Introduction to Fungi, Third Edition

652 USTILAGINOMYCETES: SMUT FUNGI AND THEIR ALLIES
mildews (p. 408). Avirulence genes involved in
gene-for-gene interactions have been desribed
for several cereal smuts (Sidhu & Person, 1972;
Eckstein et al., 2002; Hu et al., 2003). The
hypersensitive response in incompatible interactions
is often microscopically small (Hu et al.,
2003). Field resistance against smut fungi may
also occur as a combination of several genes
(Nelson et al., 1998). An interesting case of singlegene
resistance has been reported by Wilson
and Hanna (1998) as trichome-less mutants of
pearl millet (Pennisetum glaucum) showing a 50%
reduction in disease severity caused by the
smut Moesziomyces penicillariae. Curiously little is
known about resistance mechanisms in Ustilago
maydis despite its status as a well-examined
‘model organism’ and the availability of its
genome sequence.
23.3 Microbotryales
(Urediniomycetes)
The order Microbotryales contains smut fungi
with features almost indistinguishable from
those described in the preceding section. This
includes their general life cycle of teliospores
germinating by means of a promycelium which
produces haploid yeast-like sporidia, and the
infection of host plants following establishment
of a dikaryotic infection hypha. Intriguingly,
however, phylogenetic studies have clearly
shown the Microbotryales to belong to the
Urediniomycetes (Blanz & Gottschalk, 1984;
Begerow et al., 1997; Swann et al., 1999). There
are certain microscopic details which distinguish
them from Ustilaginomycetes, notably that
growth by Microbotryum and allied species
in planta is exclusively intercellular (Bauer et al.,
1997) and that the teliospores have a violetpurplish
rather than brown pigmentation.
The most important genus in the Microbotryales
is Microbotryum which currently
contains about 75 species (Vánky, 1998, 1999).
All of them parasitize dicotyledonous hosts, and
they can be resolved by DNA sequence analysis
into two groups (Almaraz et al., 2002). The original
genus Microbotryum parasitizes the anthers of
plants belonging to the Caryophyllaceae, whereas
species of the second group cause smuts on
various organs of other host plants. Until
recently, members of the second group were
considered to belong to Ustilago. The eventful
taxonomic history of these ‘dicot Ustilago’ spp. has
been recounted by Vánky (1998, 1999); based on
the findings of Almaraz et al. (2002) they will
probably have to be given a new generic name,
adding at least one further twist to the story.
Good descriptions of many ‘dicot Ustilago’ spp.
have been given by Vánky (1994, 1998). We shall
devote our attention to Microbotryum sensu stricto,
cause of anther smut on Caryophyllaceae.
23.3.1 Microbotryum violaceum
Anther smut of Caryophyllaceae has long
fascinated biologists with a wide range of
research interests. Although infection is systemic
throughout the host plant, the disease symptoms
are confined to the anthers in which pollen is
replaced by purple teliospores. Several members
of the Caryophyllaceae are infected, and there is
evidence that Microbotryum violaceum (formerly
called Ustilago violacea), the causal fungus, is
undergoing speciation in diverse host plants
(Antonovics et al., 2002), so that species delimitation
is difficult at present (see Vánky, 1994). In
dioecious hosts such as red or white campion
(Silene dioica and S. alba), the flowers of infected
female plants are stimulated to produce anthers,
i.e. their morphology changes from female to
male. A thorough review of the general biology
of M. violaceum has been written by Day and
Garber (1988).
Life cycle and genetic recombination
The diploid teliospores of M. violaceum are
transported from diseased to healthy flowers
by pollinating insects. They germinate by forming
a promycelium (Fig. 23.14) which often
separates into an exterior three-celled section
and a one-celled fragment remaining in the
teliospore. Each promycelium segment produces
sporidia. The three-celled segment becomes
readily detached from the teliospore and may
continue to develop sporidia after separation.