This Post Contains Smut

And here's some of that smut, right in your face:

Specimens of the grass Briza minor infected with the smut Jamesdicksonia brizae, from Roger Shivas.

Smuts are a form of plant-parasite fungus that produce large numbers of dusty spores from sori that rupture from the host-plant tissue. The majority of smuts belong to the basidiomycetes clade Ustilaginomycotina (making them distant relatives of the familiar mushroom). The focus of today's post will be the smut order Georgefischeriales, the vast majority of which are parasites of the vegetative tissue of grasses (Bauer et al. 2001). The exceptions include species of the genus Georgefischeria that parasitise species of the plant family Convolvulaceae (the morning-glories) and a small number of species that parasitise sedges. The species Gjaerumia ossifragi parasitises the bog-asphodel Narthecium ossifragum (Bauer et al. 2005). Members of the Georgefischeriales are distinguished from other smuts in that the septa dividing cells within mature sori lack pores. Members of one georgefischerialean family, the Gjaerumiaceae, have septal pores in young hyphae, but by the time they reach maturity the pores have closed over (Bauer et al. 2005). Like other smuts, Georgefischeriales have a life-cycle that alternates between a parasitic and a non-parasitic, saprobic stage, as summarised in this diagram from Bauer et al. (2001):

If a number of the terms on that diagram don't mean much to you: don't worry, you are not alone. The first thing to understand is that, compared to us, fungi kind of do sexual reproduction in reverse. For most of our life-cycle, we are diploid, with two complementary sets of chromosomes in each cell. When we produce sex cells (eggs and sperm), the number of chromosome sets in the cell is reduced to one, making the cell haploid, so that when egg and sperm fuse the resulting offspring is back to being diploid. Fungi resemble us in having two haploid cells fuse into a diploid offspring, but differ in that they then separate the chromosome sets again to produce separate haploid cells. Fungi are therefore haploid rather than diploid for most of their life-cycle. In the diagram above, it is the non-parasitic stage that is the haploid stage.

The parasitic stage of a smut's life-cycle comes about through the fusion of two haploid non-parasitic cells. However, even though the cells fuse, the nuclei in those cells don't. Instead, they form what is called a dikaryon, a chimaeric organism in which each cell contains two separate genomes in separate nuclei. Many fungi have lifestyles featuring dikarya: mushrooms, for instance, are also dikaryotic. The separate nuclei don't actually fuse until they form the reproductive structures, the basidia. In smuts, these basidia become thick-walled and separate from the parent sorus to produce the dispersal structures, the teliospores. The haploid basidiospores that come from the teliospores are what grow into the next non-parasitic generation.

Sori of Gjaerumia ossifragi on Narthecium, from here.

In three of the four families of Georgefischeriales (Georgefischeriaceae, Tilletiariaceae and Gjaerumiaceae), the saprobic stage of the life cycle grows into filamentous hyphae, but the fourth family, the Eballistraceae (containing the single genus Eballistra), produces a budding yeast as its non-parasitic stage instead. Eballistra also differs from other Georgefischeriales in that it does not produce ballistic spores that are flung from the parent sorus, relying instead on more passive dispersal. Eballistra does resemble Georgefischeriaceae and Gjaerumia in producing holobasidia, basidia that are not subdivided by septa. The Tilletariaceae are distinct in that they produce internally-divided phragmobasidia. Tilletiariaceae include three genera: Tilletiaria have spiny spores while those of Phragmotaenium and Tolysporella are smooth. It is worth noting that Tilletiaria is currently known only from laboratory culture and has not been identified in the wild, but it is expected to be a grass parasite like other Tilletiariaceae. Tolysporella produces teliospores that are clustered into spore-balls; those of Phragmotaenium are released individually. In the Georgefischeriaceae, two genera are distinguished by host range and appearance: Georgefischeria produces light-coloured sori on Convolvulaceae while Jamesdicksonia produces dark sori on grasses.

REFERENCES

Bauer, R., D. Begerow, F. Oberwinkler, M. Piepenbring & M. L. Berbee. 2001. Ustilaginomycetes. In: McLaughlin, D. J., E. G. McLaughlin & P. A. Lemke (eds) The Mycota vol. 7. Systematics and Evolution, part B, pp. 57-83. Springer-Verlag: Berlin.

Bauer, R., M. Lutz & F. Oberwinkler. 2005. Gjaerumia, a new genus in the Georgefischeriales (Ustilaginomycetes). Mycological Research 109 (11): 1250-1258.