Figure 1. Morphology of Phytophthora citrophthora. Upper row, Papillate, ovoid to ellipsoid sporangia, some of which have two papillae. According to Mchau and Coffey (1994), the morphology is more diverse than illustrated here. Lower row, Oospore within a globose oogonium with an amphigynous antheridium (oospores have not been seen in nature but have been induced in culture in a few cases [Kellam and Zentmyer, 1986]); a globose chlamydospore, which is also rarely found; and sporangia forming in a simple sympodium. (Courtesy A. Vaziri; Reproduced from Erwin and Ribeiro, 1996) Click image to see larger view.

 

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

Figure 3. Papillate sporangia and sporangium with two apices (arrows) of Phytophthora citrophthora. Bar = 10 µm. (Courtesy Elizabeth A. Bush; Reproduced from Bush et al., 2006)

 

Figure 4. Oogonium of Phytophthora citrophthora (×1,000) with an amphigynous antheridium and plerotic oospore. (Courtesy Jean B. Ristaino)

Figure 5. Canker caused by Phytophthora citrophthora on a clementine tree branch. (Courtesy Antonio Vicent Civera, Instituto Agroforestal Mediterráneo, Universidad Politécnica de Valencia)

Figure 6. Liquid (exudate) discharged from Phytophthora citrophthora-diseased tissues and roots of an orange tree. (Courtesy G. A. Zentmyer; Reproduced from D'Arcy et al., 2001)

Figure 7. Wilting clementine tree with Phytophthora citrophthora-diseased fruit. (Courtesy Antonio Vicent Civera, Instituto Agroforestal Mediterraneo. Universidad Politecnica de Valencia)

Figure 8. Clementine tree with a dead branch and Phytophthora citrophthora-diseased fruit. (Courtesy Antonio Vicent Civera, Instituto Agroforestal Mediterraneo, Universidad Politécnica de Valencia)

Introduction

Phytophthora citrophthora  (R. E. Sm. & E. H. Sm.) Leonian (1925)

Phytophthora citrophthora was first isolated by Smith and Smith in 1906 from rotted lemons and named Pythiacystis citrophthora (Smith and Smith, 1906). It is a major pathogen of citrus and infects not only fruit and causes a brown rot but also infects roots and crowns and causes a trunk gummosis. Leonian renamed the species P. citrophthora in 1925 (Leonian, 1925). Synonyms of P. citrophthora include Pythiacystis citrophthora R. E. Sm. & E. H. Sm. (1906) and P. imperfecta var. citrophthora (R. E. Sm. & E. H. Sm.) Sarej. (1936). Note that these are invalid names (Cline et al., 2008). A complex of species infect citrus, including P. citrophthora, which is active at moderate temperatures during the winter months (<30°C), and P. parasitica, which is active at high temperatures during the summer months (>30°C). P. hibernalis and P. syringae are also low-temperature Phytophthora species that are active during the winter months on citrus (Erwin and Ribeiro, 1996). Other species that have been reported on citrus include P. boehmeriae, P. cactorum, P. cinnamomi, P. citricola, P. dreschleri, P. megasperma, and P. palmivora. P. citrophthora is classified as a group II species (Stamps et al., 1990; Waterhouse and Waterston, 1964) (Fig. 1).

Cultural Characteristics

Mycelium is thick and cottonlike (Fig. 2). Colony growth is finely radiate with stellate and flamelike growth. The minimal temperature for growth is less than 5°C, the optimum temperature for growth is 24–28°C, and the maximum temperature for growth is 32–33°C, with no growth above 35°C.

Reproductive Structures

Asexual Structures

Sporangiophores:
 Sporangiophores branch irregularly, with swelling at the point of branching. Some sporangia are borne singly or in loose sympodia, with a swelling at the point of branching.

Sporangia:
Sporangia are noncaducous and mostly papillate , often with two widely divergent apices. P. citrophthora produces various sporangia shapes, ranging from spherical to ovoid, obpyriform, obturbinate, and ellipsoid. Distorted sporangial shapes can occur in water with multiple papillae and offset pedicel attachments. Sporangia are 18–60 × 23–90 μm (average 30 × 45 μm) (Fig. 3). The length–breadth ratio is less than 1.6.

Chlamydospores:
 Chlamydospores do not ordinarily occur on citrus isolates in culture but form in roots (Sjoerdsma et al., 1988). Chlamydospores are 25–35 μm in diameter (average 28 μm).

Hyphae:
Hyphae are smooth and coarse and 3–7 μm in diameter.

Sexual Structures

Sexual structures are rare and not considered part of P. citrophthora’s life history because they do not occur in nature on citrus. Sex organs were not included in the Stamps et al. (1990) key or in the original description. Mchau and Coffey (1994) reported that less than half of the 77 isolates of P. citrophthora (30%) they studied produced oospores when paired with the A2 mating type of P. capsici. The pathogen is heterothallic. When sex organs are produced, antheridia are amphigynous and oogonia are 26–36 μm in diameter and contain plerotic plerotic oospores that are 21–28 μm in diameter (Erwin and Ribeiro, 1996) (Fig. 4).

Host Range and Distribution

See Table 17.2 from Erwin and Ribeiro (1996) for a complete list of hosts of P. citrophthora.

Symptoms

P. citrophthora causes citrus brown fruit rot, trunk gummosis, collar and root rot, and leaf and shoot blight.

 

Infested soil is often the inoculum source. Foot rot typically begins near the soil line. Dark, water-soaked lesions form in the bark and a sour smell can occur. Gum exudes from affected areas (Fig. 5) and gummosis occurs usually as a lesion below the bud union. Foot rot occurs as a lesion above the union. Spread of bark lesions can occur vertically for 50 cm or more (Fig. 6). Fibrous root rot or infection of the small feeder roots that are produced in the upper layer of the soil can occur.

 

Infection of the fruit usually occurs at the bottom of the fruit. Infection can start in several areas on the same fruit, eventually covering the entire fruit. Diseased fruit can become firm and leathery and eventually mummify and fall off of the tree (Figs. 7 and 8).

 

Dark, water-soaked lesions can form on the leaf tips and margins, and premature leaf drop can occur in areas with high rainfall.

 

The pathogen can infect roots and trunks of almond (Prunus spp.), walnut (Juglans spp.), and pistachio (Pistacia spp.) and can cause a root rot, foot rot, and trunk canker. P. citrophthora causes a dieback of rhododendron stems, while P. cinnamomi causes a root rot. P. citrophthora can cause pod rot on cacao (Theobroma cacao) in Brazil, along with P. capsici and P. palmivora.

 

Diagnostics:
The pathogen can be isolated after washing infected tissue and plating on semiselective media, such as P10VP (Tsao and Ocana, 1969).

References

Bush, E. A., Stromberg, E. L., Hong, C., Richardson, P. A., and Kong, P. 2006. Illustration of key morphological characteristics of Phytophthora species identified in Virginia nursery irrigation water. Plant Health Progress doi:10.1094/PHP-2006-0621-01-RS.

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.

D'Arcy, C. J., Eastburn, D. M., and Schumann, G. L. 2001. Illustrated Glossary of Plant Pathology. Plant Health Instructor doi:10.1094/PHI-I-2001-0219-01.

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

Kellam, M. K., and Zentmyer, G. A. 1986. Morphological, physiological, ecological, and pathological comparisons of Phytophthora species isolated from Theobroma cacao. Phytopathology 76:159-164.

Leonian, L. H. 1925. Physiological studies on the genus Phytophthora. Am. J. Bot. 12:444-498.

Mchau, G. R. A., and Coffey, M. D. 1994. An integrated study of the morphological and isozyme patterns found within a worldwide collection of Phytophthora citrophthora and a redescription of the species. Mycol. Res. 98:1291-1299.

Sarejanni, J. A. 1936. A collar rot of cultivated Solanum and the classification of the genus Phytophthora. Ann. Inst. Phytopathol. Benaki 2:35-52.

Sjoerdsma, J. D., Menge, J. A., and Johnson, E. V. L. 1988. Ecology of Phytophthora citrophthora root rot of citrus. (Abstr.) Phytopathology 78:1519.

Smith, R. E., and Smith, E. H. 1906. A new fungus of economic importance. Bot. Gaz. 42:215-221.

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.

Tsao, P. H., and Ocana, G. 1969. Selective isolation of species of Phytophthora from natural soils on an improved antibiotic amended media. Nature 223:636-638.

Waterhouse, G. M., and Waterston, J. M. 1964. Phytophthora citrophthora. CMI Descr. Pathog. Fungi Bact. 33:1-2.