Phytophthora katsurae

Overview

The causal agent of trunk rot of Asian chestnut was originally described as Phytophthora castanea by Katsura and Uchida. The name was deemed invalid and the pathogen was renamed P. katsurae (Ko and Chang, 1979) in honor of Professor Emeritus K. Katsura. P. katsurae causes disease on Asian chestnut (Katsura, 1976), coconut palm (Uchida et al. 1992), and cacao (Liyanage and Wheeler 1989). The pathogen has been reported from Japan, Korea, Côte d’Ivoire, Hawaii, Australia, Papua New Guinea, and Jamaica and has recently been isolated from forest soils not associated with symptomatic hosts in Taiwan and Hainan Island, China. P. katsurae is closely related to P. hevea.

Morphology

Sporangia papillate, non-caducous, ovoid to obpyriform (17.0-38.9 X 14.6-29.2 µm) in filtered creek water or deionized water after cold shock. It is homothallic. Oospores on cornmeal agar amended with β-sitosterol are abundant, globose and plerotic; diameter ranges from 19.2 to 25.3 µm (mean 20 µm) with a 2.4-2.9 µm wall thickness. Oogonia diameters measure 33.7-38.5 X 24.1-31.3 µm. The oogonia (34.0-46.2 X 21.9-26.7 µm) of Korean isolates differ slightly in size from the original species description (Ho et al. 2008). Warty protuberances are present on the surface of oogonia, which is the primary means by which this species is distinguished from the closely related P. hevea, but this character may be an unstable (Ko et al. 2006). Antheridia are amphigynous with long, funnel-shaped stalks at the base of the oogonia. Chlamydospores are 12.0-19.2 µm and globose but are produced rarely (Ko and Chang 1979, Erwin and Ribeiro 1996, Oh et al. 2008). Isolates from Hawaii have fewer oogonial wall protruberances (Ko et al. 2006), and longer tapered oogonial bases (Uchida et al., 1992) than the chestnut isolates.

Genetics

Phytophthora katsurae is clustered with P. heveae in phylogenetic clade 5 (Blair et. al. 2008). P. katsurae and P. heveae are genetically very closely related (98.8%) based on ITS sequences of genomic rDNA (Cooke et al 2000; Ko et al. 2006) and nuclear gene and mitochondrial gene sequences (Kroon et al. 2004).

Growth

Temperature optimum 26-28°C, minimum 9°C, and maximum 32°C.

Distinguishing characteristics for identification

Causal species of chestnut ink disease in Asia, Europe, and the United States include P. katsurae, P. cambivora and P. cinnamomi but only P. katsurae produces papillate sporangia. P. katsurae oogonia, with warty protruberances, can be confused with those of P. cambivora but P. cambivora is heterothallic, has larger antheridia and oogonia, and larger and non-papillate sporangia. On coconut, oogonia and oospores are abundant in infected host tissue. P. katsurae is distinguishable from P. hevea by having warty protruberances on oogonia as compared to the smooth-walled oospores of P. hevea. The warty protruberances are difficult to observe in vivo but are more readily observed in pure culture. Hawaii isolates with fewer oogonial protruberances appear to be transitional between P. hevea (smooth oogonia) and the P. katsurae from chestnut and forest soil (many protruberances)(Ko et al. 2006). P. hevea is non-pathogenic to chestnut.

The searchable web-based database phytophthora-id.org is useful for rapid identification of Phytophthora species based on sequencing of the ITS or Cox spacer regions, followed by BLAST searching the database. The database includes only sequences that are associated with published Phytophthora species descriptions or classic Phytophthora phylogenetics references.

Disease History

A trunk rot of Japanese chestnut (Castanea crenata) was discovered in 1962 causing severe damage in chestnut growing areas, particularly on young trees with bare ground between them (Uchida 1967). In Japan, young infected trees died within four years after infection. Historically, disease was managed by growing grass mulches to prevent splash dispersal of soilborne inoculum onto trunks. Fungicide treatment in late spring was also effective in reducing disease. All cultivars of C. crenata as well as European chestnut (Castanea sativa) are susceptible, whereas American chestnut (C. dentata) and Chinese chestnut (C. mollissima) are resistant.

The disease on chestnut, now called chestnut ink disease, has since been found in plantation-grown and forest-grown chestnut trees (C. crenata x C. mollissima) in South Korea (Oh et al 2008). Symptomatic Tsukuba and Ginyose cultivars of chestnut trees have been found in three chestnut plantations: two in Kyungnam province and one in Jeonnam province. It is not clear how many trees have been infected and cut down, and which chestnut cultivars are susceptible to P. katsurae. However, pathogenicity tests among Korean cultivars suggests that P. katsurae is highly pathogenic to at least seven cultivars (Parkmi2, Daebo, Eunsan, Mansaki, Ibuki, Idea, Arima).

The pathogen has been found on coconut palm (Cocos nucifera L.) in Hawaii since 1971. The disease can develop in all tissues of the coconut palm beginning with the nut itself and spreading to cause heart rot (Uchida et al 1992). In Cote d’Ivoire, P. katsurae causes severe damage to coconut plantations (Pohe et al. 2003) and it has been also reported from cacao (Theobroma cacao L.) causing the disease Phytophthora pod rot (Liyanage and Wheeler 1989).

Impacts in the Forest

Phytophthora katsurae mainly attacks chestnut trees in plantations, but historically it did not have a large economic impact. However, recent disease outbreaks in chestnut trees planted in Korean forests caught the attention of forest pathologists and chestnut breeders. In 2005, 15- to 20-year-old chestnut trees were killed in different areas of the southern region of Korea. Economic losses from forest-planted chestnut trees are potentially large, since more than 100,000 tons of chestnuts are exported annually from 79,000 ha of plantations in forests (Kim 2006). The disease is favored by heavy rainfall in summer which causes flooding for hours to days.

On coconut palm (Cocos nucifera L.) in Hawaii, the disease caused by P. katsurae is very destructive, having killed hundreds of high-value trees and reducing the availability of this species for landscaping purposes (Uchida et al. 1992). First observed in Maui in 1971, disease has spread to the islands of Kauai, Hawaii, and Oahu. Other species of palm are not affected. In Côte d’Ivoire, P. katsurae causes the most severe disease of coconut palms grown in plantations. Because of the morphological differences between the coconut isolates and the chestnut isolates, it was not certain if they were the same species (Uchida et al. 1992). Originally identified as P. hevea, the Côte d’Ivoire isolates appear to be similar to the Hawaiian isolates (Uchida et al. 1992) and both are now considered to belong to P. katsurae (Ko et al., 2006).

Forest and Wildland Hosts and Symptoms

In Asian species of chestnut in Japan and Korea, P. katsurae causes chestnut ink disease. The pathogen attacks trunks, branches, and exposed roots causing necrotic lesions that exude black sap. When the stem is girdled, the tree is killed. P. katsurae is also found in forest soil in Taiwan (Ko et al. 2006) and Hainan Island in southern China (Zeng et al. 2009), not associated with any known symptomatic hosts, suggesting that these areas may represent the geographic origin of the species. Little is known about the epidemiology of P. katsurae on chestnut, but it is presumed to be soilborne (Stamps 1985).

On coconut palms, drooping and death of young fronds is the first symptom (Uchida et al. 1992). As disease progresses, the heart of the tree rots and older leaves are also killed. Bud rot and early nut fall can also occur (Pohé et al. 2003). Trunk lesions may be observed on the lower stem. The pathogen is believed to spread by wind-driven rain. Tree trimming may also spread the disease because wounding of the inner bark appears necessary for disease. The pathogen has likely been spread within Hawaii through the movement of infected trees and nuts (http://www.extento.hawaii.edu/Kbase/crop/Type/p_katsu.htm).