Introduction to Fungi, Third Edition

THE ‘TRUE’ SMUT FUNGI (USTILAGINOMYCETES)
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spores are produced in infected plant organs.
Leaves, stems, flowers and seeds of grasses and
other herbaceous plants are particularly frequently
attacked. The term ‘bunt’ is sometimes
used for smut fungi infecting the ovaries of their
hosts, the seed becoming filled with teliospores
in place of the embryo. Host tissues from which
the spores are released often appear as if burnt
or scorched, and this is why de Bary (1853)
used the term ‘Brandpilze’ to describe the smut
fungi. Various names have been given to these
spores, e.g. teliospore, chlamydospore, brand
spore, melanospore, ustospore or ustilospore.
We prefer to call them teliospores because their
function in the life cycle of smut fungi is
equivalent to that of teliospores in the rust life
cycle, i.e. they are the site of nuclear fusion and,
on germination, give rise to the promycelium in
which meiosis occurs.
Several good monographs have been written
about smut fungi, especially by Vánky (1987,
1994). The surface ornamentation of teliospores
(Figs. 23.2, 23.9) and their method of germination
(Figs. 23.3, 23.4, 23.5, 23.10, 23.12) as well as the
type of symptoms and host range are important
characters in identification.
23.2.1 The life cycle of smut fungi
The life cycle of smut fungi can be divided into
two phases, a yeast-like monokaryotic (homokaryotic)
form which grows saprotrophically but
is unable to infect plants, and a predominantly
dikaryotic (heterokaryotic) mycelial phase which
is infectious on host plants but cannot grow
saprotrophically (Fig. 23.1). The infectious dikaryotic
mycelium is often systemic, showing interor
intra-cellular growth. Meristematic host
tissues are particularly densely colonized.
Usually there are no specialized haustoria, but
hyphae may enter or even grow through host
cells, invaginating the host plasmalemma.
Intracellular hyphae are surrounded by a partial
or complete sheath (Fig. 23.6) which is formed
partly by the secretory activity of the pathogen
and partly by the contributions from the infected
host cell (Bauer et al., 1997). During sorus
development, the dikaryotic hyphae proliferate
and mass together in intercellular spaces, often
destroying the softer internal host tissues but
remaining enclosed by the host epidermis. There
are no phialides or other specialized sporeproducing
structures, but most hyphal segments
can become converted to spores. The sporogenous
hyphae are composed of binucleate cells.
After nuclear fusion, the walls thicken and
gelatinize, and the cells fragment. They then
enlarge and become globose, and finally a thick
wall is laid down (Snetselaar & Mims, 1994;
Banuett & Herskowitz, 1996). The gelatinous
matrix disappears at maturity. The ripe, uninucleate,
diploid teliospores have thick, usually
dark walls which may be smooth or ornamented
by spines or reticulations (Vánky, 1987, 1994;
Piepenbring et al., 1998a,b). In some genera, e.g.
Urocystis, a central fertile cell is surrounded by a
group of sterile cells.
The teliospores are commonly dispersed by
wind or become attached to the surface of seeds.
Teliospores of many smut fungi germinate in a
similar way to those of rust fungi by forming a
septate promycelium. The teliospore is therefore
the probasidium, with the promycelium being
the metabasidium. If this is septate, it is a
phragmobasidium. Teliospore germination can
proceed in several different ways which are
shown in subsequent sections. Typically, numerous
haploid basidiospores (often called sporidia)
are produced by direct budding from segments
of the promycelium, and these are unable to
re-infect the host. Instead, they germinate by
further budding to form elongated yeast cells
which are capable of prolonged saprotrophic
growth. Compatible yeast cells meeting on the
surface of the host plant conjugate, and this
initiates the dikaryotic hyphal stage which is
able to infect the host plant.
23.2.2 Mating systems
Many smut fungi are heterothallic with a unifactorial
(bipolar) mating system (i.e. one mating
type locus with two alleles), but Ustilago maydis
and a few other species are tetrapolar, with two
mating type loci located on different chromosomes.
The a locus has two idiomorphs and
controls fusion of sporidia which is driven by
the exchange of mating pheromones between