BIOLOGY

The smut fungi are host-specific parasites that are almost exclusively found on flowering plants. Exceptions are species of Melaniella on Selaginella (Lycopodiophyta, Selaginellaceae; Bauer et al., 1999b) and Exoteliospora osmundae (Peck) R.Bauer, Oberw. & Vánky on Osmunda (Polypodiophyta, Osmundaceae; Bauer et al., 1999a). The conspicuous stage of the smut fungus is the sorus, which is often confined to the ovary or inflorescence, but may also be found in the anthers, fruits, leaves and roots. Sori are filled with spores that often become exposed as a dark powder (hence ‘smut’). The spores may be loose or aggregated into spore balls that can either readily separate or persist. Other useful morphological characters are the presence or absence of sterile cells between the spores or in the spore balls, the occurrence of one or more columellae in the sori, the structure of spore balls and the ornamentation of the spore surface and its profile when viewed under light microscopy.

At maturity, diploid spores (teliospores, ustilospores) undergo meiosis to form a basidium (promycelium) that produces four or more haploid basidiospores (sporidia). The basidiospores are capable of saprobic, yeast-like reproduction and/or haploid mycelial growth. Although the haploid mycelium can infect host tissues directly, it cannot invade tissues extensively, nor does it cause typical symptoms. Conjugation usually occurs between germinating basidiospores (often as compatible mycelia in the host) and/or with basidial cells or even between basidia to produce a dikaryotic mycelium. This mycelium invades host tissue producing the typical symptoms of smut infection and, following karyogamy, again produces the spores. However, there are many variations to this generalised life history.

Genetically distinct mating groups (races) of smut fungi are known. However, these races are not as stable as those of rusts, as each generation on the host plant involves meiosis which results in the frequent appearance of new races (Agrios, 2005).

Some smut fungi, for example Doassansia and Doassansiopsis, have evolved adaptations that enable them to survive in aquatic habitats. These fungi produce spore balls within the tissues of aquatic and paludal plants in temperate and tropical regions. At temperate latitudes, during autumn or early winter, senescent leaves and stems of infected host plants sink to the bottom of lakes and marshes where they remain over winter. With the onset of higher water temperatures in spring the host tissues decompose and spore balls are liberated. The spore balls are often comparatively large and buoyant due to their structure which incorporates empty sterile cells. The spores germinate on the surface, often producing sigmoid basidiospores as the new generation of host plants begins to grow. This facilitates the re-infection of host plants, thereby completing the life history of the smut fungus. In tropical climates some aquatic fungi exhibit a life history  that is adapted to wet and dry seasons. During the latter spore balls survive desiccation in the remains of host tissue.

Three principal types of infection by smut fungi were documented by Kirk et al. (2004): 1) seedling infection from spores on the seed; 2) seedling infection by mycelium in the seed as a result of spore germination on the stigma at flowering; and 3) infection by wind-borne basidiospores from promycelia among decaying plant material. In the absence of their hosts, smut fungi can survive as spores on contaminated seed, in plant debris or in the soil. It is likely that short-distance dispersal occurs by wind-borne basidiosores and water-dispersed spores. Long-distance dispersal is likely to be facilitared by wind-borne spores that are better able to survive desiccation and potentially demaging ultraviolet irradiation. However, with the exception of the cereal smut fungi, very little is known about the disease cycle, infection processes and epidemiology of most smut fungi.

Control of cereal smut fungi has involved the use of resistant varieties and seed treatment. Seed treatments have included chemical dusting and dipping if spores are present on the seed surface or in the soil; and hot water treatment if the fungus is present as a mycelium within the seed. The spraying and dusting of plants with chemicals is a possible control for wind-borne infection by basidiopsores.

Most cereal smut fungi were been introduced into Australia prior to 1915 (Shivas & Vánky, 2003), and many were responsible for devastating crop losses in the late nineteenth and early twentieth centuries (McAlpine, 1910). Their importance for Australian agriculture has been reduced markedly since the introduction of effective fungicidal seed treatments and the development of disease resistant varieties. However, some smut fungi remain serious pathogens of cereal crops elsewhere in the world, including Tilletia contraversa J.G.Kühn (dwarf bunt of winter wheat), T. indica Mitra (Karnal bunt of wheat) and Sporisorium cruentum (J.G.Kühn) Vánky (loose smut of sorghum).

The seriousness of the threat that Karnal bunt presents to Australia was highlighted in 2004 when a shipment of Australian wheat was rejected by an importing country because it allegedly contained spores of Tilletia indica. The issue was resolved when Pascoe et al. (2005b) demonstrated that spores of T. ehrhartae and T. walkeri were common contaminants of Australian wheat grain and a potential source of confusion with T. indica. Nevertheless, these events highlighted the importance of accurate identification and the need for a reliable understanding of the taxonomy of the entire group, including endemic and established species. It has been our goal to achieve this level of reliability for the Australian smut fungi.