Sinclair et al., 1987 in EPPO, 2009; Tucker & Milbraith, 1942).

    General impacts
    Ecosystem change: Port Orford-cedar is an important tree in its native range (coniferous forests of southwestern Oregon and northern California) where it is found along streams and in areas with year-round seepage, and is often the dominant riparian tree especially in the southern part of its range. It tolerates ultramafic soils in the region, recycles calcium to surface soils and is often associated with rare plant species. In riparian areas it is important for providing shade to streams and stabilising banks. Wood from dead trees provides diverse habitat for salmonid fish and other aquatic life (Hansen et al., 2000).

    Port Orford-cedar has been drastically reduced or eliminated from large portions of riparian environments and wetlands by P. lateralis. Reduction of this important tree can have catastrophic impacts on streamside plant communities and aquatic ecology. Particularly on ultramafic soils, where Port Orford-cedar may be the only tree species able to grow, consequences to stand structure can be particularly pronounced (Hansen & Hamm, 1997; Hansen, 1999; Hansen et al., 2000). Loss of old-growth stands of Port Orford-cedar can have negative impact on wildlife species that require old-growth characteristics (Hansen et al., 2000). Additionally, the size and age class of cedar has shifted as a result of the disease and forest harvest, with large old trees being replaced by smaller, young trees (Hansen et al., 2000).

    While Pacific yew is also an important forest species, providing food and cover for wildlife and shade and stability for streams, it is less susceptible to P. lateralis and mortality is low (Hansen et al., 2000).

    Economic: Port Orford-cedar or Lawson’s cypress is grown as an ornamental tree in Europe and the Pacific Northwest. Since the incursion of P. lateralis the multi-million dollar ornamental nursery production in Washington and Oregon has largely been destroyed (Hansen & Hamm, 1997; Hansen et al., 2000). Port Orford-cedar trees in parks in British Columbia experience significant annual losses due to P. lateralis with a high cost of replacement (Utkhede et al., 1997).

    Port Orford-cedar has been one of the most valuable commercial timbers in the world, with a value on the export market of up to ten times that of Douglas-fir (Pseudotsuga menziesii) (Hansen et al., 2000).

    Pacific yew is less susceptible to P. lateralis, and the pathogen is likely to have only limited impact on this tree. Unusual morality of Pacific yew has only been observed in areas where it grows in close proximity to Port Orford-cedar (Murray & Hansen, 1997).

    Other: Social impacts include loss of business in nursery and forestry sectors, and effects on tourism and fishing due to forest closures (Hansen et al., 2000).

    Direct isolation of Phytophthora lateralis from soil, even on selective media, is generally not successful probably due to low numbers of propagules (Hamm & Hansen, 1984). However various baiting methods have been developed (e.g. Hansen & Hamm, 1984; Tsao et al. 1995a in EPPO, 2009), using plant tissue of its host Chamaecyparis lawsoniana. Infected tissue is then plated onto selective media, from which P. lateralis can be isolated from (Hamm & Hansen, 1984). More recently PCR-based protocols have been developed for rapid identification of the pathogen (Winton & Hansen, 2001; Schena et al., 2008) and ELISA tests have been developed, but need refining (Greenup, 1998 in EPPO, 2009).
    Geographical range
    Native range: Until recently the native range has been unknown. However the discovery of P. lateralis in a Taiwanese yellow cedar (Chamaecyparis obtuse var. formosana) forest in 2008 suggests that Taiwan and possibly Japan comprise its native range (Brasier et al., 2010).
    Introduced range: Canada (British Columbia), France, Netherlands, Scotland, United States (California, Oregon, Washington).
    Introduction pathways to new locations
    Horticulture: Transportation of C. lawsonia plants and contaminated soil are thought to be an important pathway for long-distance and international spread of this pathogen (EPPO 2009; Hunt, 1959). Long-distance movement of P. lateralis is generally via chlamydospores and oospores (Kauffmann & Jules, 2006).
    Translocation of machinery/equipment: Infested mud can be carried by heavy equipment (e.g., logging equipment) (Jules et al., 2002).

    Local dispersal methods
    Natural dispersal (local): Natural short-distance dispersal is usually via motile zoospores. Zoospores are transported through soil and water and can occasionally be spread aerially or by plant-to-plant contact, which can occur through through foliar contact or below ground via root grafting (Hunt, 1959).
    On animals: A major way this pathogen is spread is via animals and people moving infested mud (Jules et al., 2002).
    Road vehicles: Dispersal by vehicles is the primary vector for spreading of the pathogen to uninfested areas. Trees in areas crossed by roads were more likely to be infected than those not crossed by roads (Jules et al., 2002).
    Water currents: Flagellate zoospores of P. lateralis are not able to move upstream to any significant extent and thus subsequent infections via water transport only travel downslope and downstream (Zobel et al., 1985; (Hunt, 1959). Almost all Port Orford-cedar growing along streams with roots in contact with water are killed within a few years of P. lateralis introduction to the stream (Hansen et al., 2000).
    Management information
    Legislative: Phytophthora lateralis is on the EPPO A1 action list, meaning that countries at risk of invasion are recommended to regulate it as a quarantine pest. The European Union prohibits the import of Chamaecyparis plants. Other EPPO countries are recommended to establish similar measures (EPPO, 2009).

    Preventative: The US Forest Service has established permanent and wet season road closures in areas with Port Orford-cedar. These closures are an important tool to stop the spread of P. lateralis, as transportation via roads has been identified as the primary method of spread. Other preventative methods include confining harvesting, road maintenance and other activities to the summer dry season; sanitation of vehicles and equipment before they reach uninfested areas; altering and diverting roads away from cedar areas; growing cedar on sites unfavourable for disease spread (Hansen et al. 2000; Hansen & Hamm, 1997; Jules et al., 2002).

    In nurseries preventative measures include soil sterilisation, use of fungicides registered for use against Phytophthora root rots, disinfection of materials and preventing the introduction or movement of infested soil (EPPO, 2009).

    Cultural: Methods that have been suggested to reduce P. lateralis infection include growing disease-free stock in uninfected soil, avoiding monocultures of Port Orford-cedar in windbreaks or hedges and ensuring adequate drainage (Utkhede et al., 1997). However the most commonly suggested and employed technique is the reduction of cedar density, especially in infected sites near roads (Goheen, 2000 in Jules et al., 2002).

    Genetic resistance: Following observations of healthy trees in the midst of dead neighbours led Hansen et al. (1989) to demonstrate that heritable resistance to P. lateralis occurs in Port Orford-cedar. Since then a resistance breeding programme for Port Orford-cedar has been underway with the goal of providing resistant seedlings for forest regeneration.The programme has produced promising results and first generation resistant seedlings are now available (Oh et al., 2006; Sniezko, 2003; Sniezko, 2006). Resistance to P. lateralis offers the best chance of re-establishing Port Orford-cedar in areas where the pathogen is established and is important in long-term disease management. However, genetic resistance offers no protection for surviving stands of the cedar, and it will be hundreds of years before the resistant seedlings can replace the large old trees (Hansen et al., 2000).

    Biological: Treating Port Orford-cedar with drench applications of the bacteria Enterobacter aerogenes (Strain B8) has shown some success. Diseased trees treated over four years in Vancouver, British Columbia had lower disease ratings and higher growth rates than water-treated controls (Utkhede et al., 1997). However this, or any other biological control method, have not been used in practice (EPPO, 2009).

    Lifecycle stages
    Phytophthora lateralis infects roots of its hosts in the same way as other Phytophthora spp. Zoospores are produced in sporangia, and are released under suitable conditions (moist and temperatures of 10 to 20 °C). Zoospores are flagellated and can travel short distances autonomously, or may be dispersed by water. Zoospores may also encyst, and the cysts may be further transported by water and have a further opportunity to infect a susceptible root (EPPO, 2009).

    Zoospores initiate the infection in the fine roots (Kliejunas, 1994 in EPPO, 2009). The mycelium then spreads throughout the inner bark and cambium of the root system to the root collar. Infection spreads upwards in an irregular triangle. Under favourable conditions, the pathogen may be splashed from soil onto foliage, and produce sporangia on the foliage. These sporangia may be dispersed by wind and rain, and aerial spread is possible (Trione & Roth, 1957; Trione, 1959 in EPPO, 2009). P. lateralis also forms chlamydospores, thick walled resting spores, which persist in the soil and in leaf or root debris, allowing long-term survival and overland movement of the pathogen (EPPO, 2009). P. lateralis, which is homothallic, sometimes also produces oospores, which are similarly hardy and can survive long distance travel (Kauffmann & Jules, 2006).

    P. lateralis can survive and remain infectious in absence of living host tissue for at least 7 years in a range of natural environments (Hansen & Hamm, 1997).

    Reviewed by: Everett M. Hansen, Professor, Emeritus, University of Wisconsin, Madison
    Principal sources: European and Mediterranean Plant Protection Organization (EPPO) 2009. Phytophthora lateralis. Bulletin OEPP. 39(1). APR 2009. 43-47.
    Compiled by: National Biological Information Infrastructure (NBII) & IUCN/SSC Invasive Species Specialist Group (ISSG)
    Last Modified: Wednesday, 23 February 2011

ISSG Landcare Research NBII IUCN University of Auckland