Phytophthora lateralis
2009; Wiley; Volume: 39; Issue: 1 Linguagem: Inglês
10.1111/j.1365-2338.2009.02234.x
ISSN1365-2338
Autores Tópico(s)Plant Disease Resistance and Genetics
ResumoEPPO BulletinVolume 39, Issue 1 p. 43-47 Free Access Phytophthora lateralis First published: 11 March 2009 https://doi.org/10.1111/j.1365-2338.2009.02234.x European and Mediterranean Plant Protection Organization Organisation Européenne et Méditerranéenne pour la Protection des Plantes AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Identity Name: Phytophthora lateralis Tucker & Milbrath Taxonomic position: Chromista, Oomycota, Oomycetes, Pythiales, Pythiaceae Common name(s) of the disease: root rot of Chamaecyparis Special notes on taxonomy or nomenclature: Phytophthora lateralis belongs to Waterhouse group V and was in Clade 8a in the phylogenetic analysis of Cooke et al. (2000). Ribosomal DNA sequencing of the internal transcribed spacer region indicated that P. lateralis is most closely related to Phytophthora ramorum (Werres et al., 2001; Martin & Tooley, 2003) EPPO code: PHYTLA Phytosanitary categorization: EPPO A1 List no. 337. Hosts The main host of P. lateralis is Chamaecyparis lawsoniana (Lawson's cypress). Taxus brevifolia (Pacific yew) has also been reported as a host (DeNitto & Kliejunas, 1991). P. lateralis is thought to have been introduced, from an unknown origin, into North America, where it encountered the native C. lawsoniana; if this is so, it may have a native host, as yet unknown, in its area of origin (possibly another Chamaecyparis sp. or other member of the Cupressaceae). Although there are isolated records of infection of other Chamaecyparis spp. (C. formosensis, C. obtusa), it seems clear, from the absence of any published information, that these plants, which are also widely cultivated, do not suffer significant damage or loss due to P. lateralis. There are reports of P. lateralis naturally infecting other hosts, including in particular other conifers, ornamental Ericaceae, and Actinidia spp. (Robertson, 1982). These are all considered to be misidentifications of other Phytophthora spp., notably P. gonapodyides. Artificial infection has been obtained in inoculation experiments with Rhododendron spp. (Hoitink & Schmitthenner, 1974), Pseudotsuga menziesii (Pratt et al., 1976) and Chamaecyparis nootkatensis (Kliejunas, 1994). This opens the possibility that P. lateralis might be carried latently by, and survive on, plants which are not natural hosts. Geographical distribution11 An updated geographical distribution can be viewed on the EPPO website. EPPO region: France (found but not established), Netherlands (found but not established) North America: Canada (British Columbia), USA (California, Oregon, Washington) EU: France (found but not established), Netherlands (found but not established). Note: P. lateralis was first reported in Washington State (US) in 1923, and described and named by Tucker & Milbrath (1942), by which time it had spread to other parts of Washington and to Oregon. By the 1950s, the pathogen was present in British Columbia (Atkinson, 1965) and by 1980 in North-Western California (Kliejunas & Adams, 1981). Though there have been reports in other parts of North America, the Pacific seaboard appears to be the only area in which the pathogen is established. Reports in Europe are believed to be incursions (of unknown origin), and in New Zealand misidentifications. Since P. lateralis is considered to be an exotic introduction to North America from an unknown source (Hansen et al., 2000), it may be presumed that it exists elsewhere, most possibly in some other area of the Pacific Rim. Biology P. lateralis parasitizes roots in the same way as other Phytophthora spp. In an established infection on a root of C. lawsoniana, P. lateralis is present as mycelium, from which sporangia are formed. Under suitable conditions (i.e. available moisture and temperatures of 10–20°C), the sporangia release zoospores that can swim a few cm autonomously, or also be carried by natural movement of soil water. The zoospores make contact with and attach to susceptible host rootlets, germinate and infect (Kliejunas, 1994). They may also encyst, and the cysts may be further transported by water and have a further opportunity to infect a susceptible root. P. lateralis mycelium spreads through the inner bark and cambium of the root system to the root collar, which can result in the eventual death of the host. Infection can occur at temperatures of 3–25°C but temperatures of 15–20°C are optimal (Sinclair et al., 1987). The foliage of C. lawsoniana is sometimes infected, if it comes into contact with the ground. Infection spreads upwards in an irregular triangle. Under favourable conditions, the pathogen produces sporangia on the foliage, and aerial spread is possible (Trione & Roth, 1957; Trione, 1959). The mycelium of P. lateralis forms chlamydospores which persist in the soil and in leaf or root debris, ensuring the long-term survival and overland movement of the pathogen. P. lateralis, which is homothallic, sometimes also produces oospores, which can similarly survive. In buried pot tests, P. lateralis was recovered at a low frequency after seven years, but the pathogen was killed in days when infected roots were exposed to the sun on the soil surface (Hansen & Hamm, 1996). The other known host, T. brevifolia, is less susceptible (Murray & Hansen, 1997). Surveys have shown that T. brevifolia is only killed by P. lateralis where it was growing along streams in close association with dead or dying C. lawsoniana (Hansen et al., 2000). This suggests that a high level of zoospore inoculum is needed to obtain infection of this host. Detection and identification Symptoms The first above-ground symptoms of infection of C. lawsoniana are slight wilting of the foliage, which undergoes a gradual colour change to yellow, bronze and finally to a light brown or tan colour as it dries out (Erwin & Ribeiro, 1996). These symptoms are uniform throughout the foliage if only the roots are infected, but localized in the case of aerial infection. Infected roots appear water-soaked and are usually a deep cinnamon brown colour. Infection eventually spreads up to the trunk and causes girdling of the crown (Erwin & Ribeiro, 1996). Removal of the outer bark from the infected root collar can show a sharp line of demarcation between the white healthy tissue and the dark brown dead tissue; a black resinous line can be seen on the cambium (Kliejunas & Adams, 2004). This symptom distinguishes the disease from otherwise similar symptoms caused by Phytophthora cinnamomi (Erwin & Ribeiro, 1996). Trees weakened through infection are commonly attacked by bark beetles (Phloeosinus spp.). Infected seedlings die rapidly, but it can take several years for larger trees to die. Root infections kill the tree more quickly than aerial infection. T. brevifolia shows similar but less severe symptoms. Hoitink & Schmitthenner (1974), who reported that they recovered P. lateralis from rhododendron crowns, found it to cause slight damage when they inoculated rhododendron roots, similar to that caused by other minor root pathogens of rhododendron such as Phytophthora citrophthora, Phytophthora gonapodyides, Phytophthora megasperma and Phytophthora parasitica. It is not now believed that the fungus they recovered was P. lateralis, but the possibility remains that P. lateralis can infect certain plants other than its major hosts, causing only slight damage. Morphology P. lateralis is readily isolated from pieces of root and stem tissue taken from the advancing edge of symptoms of the disease (Tucker & Milbrath, 1942). It has a slow growth rate but it can be grown on cornmeal agar, potato dextrose agar, oatmeal agar (Tucker & Milbrath, 1942) and V8 sterol agar (Englander & Roth, 1980). Production of chlamydospores is most abundant in the absence of light in V8 broth with 20 µg mL−1 or β-sitosterol at 24–25°C (Englander & Roth, 1980). Maximum sporangial production is on V8 agar or broth containing 10 µg mL−1β-sitosterol in the light at 14 to 16°C (Englander & Roth, 1980). The mycelium is colourless, usually smooth but occasionally gnarled, coenocytic and up to 8 µm wide, becoming septate in older cultures. The sporangia are ovoid, ellipsoid or obovoid, colourless, non-papillate, (20)-36-(60) µm long and (12)-15-(20) µm wide. Sporangia persist on simple sporangiophores and germinate to produce either zoospores or hyphae in water. Mature sporangia contain 25–40 zoospores. The laterally biflagellate reinform zoospores are 10–12 µm in diameter, germinate to produce hyphae and are capable of forming cysts. The chlamydospores are (20)-40-(77) µm in diameter, often sessile, lateral on the mycelium (in contrast to the clustered chlamydospores of other non-papillate species of Phytophthora). P. lateralis is homothallic and produces paragynous antheridia in single culture. Oogonia are smooth, spherical and terminal and 33–50 µm in diameter. Oospores are (28)-40-(46) µm in diameter and pigmented (Erwin & Ribeiro, 1996; Hall, 1991; Tucker & Milbrath, 1942). Detection and inspection methods Various baiting methods have been developed (Trione, 1959; Ostrofsky et al., 1977; Hansen et al., 1979; Hamm & Hansen, 1984; Tsao et al., 1995a, b), involving baiting with susceptible plant tissue, incubation and plating onto a selective media. Tsao et al. (1995a) developed a quantitative protocol of this technique. Ostrofsky et al. (1977) found baiting more efficient from organic matter than from soil. Winton & Hansen (2001) developed a conventional PCR-based protocol that could detect the pathogen in water and plant tissue (including tissue used as baiting material, thereby allowing indirect testing of soil). However, this assay was shown to cross-react with the recently described P. ramorum. An ELISA test has been developed that shows promise but needs work to improve sensitivity (Greenup, 1998). Commercial ELISA kits have been used to detect P. lateralis several years after tree death (Hansen, 1997). Pathways for movement Natural short-distance dispersal can be plant-to-plant, aerial, or through soil and water. Below-ground movement is primarily by zoospores, which may be carried down slopes by water movement. Plant-to-plant contact can be above or below ground. Cases are known where C. lawsoniana has undergone abundant intraspecific root grafting, which has served as a path for vegetative spread of P. lateralis (Gordon & Roth, 1976). Above ground, foliage infection can be transmitted through contact between adjacent foliage. Aerial spread is thought to be primarily through zoospores, as mature sporangia remain attached to the sporangiophores and infection coincides with temperatures conducive for zoospore release (10 to 20°C) (Trione, 1959). P. lateralis spread slowly through the Pacific states of the USA over several decades, and its progress was monitored throughout this period. A comprehensive study of the disease in Southwest Oregon and Northwest California by Jules et al. (2002) concluded that dispersal by vehicles had the greatest effect in spreading the pathogen to uninfested areas. Trees in areas crossed by roads were more likely to be infected than those not crossed by roads. Vehicles on roads also spread inoculum further than foot traffic (both animal and human). Waterways were also pathways of spread, since hosts at sites with large or persistent streams were more likely to become infected (Jules et al., 2002). Long-distance movement of inoculum, particularly human-mediated movement of infested soil; mainly involves chlamydospores and oospores. Zoospores are more important for short-distance dispersal. In international trade, the most likely pathways for P. lateralis would be plants for planting of C. lawsoniana, or plants for planting of non-host plants with contaminated soil attached, or contaminated soil as such. Pest significance Economic impact P. lateralis is a serious pest of C. lawsoniana, which is one of the most valuable commercially harvested conifer timbers in the world, commanding up to ten times the price of Pseudotsuga menziesii wood from the same site (Hansen et al., 2000). Hansen (1985) quoted prices of 1000–4000 USD per thousand board feet for living trees of C. lawsoniana, with wood from dead trees having little value. The greatest loss in commercial forestry results from the death of young trees at the lower size limits of merchantability. Presently, the disease continues to kill trees in forestry plantations but also hedgerow and landscape trees in the Pacific states of the USA and has resulted in the loss of wood export markets especially to Japan (Hansen et al., 2000). Trees of C. lawsoniana in parks in British Columbia generally experience significant annual losses due to root rot caused by P. lateralis, and the cost of replacing them has become prohibitive (Utkhede et al., 1997). P. lateralis is thought to have nearly destroyed the multi-million dollar industry for production of ornamental C. lawsoniana in Northwest Oregon and Western Washington (Hansen et al., 2000). In addition to social impacts through loss of business in nursery and forestry sectors, tourism and fishing have been affected due to forest closures (Hansen et al., 2000). In addition, P. lateralis has destroyed large numbers of C. lawsoniana within the natural range of the species, where it grows in riparian habitats, with large trees providing shade and long lasting structure to waterways. Control Control measures can be applied in two situations, in the nursery and in the plantation. In the nursery, soil sterilization has been used in the past, and remains a possibility though it is not generally regarded as good practice. Various fungicides are registered as drench treatments against Phytophthora root rots of nursery plants. In the EPPO region, these mainly target Phytophthora cinnamomi but may have efficacy against P. lateralis. Hygiene measures are recommended for nurseries, including disinfection of materials, preventing the introduction or movement of infested soil or infected plant material, assuring adequate drainage, preventing plants in containers from becoming pot-bound, use of resistant cultivars (see below). Hunt & O’Reilly (1984) found that C. lawsoniana could be grafted onto non-susceptible hosts such as Chamaecyparis formosensis or Chamaecyparis thyoides, but it is not clear whether this was effective in protection from P. lateralis, or has been put into practice. For control of P. lateralis in plantations, cultural measures were recommended by the US Federal Agencies managing P. lateralis in the Pacific forest areas in order to prevent further spread of the pathogen (Greenup, 1998; Hansen et al., 2000). These include: conducting forestry operations in summer months; cleaning of vehicles and equipment before leaving infested areas and entering areas that are not infested; wide spacing of susceptible hosts and growing susceptible hosts on sites unfavourable for pathogen spread (i.e. at raised elevations, away from waterways and roads); regulating the harvesting of C. lawsoniana timber; road closures in infested areas. In addition to these measures, roads were engineered in ways to reduce their risk as a pathway for spread of the pathogen, and logging systems were modified to reduce the need for and extent of new roads. In a resistance breeding programme for C. lawsoniana in the USA, promising results have been obtained (Hansen et al., 2000), though even the most resistant trees appeared to be susceptible as juveniles. Hansen et al. (2000) suggest that resistant trees still offer the best chance of re-establishing infested areas with C. lawsoniana, preferably in combination with cultural and biological control. Though Utkhede et al. (1997) investigated a strain of Enterobacter aerogenes as a soil drench to control P. lateralis in naturally infected C. lawsoniana trees, and obtained encouraging results over a four-year period, it is not clear that this, or any other biological control method, has been used in practice. Phytosanitary risk P. lateralis is extremely damaging to C. lawsoniana in nurseries, plantations and natural vegetation in the Pacific regions of USA and Canada where it has been introduced and spread. The disease takes the form of a root and crown rot leading to extensive tree mortality. In the EPPO region, the endangered area is mainly the Atlantic parts of Western Europe, having a wet maritime climate, but extends to conifer nurseries in any part of the region. The phytosanitary risk mainly concerns C. lawsoniana, which is grown as a valued ornamental, produced and sold by nurseries, especially as semi-dwarf cultivars for parks and gardens. It is one of the most important ornamental conifer species for the nursery trade. In contrast to the situation in North America, C. lawsoniana is infrequently grown as a timber tree in the EPPO region, though there are plantations in Northern Spain and Portugal which would be at risk. In practice, the risk of introduction of C. lateralis into the EPPO region is reduced, because the endangered area mainly falls within the European Union, which prohibits the import of plants of Chamaecyparis, and also restricts the import of growing medium, and of trees and shrubs generally, from non-European countries. Although it is recognized that T. brevifolia is also a (less susceptible) host of P. lateralis, this species exists only in botanical collections in the EPPO region, and has no commercial importance in production or trade. Phytosanitary measures P. lateralis was added in 2006 to the EPPO A1 action list, and endangered countries are therefore recommended to regulate it as a quarantine pest. The main risk of its introduction is from the import of infested plants for planting of C. lawsoniana, of other plants which though not hosts might carry inoculum of P. lateralis, and of infested soil. The existing measures of the European Union (EU, 2000) already cover these risks by the prohibition of the import of plants for planting of Chamaecyparis, the severe restrictions applied to the import of trees and shrubs from non-European countries, and the measures concerning growing medium containing soil. Other EPPO countries are recommended to establish similar measures. Footnotes 1 An updated geographical distribution can be viewed on the EPPO website. Acknowledgement This datasheet was prepared by Dr I. M. Smith (former Director General of EPPO) on the basis of a datasheet prepared by J. Woodhall and Dr C. Sansford (Central Science Laboratory, York, GB). References Atkinson RG (1965) Phytophthora species inciting root rot of Chamaecyparis lawsoniana and other ornamentals in coastal British Columbia. Canadian Journal of Botany 43, 1471– 1475. CrossrefWeb of Science®Google Scholar Cooke DEL, Drenth A, Duncan JM, Wagels G & Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 30, 17– 32. CrossrefCASPubMedWeb of Science®Google Scholar DeNitto GA & Kliejunas JT (1991) First report of Phytophthora lateralis on Pacific yew. Plant Disease 75, 968. 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