Figure 1. Morphology of Phytophthora citricola. Sporangia are semipapillate, noncaducous, and variable in shape and are formed on a simple sympodium. Oogonia are globose with paragynous antheridia. (Courtesy A. Vaziri; Reproduced from Erwin and Ribeiro, 1966) Click image to see larger view.

 

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

 

Figure 3. Semipapillate sporangium of Phytophthora citricola. Bar = 10 µm. (Courtesy Elizabeth A. Bush; Reproduced from Bush et al., 2006)

 

Figure 4. Oogonium of Phytophthora citricola with a paragynous antheridium (×1,000). (Courtesy Jean B. Ristaino)

 

Figure 5. Canker and collar rot caused by Phytophthora citricola on an avocado tree. Symptoms usually appear relatively low on the trunk. (Courtesy Howard D. Ohr; Reproduced, by permission, from UC IPM Online, University of California Statewide Integrated Pest Management Program)

 

Figure 6. Canker and collar rot caused by Phytophthora citricola on an avocado tree. Note cracked, flaking bark from fungal infection near the root crown. (Courtesy David Rosen; Reproduced, by permission, from UC IPM Online, University of California Statewide Integrated Pest Management Program)

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Introduction

Phytophthora citricola  Sawada (1927)

 

Phytophthora citricola was first isolated from Sekkan orange fruit with brown rot symptoms in Formosa (Taiwan) and described by Sawada in 1927 (Sawada, 1927). The pathogen can also cause a root rot and trunk canker on many woody hosts. Synonyms of P. citricola include P. cactorum var. applanata Chester (1932), P. pini Leonian (1925) (note: previously considered a synonym of P. cactorum), P. pini var. pini Leonian (1925), and P. pini var. antirrhini Sundar. & T. S. Ramakr. (1928) (Erwin and Ribeiro, 1996). Tucker (1931) treated P. citricola as a synonym of P. cactorum, but Waterhouse (1963) and Ho and Chang (1992) recognized it as a distinct species. Cooke et al. (2000) suggested that P. inflata is conspecific with P. citricola, but Kroon et al. (2004) showed that the two species differ in their mitochondrial DNA (Cline et al., 2008). Gallegly and Hong (2008) divide P. citricola into three subgroups based on antheridial characters and consider P. inflata to be conspecific with P. citricola type I. The pathogen is a group III Phytophthora species (Stamps et al., 1990) (Fig. 1).

Cultural Characteristics

Cultural characteristics include a stellate or rosette pattern on agar medium (Fig. 2). The minimum temperature for growth is 3°C, the optimum temperature for growth is 25–28°C, and the maximum temperature for growth is 31°C. 

Reproductive Structures

Asexual Structures

 

Sporangiophores:

Sporangiophores are long and slender, up to 3 µm wide and often swelling, particularly at the point of branching. Branching is irregular and lax, not regularly sympodial, and not often occurring immediately beneath the sporangium (Waterhouse and Waterston, 1966).

 

Sporangia:

Sporangia are absent or rare on solid media but readily form in water solution. The shape of the sporangia is highly variable, ranging from obovoid, obclavate, and obpyriform to slightly flattened on one side to irregularly shaped with three to four lobes (Bush et al., 2006) (Fig. 3). Sporangia are semipapillate, and the papillae are wide and flat. Sporangia are 21–44 × 30–75 µm (average 34 × 47 µm). The length–breadth ratio is less than 1.6. They are noncaducous and persistent on the stalk. The cross wall at the base of the sporangium is flush with the base without a septal plug. Gallegly and Hong recognize three forms (I, II, and III), based on DNA markers, sporangia, and antheridial characters, including type I, sporangia with multiple apices, large inflated antheridia (>13 µm), distortion, and lateral attachments; type II, ovoid sporangia and small antheridia (<10 µm); and type III, ellipsoid sporangia with antheridia perpendicular to the oogonium (Gallegly and Hong, 2008).

 

Chlamydospores:

Chlamydospores are rare and reported on oatmeal agar only in some isolates.

 

Hyphae:

Hyphae are 6 µm wide and without frequent hyphal swellings.

  

Sexual Structures

 

P. citricola is homothallic and sex organs are abundant on most media.

 

Antheridia:

Antheridia are paragynous (rarely amphigynous) and often diclinous. The antheridium cell is small, 1–12 × 7.5 µm, and can be inflated or perpendicular to the oogonium.

 

Oogonia:

Oogonia are spherical and 18–35 µm in diameter (average 25.5 µm), sometimes tapering to a funnel-shaped base. The wall is smooth, thin, and pale yellow to yellowish brown.

 

Oospores:

Oospores are spherical, almost plerotic, and 16–30 µm (average 22.0 µm) (Fig. 4).

Host Range and Distribution

Host

Common Name

Disease

Geographical Distribution

Abies spp.

Balsam fir, white fir, Fraser fir

Crown rot; blight; canker

Unites States

Acer saccharum

Sugar maple

Collar rot

United States

Actinidia chinensis

Kiwifruit

Collar and root rot

New Zealand

Aesculus hippocastanum

Horse chestnut

Bleeding canker; root rot; dieback

United Kingdom

Antirrhinum spp.

Snapdragon

Root rot

United Kingdom, New Zealand

Aucuba japonica

Gold dust plant

Root rot

United States

Azalea indica

Formosa azalea

Root rot

Australia

Beaufortia sparsa

Swamp bottlebrush

Root rot

Australia

Brachychiton populneus

Bottle tree

Root rot

Argentina

Ceanothus griseus

Ceanothus

Trunk canker

United Kingdom

Chamaecyparis lawsoniana

Lawson cypress; Port Orford cedar

Wilt

Netherlands

Chamelaucium uncinatum

Geraldton wax plant

Root rot

Australia

Citrus spp.

Citrus

Shoot blight; fruit rot; brown fruit rot

Australia, Antilles, Japan, Portugal, South Africa, Taiwan, United Kingdom

Corylus avellana

European hazel

Collar and trunk canker

Greece

Cyclamen spp.

Persian violet

Leaf blight

Greece

Cydonia oblonga

Quince

Root rot

Formosa (Taiwan)

Cytisus praecox

Legume

Root rot

Netherlands

Erica hiemalis

White heather

Decline

Australia

Euphorbia resinifera

Spurge

Root rot

Formosa (Taiwan)

Feijoa sellowiana

Feijoa

Brown rot of fruit

Italy

Fragaria chiloensis

Strawberry

Fruit rot

Bulgaria, Taiwan

Hakea francisiana

Red spike hakea

Root rot

Australia

Hebe pinguifolia

Pagei Hebe

Root and stem rot

United Kingdom

Hevea brasiliensis

Rubber

Root and stem rot

Sri Lanka

Hibiscus rosa-sinensis

China rose

Root rot; wilt

United States

Hibiscus schizopetalus

Japanese lantern

Root rot; wilt; black root

New Zealand, United Kingdom, United States

Humulus lupulus

Hop

Collar and trunk canker; crown and root rot

United Kingdom, Greece

Juglans spp.

Black and English walnut

Root and crown rot

United States

Lycopersicon esculentum

Tomato

Basal rot; seedling wilt

Italy

Malus pumila

Apple

Root rot

Canada, Formosa (Taiwan), Netherlands, New Zealand, United Kingdom

Olea europaea

Olive

Collar and trunk canker

Greece

Persea americana

Avocado

Trunk canker; fruit rot

United States, Mexico

Phaseolus vulgaris

Kidney bean

Root rot

Taiwan

Pieris japonica

Japanese andromeda

Shoot blight; stem dieback

New Zealand, United States

Pinus radiata

Monterey pine

Root rot

United States

Pistacia vera

Pistachio

Apoplexy; wilt

Greece

Platanus orientalis

Oriental plane tree

Collar and trunk rot

Greece

Primula japonica

Primrose

Root rot

United Kingdom

Prunus spp.

Almond, apricot, cherry, peach

Collar rot; root and crown rot

Iran, Greece, Rhodesia, United States

Pseudotsuga menziesii

Douglas fir

Crown rot

United States

Psidium guajava

Guava

Fruit rot

Hawaii

Quercus spp.

California live oak, white oak, red oak

Trunk canker; seedling root rot

United States

Rhododendron spp.

Rhododendron

Bud, leaf, and twig blight; wilt

Australia, France, Germany, Netherlands, United States

Rubus idaeus

Raspberry

Root rot

United Kingdom, United States

Sambucus spp.

Elder

Crown rot

Canada

Schinus molle

Australian or California pepper

Crown rot

Argentina

Syringa vulgaris

Lilac

Shoot blight of suckers

United States, Canada

Tilia spp.

Lime

Bark canker

United Kingdom

Vitis vinifera

Grape

Root rot

New Zealand

Symptoms

Bleeding Canker of Horse Chestnut:

Dead and dying scaffold branches normally show the first signs of infection. A rusty red or yellow-brown fluid oozes out of recently killed bark. This fluid eventually turns black and crusty.

 

Root Rot, Leaf Spots, Shoot Blight, and Stem Dieback of Ericaceous Woody Ornamentals:

Blight occurs in young tissue (terminal growth). Mature wood is rarely affected. Spots on leafs are surrounded by a dark red margin, eventually causing leaves to fall off. Root and crown rot causes chlorosis, wilting, decreased foliage, and stunting of the plant. In advanced stages of the disease, dieback occurs. Stem necrosis from splash dispersal of soilborne inoculum can occur. P. citrophthora is more important than P. citricola on Pieris spp. P. citricola causes a stem dieback on Rhododendron spp.

 

Root Rot of Walnut:

In California, a complex of Phytophthora species, including P. citricola, P. cactorum, P. cinnamomi, P. citrophthora, P. megasperma, and P. cryptogea, has been found to cause root rot of black walnut. A seedling may be killed if the root system is infected. Root decay and crown rot can occur (Mircetich and Matheron, 1983).

 

Crown and Collar Rot of Avocado:

Disease begins as a canker at the base of the trunk (Figs. 5 and 6). This canker moves so slowly that it can go unnoticed until girdling has occurred and foliage begins to yellow (Zentmyer and Ohr, 1978). The development of cankers is favored by high soil moisture levels. Root rot caused by P. cinnamomi is more common on avocado. Infection of avocado by P. citricola may be predisposed by root pruning and wounding. Susceptibility of wounded trees to disease is seasonally affected and timed with flushes of tree growth. 

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.

 

Chester, K. S. 1932. A comparative study of three Phytophthora diseases of lilac and of their pathogens. J. Arnold Arbor. Harv. Univ. 13:232-269.

 

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.

 

Cooke, D. E. L., Drenth, A., Duncan, J. M., Wagels, G., and Brasier, C. M. 2000. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet. Biol. 30:17-32.

 

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

 

Ho, H. H., and Chang, H. S. 1992. A re-evaluation of Phytophthora species described by K. Sawada in Taiwan. Mycotaxon 43:297-316.

 

Gallegly, M. E., and Hong, C. 2008. Phytophthora: Identifying Species by Morphology and DNA Fingerprints. American Phytopathological Society, St. Paul, MN.

 

Kroon, L. P. N. M., Bakker, F. T., van den Bosch, G. B. M., Bonants, P. J. M., and Flier, W. G. 2004. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNS sequences. Fungal Genet. Biol. 41:766-782.

 

Leonian, L. H. 1925. Physiological studies on the genus Phytophthora. W. Va. Agric. Exp. Stn. Sci. Pap. 11.

 

Leonian, L. H. 1934. Identification of Phytophthora species. W. Va. Agric. Exp. Stn. Bull. 262.

 

Mircetich, S. M., and Matheron, M. E. 1983. Phytophthora root and crown rot of walnut trees. Phytopathology 73:1481-1488.

 

Sawada, K. 1927. Descriptive catalogue of the Formosan fungi III. Dep. Agric. Gov. Res. Inst. Formosa Rep. 27:1-62.

 

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.

 

Sundararaman, S., and Ramakrishnan, T. S. 1928. Foot rot and wilt of Antirrhinums. Mem. Dep. Agric. India Bot. Ser. 16:83-100.

 

Tucker, C. M. 1931. Taxonomy of the genus Phytophthora de Bary. Univ. Mo. Agric. Exp. Stn. Bull. 153:1-208.

 

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.

 

Waterhouse, G. M., and Waterston, J. M. 1966. Phytophthora citricola. CMI Descr. Pathog. Fungi Bact. 114:1-2.

 

Zentmyer, G. A., and Ohr, H. D. 1978. Avocado root rot. Div. Agric. Serv. Univ. Calif. Leaflet 2440.