EPPO Datasheet: Gymnosporangium asiaticum
Taxonomic position: Fungi: Basidiomycota: Pucciniomycotina: Pucciniomycetes: Pucciniales: Gymnosporangiaceae
Other scientific names: Gymnosporangium chinense Long, Gymnosporangium haraeanum Sydow & P. Sydow, Gymnosporangium koreense (Hennings) H.S. Jackson, Gymnosporangium photiniae (Hennings) F. Kern, Gymnosporangium spiniferum Sydow & P. Sydow, Gymnosporangium unicorne H.Y. Yun, Roestelia koreaensis Hennings, Roestelia photiniae Hennings
Common names in English: leaf rust of Japanese pear, leaf rust of juniper, rust of oriental pear
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Notes on taxonomy and nomenclature
The genus Gymnosporangium was established to accommodate G. fuscum on Juniperus sabina. To date, over 70 species of this genus have been reported worldwide (Zhao et al., 2020). This genus has long been classified in the family Pucciniaceae due to its pedicellate teliospores and Group V spermogonia (Hiratsuka & Hiratsuka, 1980; Hiratsuka et al., 1992; Cummins & Hiratsuka, 2003). However, recent phylogenetic studies suggested its phylogenetic distinction from core Pucciniaceae (Puccinia/Uromyces) (Maier et al., 2003; Aime et al., 2006). Thus, a new family, Gymnosporangiaceae, was proposed to accommodate the genus Gymnosporangium (Zhao et al., 2020), and such taxonomic treatment was widely accepted thereafter (Aime & McTarggart, 2021).
Among these Gymnosporangium species, G. asiaticum was reported as a causal agent of Japanese pear rust diseases. Historically, this species was first described by Sydow (1899) as Gymnosporangium japonicum at Komaba, Tokyo. Miyabe (1903) considered that the Japanese pear rust fungus was a new species called G. asiaticum, differing from G. japonicum, and that its aecia also occurred on Cydonia vulgaris and Chaenomeles speciosa, and its telia on leaves of Juniperus chinensis. However, he did not publish a description of this species in any form. Later Yamada (1904) validly described this species based on collections by K. Hara at Kawaue-mura, Gifu prefecture of Japan. Despite the existence of the valid name G. asiaticum, Sydow and Sydow (1912) renamed the leaf-inhabiting form observed on juniper leaves as G. haraeanum, based on the collection of Hara from Mino, Gifu prefecture, Japan. However, Hara confirmed that the alternate host (aecial host) of this rust fungus was pear (Pyrus spp.), while Ito further added Photinia villosa as an aecial host. Previously the rust fungus on Photinia villosa in Japan was first described under the name of Roestelia photiniae, and Kern (1911) classified it into the genus Gymnosporangium based on aecial similarities. Although G. photiniae was proposed, this species showed high morphological similarities with G. asiaticum and G. haraeanum. Thus, Ito (1950) treated G. haraeanum and G. photiniae as synonyms of G. asiaticum due to nomenclature priority. Moreover, Long (1914) described a new species, Gymnosporangium chinense based upon plant material imported from Japan in a nursery in Connecticut (US). The aecial state of this fungus was first described by Hennings (1899) based upon a specimen collected by O. Warburg on Pyrus sp. in Korea (Yun et al., 2019). In the next year, Dietel (1900b) identified the aecial state of this fungus on Pyrus serotina, Cydonia vulgaris and Photinia laevis var. villosa which were collected by S. Kusano in Tokyo, and called it Gymnosporangium confusum. In 1912, Sydow and Sydow regarded the aecial state of this fungus on leaves of Cydonia vulgaris as a new species giving it the name Gymnosporangium spiniferum, based upon a specimen which was collected by Sakurai (Hiratsuka et al., 1992). Yun et al. (2009) also reported a new species, G. unicorne, based on the morphological characteristics of its telia. Hitherto, these seven Gymnosporangium species, G. chinense, G. haraeanum, G. japonicum, G. koreense, G. photiniae, G. spiniferum and G. unicorne were frequently regarded as synonyms of G. asiaticum (Kern 1973, Hiratsuka et al., 1992). As a result of systematic studies of type materials, all of these species, with the exception of G. japonicum, were confirmed to be conspecific with G. asiaticum (Yun et al., 2009). In 2020, Zhao et al. (2020) designated a lectotype specimen of G. asiaticum according to Yamada (1904), and an epitype specimen was also selected. Both morphological and molecular data were obtained from those type materials. Phylogenetic studies confirmed the species delimitation of G. asiaticum, and their results agreed with the taxonomic treatment of Yun et al. (2009), who treated G. chinense, G. haraeanum, G. koreense and G. spiniferum as synonyms of G. asiaticum. Moreover, G. unicorne, which had been proposed as a new species by Yun et al. (2009), was also confirmed to be conspecific to G. asiaticum through molecular phylogenetic studies (Zhao et al., 2020). In addition, G. taianum on Cupressus duclouxiana, which has aecial hosts on Chaenomeles, Crataegus, Photina and telial hosts on Juniperus species and their varieties, was found to be conspecific to G. asiaticum. The phylogenetic relationships of G. asiaticum with other Gymnosporangium species have already been studied, and G. asiaticum was shown to be phylogenetically close to G. kanas, G. niitakayamense and G. hunglongense (Zhao et al., 2020).
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EPPO Code: GYMNAS
The most important aecial host of G. asiaticum is Japanese pear (Pyrus pyrifolia), and possibly other Asian pear species. European pear (P. communis) and quince (Cydonia oblonga) are recorded as hosts, but there is little information to suggest that they are significant hosts. Tai (1933) noted that, in China, most foreign pear cultivars were immune; a few were slightly susceptible, but much less than Japanese pear (the cultivars concerned are not currently grown in Europe). In Japan, neither of the two races of the fungus described by Sakuma (1992) gave more than tiny, limited lesions on P. communis. Other hosts, in the subfamily Pomoideae of the family Rosaceae, are Chaenomeles, Crataegus and Photinia. The telial hosts in Asia are Juniperus chinensis and the closely related J. procumbens, which are not native to Europe. The former is widely grown as an ornamental tree or as a bonsai plant. In western North America, the alternate host is the introduced species, J. chinensis (Ziller, 1974). Through literature review and comprehensive taxonomic studies, the host range and their geographic distributions were revised and illustrated in Zhao et al. (2020).Host list: Chaenomeles cathayensis, Chaenomeles japonica, Chaenomeles lagenaria, Chaenomeles x superba, Crataegus cuneata, Crataegus pinnatifida, Crataegus wilsonii, Cupressus duclouxiana, Cydonia oblonga, Juniperus chinensis var. sargentii, Juniperus chinensis, Juniperus excelsa, Juniperus procumbens, Juniperus sabina, Juniperus scopulorum, Juniperus squamata, Juniperus tibetica, Juniperus virginiana, Malus asiatica, Malus domestica, Malus ioensis, Malus prunifolia, Malus spectabilis, Malus toringo, Pourthiaea villosa, Pseudocydonia sinensis, Pyrus betulifolia, Pyrus bretschneideri, Pyrus calleryana, Pyrus communis, Pyrus fauriei, Pyrus lindleyi, Pyrus pyrifolia var. culta, Pyrus pyrifolia, Pyrus serrulata, Pyrus ussuriensis
GEOGRAPHICAL DISTRIBUTION 2022-09-07
Gymnosporangium asiaticum was first discovered in Japan, and it has since spread throughout Asia, including China, Japan, and South Korea. Zhuang et al. (2012) and Zhao et al. (2020) provided detailed geographic distributions of this species in China. Hiratsuka et al. (1992) documented the regional range of the species in Japan. Yun et al. (2009) listed detailed reports of this species from South Korea and the United States. In the EPPO region, G. asiaticum has been recorded only in the Russian Far East (Azbukina, 1984), and this single record has not been confirmed by more recent ones.EPPO Region: Russia (Far East)
Asia: China (Anhui, Beijing, Chongqing, Fujian, Gansu, Guangdong, Guangxi, Guizhou, Hebei, Heilongjiang, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Jilin, Liaoning, Neimenggu, Ningxia, Shaanxi, Shandong, Shanxi, Sichuan, Xianggang (Hong Kong), Xinjiang, Xizhang, Yunnan, Zhejiang), Japan (Hokkaido, Honshu, Kyushu, Ryukyu Archipelago, Shikoku), Korea Dem. People's Republic, Korea, Republic, Taiwan
North America: United States of America (California, Connecticut, New York, Oregon, Washington, Wisconsin)
Gymnosporangium asiaticum, like other Gymnosporangium spp., is heteroecious in that it requires Juniperus and rosaceous hosts of the subfamily Pomoideae to complete its life cycle. Telia are produced on stems and leaves of J. chinensis in the spring. In moist conditions, the telia germinate in situ and produce basidiospores which are dispersed and are able to infect nearby Pyrus pyrifolia or other rosaceous hosts. Infection of J. chinensis by G. asiaticum persists for more than 1 year; indeed, infected twigs are reported to release basidiospores over many years (Aldwinckle, 1990).
Infection from basidiospores gives rise to pycnia on the upper surface of Pyrus leaves; they are visible from late spring to early summer. Lee (1990a) has studied the conditions needed for infection of P. pyrifolia leaves by sporidia from J. chinensis. Later, aeciospores are produced inside tubular protective sheaths (peridia) on the underside of the leaf. The aeciospores are released when the peridium ruptures and can be transported by the wind over long distances to reach J. chinensis. After germinating on J. chinensis, an overwintering latent mycelium is produced. Infection of Pyrus does not persist after infected leaves have fallen. The telial state appears on J. chinensis in the spring to begin the life cycle again. For more information see Tanaka (1922), Peterson (1967).
DETECTION AND IDENTIFICATION 2022-09-07
On Juniperus chinensis, telia are produced on leaves and green stems (see Morphology). On Pyrus pyrifolia, the most conspicuous symptoms are the appearance of the aecia and pycnia on the leaves (see Morphology).
On Aecial host:
Aecia foliicolous and caulicolous, hypophyllous, roestelioid; peridium tubular, lacerating at apex or spreading, 4–7 mm high, peridial cells linear-rhomboid, 55–103 × 18–31 µm, outer walls smooth, inner walls small papillae and side walls moderately rugose; aeciospores globoid, ovoid, large coronate, 18–26 × 14–22 µm, walls yellowish, 1.0–2.0 µm thick.
On Telial host:
Uredinia absent. Telia foliicolous or on green stems, developing on witches’ broom but without causing swelling on stem, aggregated bluntly conical, hemispherical, pulvinate or somewhat wedge-shaped; 2–6 mm high, brownish orange; teliospores 2-celled, broadly to narrowly ellipsoid, 31–50 × 16–27 µm, walls 1.0–2.5 mm, pale orange to orange, pores 1 or 2 near septum or 1 apical in upper cell; pedicels cylindrical, hyaline, 2.5–5.0 µm diam.
Details can be found in Zhao et al. (2020).
Detection and inspection methods
The inspection of imported Juniperus which may have latent infection is particularly important. A secure quarantine procedure would involve retention under closed conditions for 2 years and frequent inspection during January-May. A DNA barcode using concatenated data of rDNA ITS and LSU has already been used for detection of G. asiaticum, and Duan et al. (2020) have successfully detected G. asiaticum from Juniperus chinensis imported from Japan.
The EPPO Diagnostic Protocol for Gymnosporangium spp. (non-European) provides recommendations on how to detect and identify the fungus (EPPO, 2006). In addition, detection using rDNA ITS and LSU sequence data according to Duan et al. (2020) provides a reliable molecular diagnostic method for this pathogen.
PATHWAYS FOR MOVEMENT 2022-09-07
Under natural conditions, spread of G. asiaticum is ensured by basidiospore dispersal to rosaceous hosts, and by wind-borne aeciospores to Juniperus chinensis. Pyrus pyrifolia trees within 100 m radius of a J. chinensis tree are at high risk of infection, and up to 1000 m in windy situations (Unemoto et al., 1989). In international trade, plants of J. chinensis from the Far East (especially bonsai plants) are liable to be infected by G. asiaticum. G. asiaticum has been intercepted on bonsai Juniperus from Japan and Hong Kong (Duan et al., 2020, EFSA, 2018; Henderson, 2020). As is the case for other Gymnosporangium spp., G. asiaticum can be latent during 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. asiaticum on commercial importations of plants of P. pyrifolia or other rosaceous hosts is very unlikely as infection is not persistent in the dormant stage. Fruits are usually not infected.
PEST SIGNIFICANCE 2022-09-07
Gymnosporangium asiaticum is reported to be a serious pathogen of Pyrus pyrifolia in the Far East. It is also, on its alternate host, one of the most important and widely distributed fungal pathogen of urban ornamentals (Juniperus chinensis) in China (Zhang, 1990). There is no indication that G. asiaticum has any practical importance in North America, nor that it causes significant disease of any rosaceous host other than P. pyrifolia.
As for some other Gymnosporangium spp., some success against G. asiaticum has been achieved with sterol-inhibiting fungicides, e.g. myclobutanil (Lee, 1990b). In Japan, G. asiaticum was mentioned among the most important target pests for a new triazole fungicide (Ohyama et al., 1988). Differences in susceptibility of P. pyrifolia cultivar are known. Suppression of the alternate host (J. chinensis) within a certain radius of orchards is recommended, but may be difficult as it is often present in private gardens. Several research projects revealed that mycoparasites, such as Tuberculina sp., can occur on or nearby the aecia by the sporodochia and can eliminate the aeciospores before the dispersion to Juniper species (Huang, 1993).
Gymnosporangium asiaticum is one of the non-European Gymnosporangium spp. included in the EPPO A2 List (EPPO, 2022). At present, G. asiaticum is absent from most of the EPPO region (only recorded in the Russian Far East) and has occasionally been intercepted in trade on bonsai plants from Asia. It is highly probably that it could establish in Europe since its alternate host J. chinensis does occur. In addition, G. asiaticum seems to be a more damaging species on its main host P. pyrifolia in the Far East, than G. sabinae is on P. communis in the EPPO region. However, several factors are probably limiting the risk: 1) P. communis, though recorded as a host, does not appear to suffer significant damage; 2) the main host, P. pyrifolia, is a minor crop in the EPPO region; 3) G. sabinae is easily controlled and these control measures applied in pear orchards would probably be effective against G. asiaticum; and 4) the need for specific Juniperus spp. (grown only as ornamentals in Europe) to complete the life cycle could in practice severely limit the area of establishment.
PHYTOSANITARY MEASURES 2022-09-07
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 may prohibit importation of plants for planting and cut branches of Juniperus from the Far East. If plants for planting of J. chinensis (or other Juniperus spp.) are imported from the Far East, the consignment should be kept in quarantine over the growing season and found free from Gymnosporangium spp. Plants for planting and cut branches of Juniperus from the Far East should come from a field (and its immediate vicinity) found free from diseases caused by Gymnosporangium species during the last two growing seasons. Particular attention should also be paid to imports of juniper bonsais from Asia, and these plants should have been produced under conditions ensuring their freedom from G. asiaticum. Fruits, seedlings, and cut branches of Malus and Pyrus species from the Far East, especially from China, Japan and South Korea, should be inspected to avoid the introduction of G. asiaticum to European regions, where Asian pears, Asian apples and Juniperus species have been promoted for commercial production and ornamental purposes.
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This datasheet was extensively revised in 2022 by Dr. Peng Zhao and Dr. Lei Cai from the State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences. Their valuable contribution is gratefully acknowledged.
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Datasheet history 2022-09-07
This datasheet was first published in the EPPO Bulletin in 1983 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2022. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.
CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).
EPPO (1983) Data sheets on quarantine organisms No. 13, Gymnosporangium spp. (non-European). EPPO Bulletin 13(1), 6 pp. https://doi.org/10.1111/j.1365-2338.1983.tb01713.x