Gymnosporangium yamadae
(Japanese apple rust)

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.

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.

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

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).

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).

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).

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.

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.

02/05/08 Updated by: