Gymnosporangium yamadae
(Japanese apple rust)

Pictures

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

Identity

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

EPPO code

• GYMNYA (Gymnosporangium yamadae)

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

• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Basidiomycota
•             Subphylum: Pucciniomycotina
•                 Class: Pucciniomycetes
•                     Order: Pucciniales
•                         Family: Pucciniaceae
•                             Genus: Gymnosporangium
•                                 Species: Gymnosporangium yamadae

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).

Description

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).

Distribution

Distribution Table

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.

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.

Habitat

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

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

Symptoms

List of Symptoms/Signs

Biology and Ecology

Genetics

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).

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.

Impact Summary

Impact

Economic Impact

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 Impact

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

• Host damage
• Negatively impacts agriculture

• Parasitism (incl. parasitoid)
• Pathogenic

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

Diagnosis

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 Inspection

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.

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.

References

CABI/EPPO, 2012. Gymnosporangium yamadae. [Distribution map]. Distribution Maps of Plant Diseases, No.April. Wallingford, UK: CABI, Map 528 (Edition 3).

Cao ZhiMin; Li ZhenQi; Zhuang JianYun, 2000. Uredinales from the Qinling Mountains. Mycosystema, 19(1):13-23.

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.

Cummins GB; Hiratsuka Y, 1983. Illustrated genera of rust fungi. Revised edition. Minnesota, USA: American Phytopathological Society, 152 pp.

EPPO, 2006. Gymnosporangium spp. (non-European). Bulletin OEPP/EPPO Bulletin, 36(3):441-446. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=epp

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

Guo L, 1989. Uredinales of Shennongjia, China. In: Fungi and Lichens of Shennongjia. Beijing, China: World Publishing Corporation, 107-156.

Guo YN, 1994. The integrated management of the rust of apple (Gymnosporangium yamadae Miyobe). Bulletin of Agricultural Science and Technology, No. 4:28.

Ha YM; Shim KK, 1995. Selection of new crabapple cultivars by cross and open pollination for landscape use. Journal of the Korean Society for Horticultural Science, 36(1):132-149; 15 ref.

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, 1975. Notes on the specific name of the cedar apples of pears and apples in Japan. Transactions of the Mycological Society of Japan, 16(1):90-92

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.

Kim SC; Kim CH, 1980. Studies on the disease of pear rust caused by Gymnosporangium haraeanum Sydow. I. Some ecological investigation of inoculum source. Korean Journal of Plant Pathology, 19:39-44.

Laundon G, 1977. Gymnosporangium yamadae. CMI Descriptions of Pathogenic Fungi and Bacteria No. 550. Wallingford, UK: CAB International.

Lee JC; Lim MS, 1984. Prevention experiment of disease in horticultural plants. Chungnam Rural Development Administration, Research Reports. 414-418.

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.

Sakuma T, 1985. On the pathogenic races of Gymnosporangium yamadp on apple. Annals of the Phytopathological Society of Japan, 51(2):139-144

Sinclair WA; Lyon H, 2005. Diseases of Trees and Shrubs. Second edition. Ithaca, USA: Cornell University Press, 660 pp.

Smith IM; Dunez J; Lelliott RA; Phillips DH; Archer SA(Editors), 1988. European handbook of plant diseases. Oxford, UK: Blackwell Scientific Publications.

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.

Tanaka T, 1922. New Japanese fungi. Notes and translations XII. Mycologia, 14:282-287.

UK CAB International, 1994. Gymnosporangium yamadae. [Distribution map]. Distribution Maps of Plant Diseases, September (Edition 2). Wallingford, UK: CAB International, Map 528.

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, 2003. Thesis for the degree of Master of Science. Seoul, Korea: Seoul National University.

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

Zhang N; Zhuang JY; Wei SX, 1997. Fungal flora of the Daba Mountains: Uredinales. Mycotaxon, 61:49-79.

Zhuang WY, 2005. Fungi of Northwestern China. Ithaca, USA: Mycotaxon Ltd, 430 pp.

Distribution References

CABI, Undated. Compendium record. Wallingford, UK: CABI

CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

CABI/EPPO, 2012. Gymnosporangium yamadae. [Distribution map]. In: Distribution Maps of Plant Diseases, Wallingford, UK: CABI. Map 528 (Edition 3).

Cao ZhiMin, Li ZhenQi, Zhuang JianYun, 2000. Uredinales from the Qinling Mountains. Mycosystema. 19 (1), 13-23.

Chen M M, 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, 2020. EPPO Global database. In: EPPO Global database, Paris, France: EPPO.

Gregory N F, Bischoff J F, Dixon L J, 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 DOI:10.1094/PDIS-94-9-1169B

Guo L, 1989. Uredinales of Shennongjia, China. In: Fungi and Lichens of Shennongjia. Beijing, China: World Publishing Corporation. 107-156.

Guo Y N, 1994. The integrated management of the rust of apple (Gymnosporangium yamadae Miyobe). Bulletin of Agricultural Science and Technology. 28.

Hiratsuka N, 1975. Notes on the specific name of the cedar apples of pears and apples in Japan. Transactions of the Mycological Society of Japan. 16 (1), 90-92.

Hiratsuka N, Chen ZC, 1991. A list of Uredinales collected from Taiwan. In: Transactions of the Mycological Society of Japan, 32 3-22.

Sakuma T, 1985. On the pathogenic races of Gymnosporangium yamadae on apple. Annals of the Phytopathological Society of Japan. 51 (2), 139-144. DOI:10.3186/jjphytopath.51.139

UK, CAB International, 1994. Gymnosporangium yamadae. [Distribution map]. In: Distribution Maps of Plant Diseases, Wallingford, UK: CAB International. Map 528.

Yen J-m, 1975. (Étude sur les Champignons parasites du Sud-Est Asiatique. XXIV. Les Urédinées de Formose). In: Revue de Mycologie, 39 251-267.

Yun H Y, Minnis A M, Rossman A Y, 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 DOI:10.1094/PDIS-93-4-0430A

Yun HyeYoung, Hong SoonGyu, Rossman A Y, 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. DOI:10.3852/08-221

Zhang N, Zhuang J Y, Wei S X, 1997. Fungal flora of the Daba Mountains: Uredinales. Mycotaxon. 49-79.

Zhuang W Y, Guo L, Guo S Y, Guo Y L, Mao X L, Sun S X, Wei S X, Wen H A, Yu Z H, Zhang X Q, Zhuang J Y, 2005. Fungi of Northwestern China. [ed. by Zhuang W Y]. Ithaca, NY, USA: Mycotaxon Ltd. 430 pp.

Contributors

02/05/08 Updated by:

Distribution Maps