Gymnosporangium yamadae (Japanese apple rust)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Impact Summary
- Economic Impact
- Social Impact
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Gymnosporangium yamadae Miyabe ex G. Yamada 1904
Preferred Common Name
- Japanese apple rust
International Common Names
- English: apple-juniper rust; cedar rust; cedar-apple rust; rust: apple
- Spanish: roya japonesa del manzano
- French: rouille japonaise du pommier
Local Common Names
- Japan: akahoshi-byo
- GYMNYA (Gymnosporangium yamadae)
Summary of InvasivenessTop of page
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 TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Pucciniomycotina
- Class: Pucciniomycetes
- Order: Pucciniales
- Family: Pucciniaceae
- Genus: Gymnosporangium
- Species: Gymnosporangium yamadae
Notes on Taxonomy and NomenclatureTop of page
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).
DescriptionTop of page
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.
DistributionTop of page 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 TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||CABI/EPPO, 2012; EPPO, 2014|
|-Gansu||Present||IMI, 1994; UK CAB International, 1994; Zhuang, 2005; CABI/EPPO, 2012; EPPO, 2014|
|-Guangxi||Present||IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|-Hebei||Present||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Henan||Present, few occurrences||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Hubei||Present||IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012|
|-Hunan||Present||CABI/EPPO, 2012; EPPO, 2014|
|-Jiangsu||Present||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Jilin||Present||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Liaoning||Present||Guo, 1994; IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Shaanxi||Present||IMI, 1994; UK CAB International, 1994; Zhang et al., 1997; Cao et al., 2000; Zhuang, 2005; CABI/EPPO, 2012; EPPO, 2014|
|-Shandong||Present||Guo, 1989; IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|-Shanxi||Present||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Sichuan||Present||IMI, 1994; UK CAB International, 1994; Chen, 2002; CABI/EPPO, 2012; EPPO, 2014|
|-Xinjiang||Present||Chen, 2002; Zhuang, 2005; CABI/EPPO, 2012|
|-Yunnan||Present||IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|-Zhejiang||Present||IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|Japan||Present||Hiratsuka, 1975; CABI/EPPO, 2012; EPPO, 2014|
|-Hokkaido||Present||Sakuma, 1985; IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|-Honshu||Present||Sakuma, 1985; IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|Korea, DPR||Present||IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|Korea, Republic of||Present||Yun et al., 2009a; IMI, 1994; UK CAB International, 1994; CABI/EPPO, 2012; EPPO, 2014|
|Taiwan||Present||Yen J-m, 1975; Hiratsuka and Chen, 1991; CABI/EPPO, 2012|
|Canada||Present, few occurrences||CABI/EPPO, 2012|
|-Ontario||Present, few occurrences||CABI/EPPO, 2012|
|USA||Present||CABI/EPPO, 2012; EPPO, 2014|
|-Connecticut||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service No. 2011/005.|
|-Delaware||Present||Introduced||Invasive||Yun et al., 2009b; Gregory et al., 2010; EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014|
|-Maine||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014|
|-Maryland||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service 2011/005.|
|-New Hampshire||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service No. 2011/005.|
|-New Jersey||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service No. 2011/005.|
|-New York||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service No. 2011/005.|
|-Pennsylvania||Present||Introduced||Invasive||Yun et al., 2009b; EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014|
|-Rhode Island||Present||EPPO, 2011; CABI/EPPO, 2012; EPPO, 2014||EPPO Reporting Service No. 2011/005.|
|Netherlands||Absent, confirmed by survey||EPPO, 2014||Based on long-term annual surveys.|
|Russian Federation||Restricted distribution||CABI/EPPO, 2012|
|-Russian Far East||Present||CABI/EPPO, 2012|
Risk of IntroductionTop of page
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.
HabitatTop of page
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 ListTop of page
|Terrestrial – Managed||Cultivated / agricultural land||Present, no further details|
|Managed forests, plantations and orchards||Present, no further details|
|Disturbed areas||Present, no further details|
|Urban / peri-urban areas||Present, no further details|
|Terrestrial ‑ Natural / Semi-natural||Natural forests||Present, no further details|
Hosts/Species AffectedTop of page
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 AffectedTop of page
|Juniperus chinensis (Chinese juniper)||Cupressaceae||Main|
|Juniperus chinensis var. kaizuka||Cupressaceae||Main|
|Juniperus chinensis var. sargentii||Cupressaceae||Wild host|
|Juniperus sabina (savin juniper)||Cupressaceae||Wild host|
|Malus baccata (siberian crab apple)||Rosaceae||Wild host|
|Malus domestica (apple)||Rosaceae||Main|
|Malus halliana||Wild host|
|Malus hupehensis (hupeh crab-apple)||Rosaceae||Wild host|
|Malus micromalus||Rosaceae||Wild host|
|Malus platycarpa||Rosaceae||Wild host|
|Malus prunifolia (plum-leaved crab apple)||Rosaceae||Main|
|Malus scheideckeri||Rosaceae||Wild host|
|Malus spontanea||Rosaceae||Wild host|
|Malus toringo (toringo crab-apple)||Rosaceae||Main|
|Malus transitoria||Rosaceae||Wild host|
|Malus yunnanensis||Rosaceae||Wild host|
SymptomsTop of page 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/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal leaf fall|
|Leaves / fungal growth|
|Leaves / honeydew or sooty mould|
|Leaves / wilting|
|Stems / canker on woody stem|
|Stems / galls|
Biology and EcologyTop of page
Nothing is known about the genetics of G. yamadae. This species cannot be grown in culture and has not been sequenced.
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.
Means of Movement and DispersalTop of page
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.
Impact SummaryTop of page
ImpactTop of page The rust is an important pest of apple in northern Japan, causing defoliation.
Economic ImpactTop of page
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).
Social ImpactTop of page
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 FactorsTop of page Invasiveness
- Invasive in its native range
- Proved invasive outside its native range
- Abundant in its native range
- Highly adaptable to different environments
- Host damage
- Negatively impacts agriculture
- Parasitism (incl. parasitoid)
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
DiagnosisTop of page
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).
Detection and InspectionTop of page 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.
Similarities to Other Species/ConditionsTop of page
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.
Prevention and ControlTop of page
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.
ReferencesTop of page
Chen MM, 2002. Forest fungi phytogeography: Forest fungi phytogeography of China, North America, and Siberia and international quarantine of tree pathogens. Sacramento, USA: Pacific Mushroom Research and Education Center, 469 pp.
EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
Gregory NF; Bischoff JF; Dixon LJ; Ciurlino R, 2010. First report of the telial stage of Japanese apple rust on Juniperus chinensis in North America and the aecial stage on Malus domestica. Plant Disease, 94(9):1169. http://apsjournals.apsnet.org/loi/pdis
Harada Y; Sawamura K, 1980. Basitac (Mepronil), a promising agent for preventing basidiospore production by galls of Japanese apple rust (Gymnosporangium yamadp) on junipers. Annual Report of the Society of Plant Protection of North Japan, No. 31:84
Hiratsuka N; Chen ZC, 1991. A list of Uredinales collected from Taiwan. Transactions of the Mycological Society of Japan, 32:3-22.
Hiratsuka N; Sato S, 1973. Conclusive summary of the positive results of the inoculation experiments with heteroecious species of the Japanese rust fungi (1937-1973). Reports of the Tottori Mycological Institute (Japan), 10:141-154.
Hiratsuka N; Sato S; Kakishima M, 1984. Summary of the positive results of inoculation experiments with the heteroecious rust fungi in Japan (1899-1983). Reports of the Tottori Mycological Institute, No.22:9-41.
Hiratsuka N; Sato S; Katsuya K; Kakishima M; Hiratsuka Y; Kaneko S; Ono Y; Sato T; Harada Y; Hiratsuka T; Nakayama K, 1992. The Rust Flora of Japan. Takezono, Ibaraki, Japan: Tsukuba Shuppankai, 1205 pp.
Kern FD, 1973. A Revised Taxonomic Account of Gymnosporangium. University Park, USA: Penn State University Press.
OEPP/EPPO, 2000. EPPO Standards PM 1/2(8) EPPO A1 and A2 lists of quarantine pests. In: EPPO Standards PM 1, General Phytosanitary Measures. Paris, France: EPPO, 5-17.
Ohyama H; Wada T; Ishikawa H; Chiba K, 1988. HF-6305, a new triazole fungicide. Brighton Crop Protection Conference. Pests and Diseases - 1988. Vol.2 Thornton Heath, UK; British Crop Protection Council, 519-526
Peterson RS, 1967. Studies of juniper rusts. The West Madrono, 19: 9-91.
Smith IM; McNamara DG; Scott PR; Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref.
Yen J-m, 1975. Étude sur les Champignons parasites du Sud-Est Asiatique. XXIV. Les Urédinées de Formose. Revue de Mycologie, 39:251-267.
Yun HY; Lee SK; Lee KJ, 2005. Identification of aecial host ranges of four Korean Gymnosporangium species based on the artificial inoculation with teliospores obtained from various forms of telia. Plant Pathology Journal, 21:310-316.
Yun HY; Minnis AM; Rossman AY, 2009. First report of Japanese apple rust caused by Gymnosporangium yamadae on Malus spp. in North America. Plant Disease, 93(4):430. http://apsjournals.apsnet.org/loi/pdis
Yun HyeYoung; Hong SoonGyu; Rossman AY; Lee SeungKyu; Lee KyungJoon; Bae KyungSook, 2009. The rust fungus Gymnosporangium in Korea including two new species, G. monticola and G. unicorne. Mycologia, 101(6):790-809. http://msafungi.org
ContributorsTop of page
02/05/08 Updated by:
Distribution MapsTop of page
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