Figure 1. Morphology of Phytophthora fragariae. Sporangia are nonpapillate, form sympodially, and proliferate internally and externally. Antheridia are mostly amphigynous but are sometimes paragynous. (Courtesy A. Vaziri; Reproduced from Erwin and Ribeiro, 1996) Click image to see larger view.

 

Figure 2. Culture of Phytophthora fragariae grown on V-8 juice agar. (Courtesy Jean B. Ristaino)

 

Figure 3. Sporangia of Phytophthora fragariae on an infected root surface. (Courtesy Robert D. Milholland; Reproduced, by permission, from Milholland, 1994)

 

Figure 4. Oospores of Phytophthora fragariae in root of infected strawberry plant. (Courtesy Robert D. Milholland; Reproduced, by permission, from Milholland, 1994)

 

Figure 5. Advanced stage of red stele disease, resulting in the wilting and death of the plant. (Courtesy Robert D. Milholland; Reproduced, by permission, from Milholland, 1994)

 

Figure 6. Rat's tail appearance of primary roots infected with Phytophthora fragariae. (Courtesy Robert D. Milholland; Reproduced, by permission, from Milholland, 1994)

 

Figure 7. Longitudinal section of roots of strawberry plants showing typical red-core symptoms caused by Phytophthora fragariae. (Used, by permission, from SCRI-Dundee Archive, Scottish Crop Research Institute, www.bugwood.org)

 

Introduction

Phytophthora fragariae  C. J. Hickman (1940)

 

Phytophthora fragariae was first isolated by Hickman in 1940 from strawberries in the United Kingdom (Hickman, 1940). It causes red core disease in the United Kingdom and red stele disease in the United States. It is an important pathogen of strawberries and has a limited host range. There are no synonyms known for this pathogen (Cline et al., 2008). Two closely related subspecies include P. fragariae var. rubi, which causes root rot of red raspberries ( Forster and Coffey, 1992; Wilcox et al., 1993), and P. fragariae var. oryzobladis, which causes a leaf disease on rice (Wang and Lu, 1978). The two varieties do not cause disease on strawberry and are distinct based on analysis of mitochondrial DNA. Ho and Jong studied isolates from strawberry and loganberry and redescribed the species in 1988 (Ho and Jong, 1988). It is a group V species (Stamps et al., 1990). Waterhouse (1963) noted the absence of hyphal swelling and chlamydospores and the large sporangia of P. fragariae to distinguish it from P. megasperma (Fig. 1).

Cultural Characteristics

The minimum temperature for growth is 3°C, the optimum temperature for growth is 18–22°C, and the maximum temperature for growth is 30°C. Some isolates have a temperature maximum of 25°C. It is considered a low-temperature species and grows slowly in culture (Fig. 2). 

Reproductive Structures

Asexual Structures

 

Sporangiophores:

Sporangiophores branch sympodially in water and bear sporangia on the tips.

 

Sporangia:

Sporangia are mostly large, measuring 22–52 × 32–91 µm (Fig. 3). Sporangia are ovoid to ellipsoid to obpyriform. Sporangia are nonpapillate and noncaducous and form sympodially. They proliferate internally and externally.

 

Chlamydospores:

Chlamydospores are not formed.

 

Hyphae:

P. fragariae produces thick and fluffy aerial hyphae on clarified V-8 agar with a slight brown discoloration of the media on the bottom of the plate (Fig. 2). Hyphae are meandering and coiling with sparse elongated branches. Small hyphal swellings, often in clumps, may form.

 

Sexual Structures

 

P. fragariae is homothallic.

 

Antheridia:

Antheridia are mostly amphigynous and single celled but are sometimes paragynous.

 

Oogonia:

Oogonia are globose to subglobose and often have a tapered base. Oogonia are 28–44 µm in diameter.

 

Oospores:

Oospores are globose and 34 to greater than 40 µm in diameter and form readily in the host but scantily in culture (Fig. 4). Oospores do not fill the oogonium (aplerotic). Oospores turn golden brown with age. 

Host Range and Distribution

Host

Common Name

Disease

Geographical Distribution

Dryas drummondii

Drummond's mountain avens

Red stele

Canada

Fragaria ×ananassa

Strawberry

Red stele; red core; brown-core root rot; black stele; Lanark-shire disease

England, Scotland, United States, Canada, New Zealand, France, Austria, Russia, Czechoslovakia, Japan, Netherlands, Italy, Bulgaria, Taiwan, Sweden

Fragaria spp.

Beach and woodland strawberry, strawberry

Root rot

United States

Geum spp.

Avens

Red stele; root rot

Canada, United States

Lycopersicon esculentum

Tomato

Root rot

Canada

Nicotiana tabacum

Tobacco

Root rot

Canada

Potentilla spp.

Cinquefoil, five-finger, tormentil

Root rot; red stele

Canada, United States

Rubus spp.

Red raspberry, loganberry, thimbleberry

Root rot; red rot

Canada

Spinacia oleracea

Spinach

Seedling rot

Canada

Symptoms

Red stele or red core is the most important disease of strawberry worldwide. It can be detected by severely stunted plants. On warm days, entire plants or outer leaves of plants wilt suddenly (Fig. 5). Older leaves of infected plants become yellow, red, and brown. The root systems of infected plants are devoid of lateral roots, giving larger roots with black tips and a "rat's tail" appearance (Fig. 6). When the stele is cut, a red or reddish brown color is seen surrounding the white cortical tissue (Fig. 7). The red discoloration can extend up the root into the crown of the plant. Roots that develop during the summer months do not become infected and the plant can partially recover during the warm season. Oospores form in the root, crown, and leaves and can survive in the soil for many years (Erwin and Ribeiro, 1996).

References

Cline, E. T., Farr, D. F., and Rossman, A. Y. 2008. A synopsis of Phytophthora with accurate scientific names, host range, and geographic distribution. Plant Health Progress doi:10.1094/PHP-2008-0318-01-RS.

 

Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society, St. Paul, MN.

 

Forster, H., and Coffey, M. D. 1992. Molecular characterization of Phytophthora isolates with non-papillate sporangia causing root rot of raspberry using mtDNA restriction fragment length polymorphisms. Mycol. Res. 96:571-577.

 

Hickman, C. J. 1940. The red core disease of the strawberry caused by Phytophthora fragariae n. sp. J. Pomol. Hortic. Sci. 18:89-118.

 

Ho, H. H., and Jong, S. C. 1988. Phytophthora fragariae. Mycotaxon 31:305-322.

 

Milholland, R. D. 1994. A monograph of Phytophthora fragariae and the red stele disease of strawberry. N. C. Agric. Res. Serv. Tech. Bull. 306.

 

Stamps, D. J., Newhook, F. J., Waterhouse, G. M., and Hall, G. S. 1990. Revised tabular key to the species of Phytophthora de Bary. Mycol. Pap. 162. CAB International, Wallingford, United Kingdom; Commonwealth Mycological Institute, Kew, Surrey, England.

 

Wang, P., and Lu, J. Y. 1978. Phytophthora leaf blight of rice seedlings, a new disease of rice. Acta Microbiol. Sin. 18:95-101. (In Chinese with English summary)

 

Waterhouse, G. M. 1963. Key to the species of Phytophthora de Bary. Mycol. Pap. 92. CAB International, Wallingford, United Kingdom; Commonwealth Mycological Institute, Kew, Surrey, England.

 

Wilcox, W. F., Scott, P. H., Hamm, P. B., Kennedy, D. M., Duncan, J. M., Brassier, C. M., and Hansen, E. M. 1993. Identity of Phytophthora species attacking raspberry in Europe and North America. Mycol. Res. 97:817-831.