Gymnosporangium yamadae Miyabe ex G. Yamada 1904

Gymnosporangium yamadae

A. Taxonomy and Phylogeny

Gymnosporangium yamadae Miyabe ex Yamada was first collected June 23, 1904 on Pyrus spectabilis, the Chinese apple tree, in Toyko, Japan by Dr. G. Yamada of Japan (Fukushi 1926).

The common name of the disease is Japanese apple rust, whose fungal pathogen belongs in the Phylum Basidiomycota, Class Pucciniomycetes, Order Pucciniales, and Family Pucciniaceae, with its closest relatives in the same genus Gymnosporangium, as other various apple rusts (“G. yamadae”, 2013). All are heteroecious plant pathogens. The rDNA large subunit (LSU) sequence collected from fungus telial galls (GenBank Accession No. GU058012) on host plants were used for molecular phylogenetic Gymnosporangium studies and morphometric data sequencing (Yun, Soon et. al. 2009).

B. Morphology

This rust fungus has a heteroecious, pathogenic lifestyle on two hosts: Juniper trees, Juniperus spp. (and Sabina spp. according to various literature), and rosaceous hosts, specifically apple trees, of the subfamily Maloideae and genus Malus (Kern 1911). G. yamadae has four different spore types or stages, and includes the fruiting structures of spermagonia, aecia, and telia, but lacks uredinia and urediniospores (“Data sheets on quarantine pests”, n.d.). Two characteristic identifiers of this species include the “teleuto” or telial and aecial stages (Hiratsuka 1936). Telia produce and grow on the stems of Juniperus, caulicolous, rarely foliicolous, creating globoid swellings or small galls. Telial horns are cylindric-acuminate, 1-3 mm in diameter, 5-8 mm in length, orange, and gelatinous (“G. yamadae” Invasive Species Compendium 2013). Teliospores are two-celled, oblong, ellipsoid or obovoid, 15-28 by 32-56 µm, with walls 0.8-2.0 µm thick. They are usually yellow or orange in color, with two pores near septum and one pore toward apex in upper cell, commonly with an obtuse, hyaline papilla located there (Yun, Soon et. al. 2009). Following germination of basidiospores from telia, wind disperses progeny and can infect other nearby apple trees, up to distances of 2.5-5 km. It is frequently mistaken for Gymnosporangium juniper-virginianae, or cedar-apple rust; however, G. yamadae have much thinner, longer and jettisoned aecia on apple leaves, as opposed to G. juniperi-virginianae that has much flatter aecia against the apple leaf. Infected apple trees then generate G. yamadae pycnia—aecia—born in groups on the adaxial leaf surface of branches. Aecia grow on Malus, are hypophyllous, and also less commonly caulicolous, and fructicolous (Yun 2010). They initially develop a whitish leaf spot that becomes rose red with a distinct margin. Aeciospores are globoid, 16-26 by 18-27 µm, with walls a dark yellow, 1.0-2.5 µm thick, rarely up to 3.5 µm thick, sparsely echinulate, and have 4-7 pores scattered on surface. Peridium develop cornute to tubular, 3-8 mm high, retaining this shape at maturity but with lacerate sides that often form a reticulate pattern (Laundon 1977). Their apex typically is closed to occasionally dehiscent, yellow-brown to brown. Structural peridial cells are long-narrow rhomboid, 59-115 µm long, pale yellow, appearing verrucose with long papillae to tuberculate, outer walls smooth, surrounded by sparsely echinulate inner and side walls (Yun, Soon et. al. 2009).

Following dikaryotization of spermatia and the “sexual” stage of the lifecycle, aeciospores produce from the pycnia and aecia on the abaxial surface of apple leaves, which release spores capable of wind dispersal and infection to alternate hosts of Juniperus spp. and Sabina spp. Once germinated on either of these two alternate hosts, an overwintering mycelium hyphal mass grows (Yun 2010). Then, teliospores of G. yamadae emerge on Juniperus spp. and Sabina spp. and infect apple trees in the spring, commencing the rust’s life cycle once again. Although its pathogenic lifestyle has been widely described, the fungus cannot be grown in culture and has not been genetically sequenced in its entirety.

C. Ecology

This fungal species is obligate, perennial, and plant pathogenic, acquiring its energy from the juniper and apple tree hosts it colonizes. Temperature range for basidiospore germination of G. yamadae is 7-30⁰C with an optimum temperature of 16-20⁰C (Yun, Soon et. al. 2009). Apple hosts succumb most easily to infection by Gymnosporagnium spp. from the period of early bloom to until about 30 days after blooming (Ellis 2008). Life cycles can last up to two years without disturbance. It produces the disease Japanese apple rust and primarily colonizes host leaves and stems. This leads to damage by defoliation and rapid loss of photosynthesis and subsequent fruit production. When apple trees succumb to fungal infection and disease, fruit can drop, reducing apple yield and quality (“Gymnosporangium rusts: commonly called juniper rust” 2011). Geographic distribution is in Japan, China, and Korea, and recently the state of Delaware in the United States (Gregory 2009). Abundance and spread of Japanese apple rust potentially originated from the general practice of utilizing juniper trees as ornamental trees in various gardens (Fukushi 1926). Although G. yamadae can tolerate a wide range of climates, it has a restricted host range and high host specificity, to only Juniperus spp. (Sabina spp.) and Malus spp., allowing possible elimination of fungal spore dispersal if an area can properly remove host plants. It has a considerably minor significance to other aspects of the environment; however, it would be detrimental to uncontaminated ornamental Juniperus spp (“G. yamadae” 2013). Common and described symptoms of the disease include fungal growth of the pathogen on leaves, premature/abnormal leaf drop, unusual leaf forms and colors, wilting, and even the presence of honeydew or sooty mold (“G. yamadae”Plantwise 2013). Stems also exhibit galls and/or cankers on woody stems.

G. yamadae is quite abundant and invasive in its native range, as well as proven invasive beyond its native range (“G. yamadae” 2013).

D. Overall Biology and Relevance for Humans

It is a very destructive plant disease, causing economic harm to the apple industries and pome fruit producers of Asian markets. As an important pest in northern Japan, it causes defoliation of the plant, and weakens photosynthetic production of sugars and metabolic energy. G. yamadae can also increase respiration rate, thus delaying fruit harvests (Yun, Soon, et. al. 2009). High risk scenarios exist for humans to consume this fungal pathogen without knowledge, originating from the harvesting, packaging, and exporting of symptomless infected fruit. There are no reported human symptoms of the disease, but ingesting infected fruit is not advised. G. yamadae production of apple rust in China is common and can be widely distributed across major apple production areas around the world (“Biosecurity Australia” 2009). Although fruit with obvious visual symptoms of the Japanese apple rust disease incur rejection during harvesting and routine grading for packaging operations, it is typical for symptomless infected fruit and apple fruit with small lesions to avoid detection during such processes (“Biosecurity Australia” 2009). This causes unseen contamination that is potentially harmful to commodity consumers of such fruit. Such a wide distribution of this fungus in China and Japan, accentuated by the risk of symptomless and infected fruit avoiding detection during production screening, threatens markets and classifies as a “moderate” risk rating for importation of apple shipments to countries and global clientele (“Biosecurity Australia” 2009).

Field detection has also been proven difficult and costly to control. Conversely, in Japan, a new triazole fungicide was discovered to be successful in targeting G. sporangium proliferation. Mepronil can also be used to control—to a limited extent—disease on Juniperus spp. (“G. yamadae” Plantwise 2013). Managing this disease can inundate owners of infected crops, requiring extensive pathological prevention on two unrelated hosts (“Under the Scope” 2013). It was discovered, though, that approximately eight apple cultivars, including Fuji apples, a favorite cultivar in Asian countries, had a moderately high 35.5% infection rate of G. yamadae (“G. yamadae” Invasive Species Compendium 2013). In contrast, after inoculation trials, most economically important apple cultivars have been determined resistant to Gymnosporangium species, like G. yamadae (“G. yamadae” Plantwise 2013). In order to accurately determine the how successful G. yamadae rust infection was to different apple varieties, multiple inoculation experiments were implemented during the growing seasons of 1918, 1919, and 1920 (Fukushi 1926). From these experiments, Mr. Shima of the Aomori Agr. Exp. Station in Japan discovered resistance of the apple cultivars Red McIntosh and Fameuse to rust infection in that locality; however, if rust spot do produce, they are of usual lesion size on the Malus leaves (Fukushi 1926).

The Japanese apple rust disease was first confirmed in the Eastern United States in 2009 after specimens submitted to the National Mycologist revealed widespread prevalence in the Northeast, including the states of Maryland, Maine, New Hampshire, New Jersey, New York, Pennsylvania, and Rhode Island (Gregory, 2009). Also observed colonizing the leaves of toringo crab apple, Malus toringo in Wilmington, Delaware and near in Media, Pennsylvania, the aecial identifiable stage of G. yamadae was later confirmed genetically by morphological and molecular characteristics (Yun, Minnis et. al. 2009). The range of incidence without previous detection suggests possible confounding of symptoms with the more notorious cedar-apple rust disease. The USDA/APHIS continues to collaborate with states to determine a more accurate distribution and impact of G. yamadae. Constantly preventing the success of any chemical treatment, rust infection of Juniperus hosts is systemic in stems and evergreen leaves (“G. yamadae” Plantwise 2013). American regions with possible infection sightings have been recommended to grow resistant Juniperus and Malus species, as well as to destroy infected wild and ornamental junipers.

With its given proximity to the origin of Japanese apple rust, the country of Australia has also organized strict control of trade with Asian apple markets (“Biosecurity Australia”, 2009). Protection against the probability of entry, establishment, spread of the disease, and thorough inspection of fruit imports steer a majority of their phytosanitary measures.

Gymnosporangium yamadae is a plant pathogen that causes Japanese apple rust.

Gymnosporangium yamadae je grzib, co go ôpisoł Miyabe ex G. Yamada 1904. Gymnosporangium yamadae nŏleży do zorty Gymnosporangium i familije Pucciniaceae. Żŏdne podgatōnki niy sōm wymianowane we Catalogue of Life.