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2 May 2008

Gymnosporangium yamadae (Japanese apple rust)

Datasheet Types: Pest, Invasive species


This datasheet on Gymnosporangium yamadae covers Identity, Overview, Distribution, Dispersal, Hosts/Species Affected, Diagnosis, Biology & Ecology, Impacts, Prevention/Control, Further Information.


Preferred Scientific Name
Gymnosporangium yamadae Miyabe ex G. Yamada 1904
Preferred Common Name
Japanese apple rust
International Common Names
apple-juniper rust
cedar rust
cedar-apple rust
rust: apple
roya japonesa del manzano
rouille japonaise du pommier
Local Common Names
EPPO code
GYMNYA (Gymnosporangium yamadae)


Telia (big gall) of G. yamadae on on Juniperus chinensis var. kaizuka Hort.
Telia (big gall) of G. yamadae on on Juniperus chinensis var. kaizuka Hort.
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Telia (big gall) of G. yamadae on Juniperus chinensis.
Telia (big gall) of G. yamadae on Juniperus chinensis.
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia of G. yamadae on Malus toringo (Siebold) Siebold ex de Vriese
Aecia of G. yamadae on Malus toringo (Siebold) Siebold ex de Vriese
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aecia of G. yamadae on Malus prunifolia Borkh.
Aecia of G. yamadae on Malus prunifolia Borkh.
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospore and peridial cells of G. yamadae on Malus sieboldii. Note scale. (Original X400)
Aeciospore and peridial cells
Aeciospore and peridial cells of G. yamadae on Malus sieboldii. Note scale. (Original X400)
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Peridial cells of G. yamadae on Malus sieboldi. Note scale. (Original X400)
Peridial cells
Peridial cells of G. yamadae on Malus sieboldi. Note scale. (Original X400)
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Aeciospore of G. yamadae on Malus sieboldii Note scale. (Original X400)
Aeciospore of G. yamadae on Malus sieboldii . Note scale. (Original X400)
USDA-ARS/Systematic Mycology & Microbiology Laboratory
Teliospores of G. yamadae on Juniperus chinensis var. sargentii. (Original X400) Note scale bar.
Teliospores of G. yamadae on Juniperus chinensis var. sargentii. (Original X400) Note scale bar.
USDA-ARS/Systematic Mycology & Microbiology Laboratory

Summary of Invasiveness

G. yamadae belongs to the Uredinales, which includes the rust fungi, all of which cause diseases on plants. At present, G. yamadae, which is a serious pathogen of domestic apples [Malus domestica], has limited distribution.

Taxonomic Tree

This content is currently unavailable.

Notes on Taxonomy and Nomenclature

This fungus was originally named by Yamada in 1904, without a description. There are no additional, legitimate synonyms of this species. For further information on the taxonomy of Gymnosporangium species, see Kern (1973).


Aecia foliicolous, then hypophyllous, also caulicolous, fructicolous, roestelioid, 2-8 mm high. Peridium balanoid, dehiscent at apex, retaining a cornute shape; peridial cells long-narrow rhomboid to linear-rhomboid, verrucose with long papillae, pale-yellow, 59-115 µm long, outer walls smooth, inner and side walls sparsely echinulate; aeciospores globoid, 16-26 x 18-27 µm, walls dark-yellow, 1.0-2.5 µm thick.
Telia foliicolous or caulicolous, producing globoid swellings or small galls, sori cylindric-acuminate, 1-3 mm diameter, in large galls, sori tongue-shaped, 5-8 mm high or more, orange; teliospores two-celled, oblong, ellipsoid or obovoid, 15-28 x 32-56 µm, walls 0.8-2.0 µm, yellow or orange, with two pores near septum and one pore toward apex in upper cell, frequently with an obtuse hyaline, papilla at the apex.
On Juniperus chinensis, G. yamadae causes swelling of the stems, and the teliospores are produced on tongue-shaped yellowish-red telial masses, 3-5 mm long. The teliospores are two-celled, ellipsoid, 15-24 x 32-45 µm, wall 1-1.5 µm thick. On apple [Malus spp.], the aecia are roestelioid, hypophyllous with the peridia long-tubular or horn-shaped, 3-8 mm high, lacerate at the sides. The aeciospore mass is chestnut-brown. Aeciospores are 17-28 µm diameter.
For more detailed descriptions consult Kern (1973), Laundon (1977), Hiratsuka et al. (1992), Yun (2003) and Yun et al. (2005).


The rust was confined to the Far East (mainly China and Japan) until recently, when it was reported in Delaware and Pennsylvania, USA (Yun et al., 2009b).

Distribution Map

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Distribution Table

This content is currently unavailable.

Risk of Introduction

G. yamadae is one of the non-European Gymnosporangium species listed as A1 quarantine organisms by EPPO (OEPP/EPPO, 2000). It is also listed as a quarantine pest by IAPSC. Other species of Gymnosporangium already occur on apples [Malus spp.] in other parts of the world, for example, Gymnosporangium tremelloides in Europe, with Juniperus communis as the alternate host (Smith et al., 1988). The severity of infection on apples is determined by the proximity of infected alternate hosts and, in practice, G. tremelloides is of very minor importance. G. yamadae appears to be a more damaging species than its European counterpart and could very probably establish in Europe and other apple-growing areas around the world.
The telial host of G. yamadae, Juniperus chinensis, occurs in native forests in China, Japan and Korea, but it is also cultivated in gardens (Yun et al., 2005). The alternate hosts, Malus baccata, Malus domestica, Malus prunifolia and Malus toringo are often planted in the same place with J. chinensis. With the increased movement of juniper as nursery stock and cultivated apple as both nursery stock and fruits for consumption, the risk of introduction is high. This rust was recently reported in the USA (Delaware, Pennsylvania) in the aecial state (Yun et al., 2009b). Bonsai junipers present a likely pathway for entry of G. yamadae.

Means of Movement and Dispersal

Natural Dispersal (Non-Biotic)

The infective aeciospores and basidiospores of G.yamadae are spread from plant to plant primarily by windblown spores and rain. After rain, during the spring, the basidiospores are windborne and may be carried approximately 3 to 5 km to the aecial host. Infection of aeciospores to the telial host is also windborne in dry weather during the summer and early autumn.

Movement in Trade

In international trade, all plants of Juniperus chinensis from the Far East are liable to be infected by G. yamadae. Like other Gymnosporangium species, G. yamadae can be latent during the winter (the probable importing period) and may not be detectable at pre-export phytosanitary certification. Infection may also have remained latent on the plants in the previous growing season. Introduction of G. yamadae on commercial importations of plants of apple [Malus spp.] is very unlikely as infection is not persistent in the dormant stage. Fruits are rarely infected.

Plant Trade

Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
fungi/fruiting bodies
Fruits (inc. pods)
fungi/fruiting bodies
fungi/fruiting bodies

Hosts/Species Affected

G. yamadae has high host specificity. The telial stage is known on Juniperus sect. Sabina and the aecial stage is restricted to species of Malus. The host range of G. yamadae was confirmed with telia on Juniperus chinenesis and the aecia on Malus halliana, Malus pumila var. domestica, and Malus sieboldii by artificial inoculation experiments (Hiratsuka et al., 1992).

Host Plants and Other Plants Affected

HostFamilyHost statusReferences
Juniperus chinensis (Chinese juniper)CupressaceaeMain 
Juniperus chinensis var. kaizukaCupressaceaeMain
Juniperus chinensis var. sargentiiCupressaceaeWild host 
Juniperus sabina (savin juniper)CupressaceaeWild host 
Malus baccata (siberian crab apple)RosaceaeWild host 
Malus domestica (apple)RosaceaeMain
Malus halliana Wild host 
Malus hupehensis (hupeh crab-apple)RosaceaeWild host 
Malus micromalusRosaceaeWild host 
Malus platycarpaRosaceaeWild host 
Malus prunifolia (plum-leaved crab apple)RosaceaeMain 
Malus scheideckeriRosaceaeWild host 
Malus spontaneaRosaceaeWild host 
Malus toringo (toringo crab-apple)RosaceaeMain
Yun et al. (2009)
Malus transitoriaRosaceaeWild host 
Malus yunnanensisRosaceaeWild host 


On Juniperus chinensis, G. yamadae causes fusiform swellings on stems that can produce telial horns under wet conditions. On apple [Malus spp.], the most conspicuous symptoms are the appearance of the aecia and pycnia on the leaves. On susceptible cultivars, G. yamadae can cause very severe defoliation. Infections on fruits are rare.

List of Symptoms/Signs

Symptom or signLife stagesSign or diagnosisDisease stage
Plants/Leaves/abnormal colours   
Plants/Leaves/abnormal forms   
Plants/Leaves/abnormal leaf fall   
Plants/Leaves/fungal growth   
Plants/Leaves/honeydew or sooty mould   
Plants/Stems/canker on woody stem   


Rust fungi are obligate parasites that only infect specific plant genera or species (Sinclair and Lyon, 2005). In G. yamadae, the aecial stage only occurs in one species of Malus (Hiratsuka and Sato, 1973; Kern 1973; Hiratsuka et al., 1984; Hiratsuka et al., 1992; Yun et al., 2005). Eighteen other species of Gymnosporangium produce their aecial states on Malus. These species are difficult to differentiate except using microscopic and molecular characteristics. A diagnostic protocol for G. yamadae is given in OEPP/EPPO (2006).

Similarities to Other Species/Conditions

G. yamadae is morphologically similar to Gymnosporangium globosum, American hawthorn rust. Specific differences exist in the shape and size of the teliospores, aecia and peridial cells. The aecial and peridial cells of G. yamadae are larger than those of G. globosum whereas the telia of G. globosum are larger than those of G. yamadae.


G. yamadae occurs as a perennial pathogen on juniper [Juniperus] and produces telia on galls and swellings on the host (Sinclair and Lyon, 2005).

Habitat List

CategorySub categoryHabitatPresenceStatus
TerrestrialTerrestrial – ManagedCultivated / agricultural landPresent, no further details 
TerrestrialTerrestrial – ManagedManaged forests, plantations and orchardsPresent, no further details 
TerrestrialTerrestrial – ManagedDisturbed areasPresent, no further details 
TerrestrialTerrestrial – ManagedUrban / peri-urban areasPresent, no further details 
TerrestrialTerrestrial ‑ Natural / Semi-naturalNatural forestsPresent, no further details 

Biology and Ecology


Nothing is known about the genetics of G. yamadae. This species cannot be grown in culture and has not been sequenced.

Reproductive Biology

Rust fungi are obligate parasites of living plants in nature, with a strong host-specialization. Their life cycle is completed through alternating between two sets of plant hosts. Like all species of Gymnosporangium, G. yamadae has the fruiting structures: spermagonia; aecia; and telia, but lacks urediniospores.
Telia develop on swollen stems that may become galls on juniper [Juniperus] trees. Telia develop on sori that extrude telial horns. When telial horns absorb water, they become swollen, turn orange-brown, and are gelatinous in the spring; the teliospores germinate producing basidia and basidiospores. The basidiospores are dispersed by air and infect their rosaceous hosts. Basidiospores germinate on apple leaf tissue and penetrate cells directly, producing haploid mycelia, which form spermogonia that open at the upper surface. After the spermatia fertilize compatible, receptive hypha, aecial structures are produced on the opposite leaf surface. Aeciospores are windborne and infect the telial host during the summer and autumn.

Physiology and Phenology

The production of basidiospores on telia occurs in spring, especially during warm, wet weather usually after rain. After rain, the basidiospores are carried by the wind to apple [Malus spp.] trees where they infect the leaves. The teliospores on galls die after producing basidiospores, but may remain attached to the telial host for several years. When the same trees are observed for several years, damage to the host can be serious (Harada and Sawamura, 1980). By the following summer or early autumn, aeciospores have developed on the apple leaves and are carried by wind to juniper trees. This occurs primarily during dry weather when the aecia crack and break into pieces.
For more information see Tanaka (1922) and Peterson (1967).

Impact Summary

Environment (generally)Negative


The rust is an important pest of apple in northern Japan, causing defoliation.

Impact: Economic

Many species of rust fungi are the cause of internationally important plant diseases. G. yamadae, causing Japanese apple rust, may debilitate plants, which wither and die due to heavy infection of the telial host. This rust may reduce fruit yield by inhibiting photosynthesis and increasing respiration due to infection (Kim and Kim, 1980).

Impact: Social

Fungi in the genus Gymnosporangium cause diseases, so-called ‘cedar rust’ or more specifically ‘cedar-apple rust’ (Kern, 1973). In recent years, there has been renewed interest in these fungi because many of the hosts are popular as landscape trees and ornamental plants (Kim and Kim, 1980).

Risk and Impact Factors


Invasive in its native range
Proved invasive outside its native range
Abundant in its native range
Highly adaptable to different environments

Impact outcomes

Host damage
Negatively impacts agriculture

Impact mechanisms

Parasitism (incl. parasitoid)

Likelihood of entry/control

Difficult to identify/detect as a commodity contaminant
Difficult to identify/detect in the field
Difficult/costly to control

Detection and Inspection

The inspection of imported Juniperus that may have latent infection is particularly important. A secure quarantine procedure would involve retention under closed conditions for 2 years and frequent inspection from January-May.

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Other Gymnosporangium species can be adequately controlled on apples by routine fungicide applications (for example, sterol-inhibiting fungicides), and this probably applies to G. yamadae. In Japan, G. yamadae was mentioned among the most important target pests for a new triazole fungicide (Ohyama et al., 1988). Mepronil can be used to control the disease on juniper [Juniperus] (Harada and Sawamura, 1980). In China, integrated management systems are proposed (Guo, 1994).
Most economically important apple cultivars are resistant to species of Gymnosporangium including G. yamadae as determined through inoculation experiments (Lee and Lim, 1984; Ha and Shim, 1995). However, eight apple cultivars including Fugi apple, a favourite cultivar in Asia, had a 35.5% infection rate, whereas other apple cultivars have a 15-20% infection rate (Lee and Lim, 1984). Sinclair and Lyon (2005) reported a summary of the junipers resistant to cedar-apple rust.
Suppression of the alternate host (Juniperus chinensis) within a certain radius of orchards is recommended, but may be difficult as it is often present in private gardens.

As infection of Juniperus is systemic in stems and evergreen leaves, no chemical treatment is likely to be completely effective to treat imported plants found to be infected. It is most unlikely that infection from the telial stage could be carried on packing materials and the risk is virtually confined to infected plants.

Countries should prohibit importation of plants for planting and cut branches of J. chinensis from countries where G. yamadae occurs, unless they are held in quarantine for a full growing season and found free from G. yamadae. Plants for planting and cut branches of Malus from the Far East should be dormant and free from leaves.


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